Sexual selection and biological diversification: Patterns and processes

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SEXUAL SELECTION AND BIOLOGICAL DIVERSIFICATION:

PATTERNS AND PROCESSES

by

Sarah Lynne Mesnick

A Dissertation Submitted to the Faculty of the

DEPARTMENT OF ECOLOGY & EVOLUTIONARY BIOLOGY

In Partial Fulfillment of the Requirements For the Degree of

DOCTOR OF PHILOSOPHY

In the Graduate College

THE UNIVERSITY OF ARIZONA

1996 UMI Ntjjnber: 9720o29

UMI Microform 9720629 Copyright 1997, by UMI Company. All rights reserved.

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THE UNIVERSITY OF ARIZONA (S GRADUATE COLLEGE

As members of the Final Examination Committee, we certify that we have

read the dissertation prepared by Sarah L. Mesnick

entitled Sexual Selection § Biological Diversification: Patterns §

Processes

and recommend that it be accepted as fulfilling the dissertation

requirement for the Degree of Doctor of Philosophy

Donald Thomson Date 15 iff/: Wayne Maddi^n Date

Rdbert'^-if/ Smith Date

\S\to.: /99g Judith Bronstein Date

Final approval and acceptance of this dissertation is contingent upon the candidate's submission of the final copy of the dissertation to the Graduate College.

I hereby certify that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement.

ii^w Dissertation Director Date STATEMENT BY AUTHOR

This dissertation has been submitted in partial fulfillment of requirements for an advanced degree at the University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library.

Brief quotations from this dissertation are allowable without special permission, provided that accurate acknowledgment of source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her judgment the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author.

SIGNED:

/ 4

ACKNOWLEDGEMENTS

This dissertation was built upon a foundation of help, friendship and support that I received from ray committee, ray friends, my colleagues, and my family. My deep gratitude to all, for not only making this effort possible, but for making it a rich and enduring experience as well. My committee has been supportive and inspiring, each in his or her own way. The wisdom and vision of Donald A. Thomson, major advisor and friend, first saw the possibility of the importance of studying sexual dimorphism and species diversity and encouraged me to pursue it. 1 thank him, most of all, for encouraging me to follow my heart and to create my own path. Phil Hastings was generous with his knowledge of chaenopsids and his insights into social behavior, beyond my capacity to thank him. Judie Bronstein has been an inspiration in terms of her own pursuit of a career in science. Wayne Maddison provided stimulating discussion on social behavior and seemingly inexhaustable enthusiasm for this project. I thank Bob Smith for his encouragement to pursue my ideas on the evolution of human behavior and his faith in rae throughout this project. Special people, both friends and invaluable colleges, include Katrina Mangin, Luis Bourilldn Moreno, Marisol Tordesillas Barnard, Ellinor Michel, Dave Gori, Andy Cohen, Scott Wilson, Eric Dyreson, Liz Waters, Ed Boyer, Judy Stahl, Jody Sherman, Kurt Thomson, Scott Wilson, and Laurent Kanzler. These wonderful people provided excellent scientific guidance, spirited discussions, and demonstrated countless times what true friends are. For support during the final phases of this dissertation, I thank Brent Burt, Shelley McMahan, and Susan Crowell. And to the many others, for their help along the way. My deep gratitude to Shawn McLaughlin for his attention to detail and for preparation of the final manuscript, and moreover, for his patience and friendship. In the field, many thanks to Keith Meldahl who provided companionship and adventures during many months in Baja California, and to Tad Pfister, Andy Cohen, Debbie Gevirtzman, and Melonie Stinger for their support during dive trips. In the lab, I thank Susan Crowell and Theresa Friend for caring and recording blenny data. I thank Sonja Peterson for her tenacity in cracking the blenny genetic code. To my family, who have always been ready with their love, encouragement, and emotional and financial support. To my father, for being wise and caring, and for showing me the value of a challenging and flexible career. To my mother, for the example she sets in strength and in love, and for editing, literally every word, of this dissertation. To my sister Miriam, for her absolute love and her tenacity, which are standards I try to live up to. To my niece for her natural curiosity and enthusiasm for life. To my wonderful dogs Kiska and Scooby. To my Tucson cousins, the Kivel family, who shared their home and holiday celebrations with me. I thank the government of Mexico for granting rae perraission to conduct research in the Gulf of California. Considerable financial support came from the Research Training Grant in Biological Diversification in the Department of Ecology & Evolutionary Biology, the Graduate College, and the Department of Ecology & Evolutionary Biology at the University of Arizona, and the Lemer Gray Fund for Marine Research. 5

DEDICATION

This dissertation is dedicated to

my family,

whose love and support

have truly given me roots and wings;

DAT,

mentor and friend, who has always encouraged me to follow my heart;

and to the islands of the Gulf of California,

and the promise to help keep them wild. 6

TABLE OF CONTENTS

LISTOFHGURES 10

UST OF TABLES 11

ABSTRACT 12

INTRODUCTION 14

CHAPTER I - SEXUAL SELECTION, COURTSHIP DISPLAYS, AND SPECIES DIVERSITY IN TELEOST HSHES: DOES SEXUAL DIMORPHISM PROMOTE DIVERSIHCATION? 17

INTRODUCTION 17

COMPARATIVE ANALYSES 19

METHODS 20

THE DATA SET 21 IDENTIHCATION OF SEXUALLY DIMORPHIC TAXA 22 SISTER-TAXA COMPARISONS 24 DIVERSITY ESTIMATES 27 STATISTICAL ANALYSES 27

RESULTS 28

DESCRIPTIVE PATTERN 28 SISTER-TAXA COMPARISONS 29

DISCUSSION 31

POTENTIAL BL\SES IN THE DATA 34 EVOLUTIONARY IMPUCATIONS 36 OTHER TAXA 39 PRIORITIES FOR FUTURE RESEARCH 44

CONCLUSIONS 45

SUMMARY 46

HGURES 48

TABLES 51 7

TABLE OF CONTENTS - Continued

CHAPTER N - GEOGRAPHIC VARLVTION IN COLOR IN THE BROWNCHEEK BLENNY, ACANTHEMBLEMARIA CROCKERI (TELEOSTEI; CHAENOPSIDAE): CAN THE DIVERGENCE OF SIGNALS USED IN SEXUAL INTERACTIONS PROMOTE REPRODUCTIVE ISOLATION? 64

INTRODUCTION 64

METHODS 66

STUDY SPECIES 66 GEOGRAPHIC VARIATION 67 MALE COURTSHIP DISCRIMINATION EXPERIMENTS 69

Intrapopulation Field Experiment 70 Interpopulation Field Experiment 71 Interpopulation Laboratory Experiment 71

FEMALE SPAWNING EXPERIMENTS 72

General Laboratory Conditions 72 Single Female - Single Male Experiment 73 Choice Experiment 73

RESULTS 74

GEOGRAPHIC VARIATION 74 COLOR 77 MALE CouRTSfflp DISCRIMINATION EXPERIMENTS 79

Intrapopulation Field Experiment 79 Interpopulation Field Experiment 80 Interpopulation Laboratory Experiment 80

FEMALE SPAWNING EXPERIMENTS 81

Single Female - Single Male Experiment 81 Choice Experiment 82 Individual Spawning Histories 82

DISCUSSION 83 8

TABLE OF CONTENTS - Continued

SUMMARY 88

NOURES 90

TABLES 110

CHAPTER M — SEXUAL COERCION AND SEXUAL ALLIANCES: IMPLICATIONS FOR THE EVOLUTION OF ANIMAL M\TING SYSTEMS 122

INTRODUCTION 122

FEMALE INTERESTS DURING MATING 124

ASYMMETRICAL INTERESTS DURING REPRODUCTION 124 BEYOND DARWIN: SEXUAL COERCION AND RESOURCE BROKERING 125 TERMINOLOGY 126

Forced Copulation 126 Harassment 127 Resistance 127

COSTS OF SEXUAL COERCION FOR FEMALES 128 FEMALE COUNTERSTRATEGIES TO SEXUAL COERQON 131

Avoidance/Resistance 131 Behavioral/Physiological 131 Morphological 132 Female Coalitions 132 Alliances with Male Non-mates or "Friends" 132 Convenience Polyandry 133 Copulation Solicitation 133 Sexual Alliances 133

THE BODYGUARD HYPOTHESIS 134

BASIC TENETS 134 COSTS AND BENEFITS OF PROTECTION 136 ASSUMPTIONS AND PREDICTIONS 139 CRITICAL TESTS OF THE HYPOTHESIS 141 9

TABLE OF CONTENTS - Continued

IMPLICATIONS FOR THE EVOLUTION OF ANIMAL MATING SYSTEMS ... 144

EXAMPLES 144

Ungulate Leks 144 Mate-guarding in Birds 146 Female Gregariousness and Breeding Synchrony in Pinnipeds 148 Dominance and Territoriality in Horses 150 Post-insemination Guarding in Insects 150 Sociality in Non-human Primates and Lions 152

CASE STUDY: THE DEPARTURE OF FEMALE ELEPHANT SEALS FROM THE ANO NUEVO ROOKERY AND THEIR MALE ESCORTS 155

PAIR-BONDING IN HUMANS 159

Cultural and Biological Influences on Human Behavior 159 Pair-bonding 160

CONCLUSIONS 169

SUMMARY 171

TABLES 172

APPENDIX A - SEXUAL DIMORPHISM, SPECIES DIVERSITY, HABITAT, AND EGG TYPE OF FAMILIES OF TELEOST FISHES 175

APPENDIX B - SUMMARY OF MULTIPLE SISTER-TAXA COMPARISONS 204

APPENDIX C - CHARACTERS, AND CHARACTER STATES 242

APPENDIX D - COLOR AND PATTERN STATES 249

APPENDDC E - FEMALE AGGRESSION TOWARD MALES DURING MATING . . 253

REFERENCES 255 10

LIST OF FIGURES

CHAPTER I

FIGURE 1. The sister-taxa comparison method 48 RGURE 2. Distribution of sexually selected traits 50

CHAPTERn

FIGURE 1. Study sites 90 FIGURE 2. Body regions scored for color and pattern 91 FIGURE 3. Laboratory aquaria set-up 92 FIGURE 4. The total number of different color states in males and females 93 FIGURE 5. Mean number of dorsal fin iridescent spots 94 FIGURE 6. Mean color score for dorsal fm pigmented area 95 FIGURE 7. Mean color score for pectoral-fin base 96 HGURE 8. Mean color score for body midline 97 FIGURE 9. Geographically informative body regions 98 nGURE 10. Male courtship discrimination trials: intrapopulation 99 RGURE 11. Male courtship discrimination trials: interpopulation - field 101 FIGURE 12. Presentees us^ in the Bahia de los Angeles field courtship discrimination trials 105 FIGURE 13. Male courtship discrimination trials: interpopulation - laboratory. 106 11

LIST OF TABLES

CHAPTER I

TABLE 1. Predicted association between the intensity of sexual selection 51 TABLE 2. Categories of sexual dimorphism used in this study 52 TABLE 3. Qualitative sexual dimorphism scores used in this study 53 TABLE 4. Sexual dimorphism and habitat of families of teleost fishes 54 TABLE 5. Sexual dimorphism and egg type in families of marine teleosts 55 TABLE 6. Examples of sister-group species diversity comparisons in teleost fishes 56 TABLE 7. Mating system correlates of character state change in sexual dimorphism 60 TABLE 8. Examples of sister-group species diversity comparisons in other taxa . 62 TABLE 9. Cichlid radiation and correlates of species diversity 63

CHAPTER II

TABLE 1. Habitat characteristics of study sites 110 TABLE 2. Behavior of focal individuals Ill TABLE 3. Preliminary observations on the monthly reproductive condition of/4. crocitm 112 TABLE 4. Courtship behavior of males during 30 second focal periods 113 TABLE 5. Number of dorsal fin and anal fm elements in focal individuals. ... 114 TABLE 6. Geographically informative and non-informative color states 115 TABLE 7. Male courtship discrimination trials: intrapopulation 116 TABLE 8. Male courtship discrimination trials: interpopulation - field 117 TABLE 9. Summary of laboratory single female - single male trials 118 TABLE 10. Results of laboratory choice spawning trials 119 TABLE 11. Spawning history of female "Venecia 38.78" 120 TABLE 12. Spawning history of female "Cabo 34.5" 121

CHAPTER III

TABLE 1. Potential costs of sexual coercion for females 172 TABLE 2. Hypotheses, predictions, and tests of the benefits of mate-guarding 173 TABLE 3. Hypotheses, predictions, and tests of the benefits to females of mating with dominant males 174 12

ABSTRACT

This dissertation investigates the evolutionary consequences three very different behavior­

al mechanisms by which males may bias female mating decisions in their favor, elaborate male

displays (Chapters I and II) and sexual coercion and resource brokering (Chapter ni). The results

presented here suggest that sexual selection is an important force in evolution. In Chapters I and

II, I investigate the relationship between male courtship displays and speciation. Chapter I utilizes

the multiple sister-taxa comparison method to test the hypothesis that sexual dimorphism is cor­

related with increased species diversity in teleost fishes. In 21 of 27 sister-group comparisons,

the lineage with the greater degree of sexual dimorphism was more species-rich than its hj'po-

thesized sister taxa. The pattern holds across taxonomic levels and sensory modalities, and

whether the male, or the female, is the displaying sex. Additional data supporting the sexual selection-diversity hypothesis in other taxa are also discussed. Chapter II investigates how

variation in the signals displayed during social and sexual interactions affect reproductive isolation and may facilitate subsequent speciation, utilizing both field and laboratory experiments with the marine fish, Acanthemblemaria crockeri, a chaenopsid blenny endemic to the Gulf of California,

Mexico. The anterior portion of the body, the "signal organ", displayed during social inter­ actions, was found not only to be the most variable but was also the most geographically inform­ ative. The behavioral responses of the fish themselves, in both male courtship discrimination trials and in female spawning trials, reinforce these geographical differences and results suggest that variation in socially selected traits may accelerate reproductive isolation. In Chapter III, I exam­ ine how, if some males in a population use force to bias female mating decisions, protection can become a valuable resource that other males can use to attract females. I term this the bodyguard hypothesis of female mate choice. I present data illustrating the effectiveness of protective males 13

in reducing the probability of aggression from other males and suggest the importance of pro­

tective mating alliances in the evolution of a diversity of animal mating systems including mate guarding, leks, "harems", monogamy, polygyny, and pair-bonding in humans. 14

INTRODUCTION

Sexual selection is the differential ability among individuals, usually males, to acquire mates (Darwin 1871). At present, studies of sexual selection tend to focus on the factors influencing differential mating success: the origin and maintenance of female choice, the origin and maintenance of exaggerated male traits, and the affect of these factors on individual fitness.

My dissertation, in contrast, investigates the evolutionary consequences of these events. What happens over evolutionary time to lineages in which males evolve enormous tails, or flashy colors, or are four times the size of females? Are these male traits and "overflow of Nature's creative forces"? "beautiful nonsense"? or a creative force in evolution? I will argue, and provide some of the first data, that indeed, the later is true, sexual selection is an important force in evolution.

Darwin (1859, 1871) proposed both natural and sexual selection as mechanisms of evolutionary change. He argued extensively in the Descent of Man and Selection in Relation to

Sex that sexual selection could be an important source of the variation observed between closely related species. Since its inception, however, the concept of sexual selection was not well received (Wallace 1889; Mivart 1871; Groos 1898; Kropotkon 1903; Huxley 1938; reviewed in

Cronin 1992; Andersson 1995), and it was subsequently overlooked as modem evolutionary theory developed (Dobzhansky 1937; Mayr 1942). Traditionally, evolution has been viewed as a consequence of ecological adaptation in geographically isolated populations (Dobzhansky 1937;

Mayr 1942, 1963; Grant 1963). Reproductive characters were thought to evolve incidentally, as byproducts of genetic drift or pleiotropy, through selection against hybrids, or by perfection of intraspecific compatibility (Dobzhansky 1937; Mayr 1963; Paterson 1985). Proponents of sexual 15 selection have challenged this paradigm. Darwin (1871), West-Eberhard (1979, 1983, 1986) and others {e.g., Lande 1981; Dominey 1984; Carson 1986) have suggested that sexual selection plays an active and creative role in evolution.

Darwin recognized that males can increase their mating success by competing against other males for access to females and/or by biasing female mating decisions in their favor. The behavioral mechanisms by which maies may bias female mating decisions can be represented as a continuum, based on their affect on female survival;

Behavioral Mechanisms by which Males Can Bias Female Mating Decisions

QO

Negative Neutral Positive Effect on Female Survival

At one end of the continuum are mechanisms that bias female mating decisions indirectly, by exploiting female sensory biases or by brokering female access to limiting resources, mechanisms that may be neutral or beneficial to female survival. At the other end of the continuum are mechanisms that are detrimental to female survival, such as sexual coercion or forced copulation.

In this dissertation, I investigate the evolutionary consequences of these three very different behavioral mechanisms by which males may bias female mating decisions in their favor, elaborate male displays (Chapter I and Chapter II) and sexual coercion and resource brokering (Chapter

III). 16

In Chapter I and Chapter II, I investigate the relationship between elaborate male courtship displays and speciation. Chapter I utilizes the multiple sister-taxa comparison method to test the hypothesis that sexual dimorphism is correlated with increased species diversity in teleost fishes. Chapter D investigates how variation in the signals displayed during social and sexual interactions affect reproductive isolation and may facilitate subsequent speciation, utilizing both field and laboratory experiments with the marine fish. Acanthemblemaria crockeri, a chaenopsid blenny endemic to the Gulf of California. In Chapter III, I examine how, if some males in a population use force to bias female mating decisions, protection can become a valuable resource that other males can use to attract females and I review how this may be an important factor in the evolution of a diversity of animal mating systems. 17

CHAPTER I

SEXUAL SELECTION, COURTSHIP DISPLAYS, AND SPECIES DIVERSITY IN TELEOST FISHES: DOES SEXUAL DIMORPHISM PROMOTE DIVERSmCATION?

INTRODUCTION

Why do some groups of organisms have more species than others? Explaining differential

patterns of species diversity necessitates an understanding of the processes by which new species originate — the processes of speciation. Traditionally, speciation has been viewed as a consequence of ecological adaptation in geographically isolated populations (Dobzhansky 1937;

Mayr 1942, 1963; Grant 1963). Reproductive characters were thought to evolve incidentally, as

by-products of genetic drift or pleiotropy, through selection against hybrids, or by perfection of intraspecific compatibility (Dobzhansky 1937; Mayr 1963; Paterson 1985). Proponents of sexual selection have challenged this paradigm. Darwin (1871), West-Eberhard (1979, 1983, 1986) and others (e.g., Lande 1981, Dominey 1984, Carson 1986) have suggested that sexual selection plays an active and creative role in speciation. They propose that the rapid evolution of traits important in sexual selection often provides the impetus for new species formation with or without ecological differences.

Sexual selection may accelerate evolution in two ways: by enhancement of deme formation and by the rapid divergence of sexually selected traits. Organisms subject to strong sexual selection are often found in localized breeding populations, with small effective population sizes, such as harems or leks. Genetic drift in small, isolated populations can produce rapid divergence and promote speciation (Wright 1940). But what prevents these isolated, or semi- isolated, populations from re-mixing? An underlying assumption of most speciation theories is the necessity of reproductive isolation (Hodges & Arnold 1995; Dobzhansky 1937; Mayr 1942; 18

Grant 1963). Sexual selection should be especially effective at facilitating this final step because

the divergent characters are directly involved in the mating process. Any trait that can increase

the likelihood of reproductive isolation may therefore increase the rate of speciation and lead to

differential clade diversity.

In competition for mates under sexual selection, the signals used by males to attract

females should experience accelerated rates of evolution because (1) of their importance in

determining access to critical resources, (2) the reduction of a limit to change (except by selection

in other contexts), (3) the large number of factors that can initiate trends {e.g., selection operating

under different social or ecological conditions, drift, selection for novelty, and others), and (4)

the potential for mutually accelerating evolution (West-Eberhard 1983). Specifically, if there is

a correlation between male display and female preference within populations', relatively small

differences in male display between populations may accelerate speciation, due to affects on pre-

mating interactions or because hybrids are at a social disadvantage, and lead to differential

diversification rates among lineages. The more complex the courtship, and the more numerous

the characters involved, the greater the probability that one or more will diverge in isolation.

Sexual selection, and sexually selected signals in particular, may therefore represent a "key

innovation" in biological diversification.

' The relative position of two isolated (or semi-isolated) populations — either together toward reproductive cohesion, or away toward reproductive isolation — can be determined by the amount of genetic linkage-disequilibrium that evolves between the male trait and the female preference within each population. The amount of linkage-disequilibrium, in nira, is determined by the initial frequencies of the preference and trait in each population, the relative amounts of migration among populations, and the degree of selection against hybrids (O'Donald 1990, in prep.). Precise data regarding sexual-selection gradients are extremely difficult to obtain in natural populations (Lande & Arnold 1983, Andersson 1995). However, experimental evidence from stalk-eyed flies (Wilkinson & Reillo 1994), sticklebacks (Bakker 1993), and guppies (Houde & Endler 1990) supports this mechanism of assonative mating (reviewed in Pomiankowski & Sheridan 1994). There is theoretical justification to support the relationship between the action of sexual selection and the process of speciation by the divergence of sexually selected traits in allopatry,

parapatry, and sympatry (Lande 1981, 1982; Turner & Burrows 1995). Butlin (1995) and

Kirkpatrick (pers. comm. to G. Amqvist) note that the genetic correlation that arises in sexually selected taxa between a female preference and a male signal is difficult to invade, can amplify divergence initially generated by reinforcement, and can drive speciation to completion.

Classically cited examples consistent with the hypothesis that sexual selection, and sexually selected traits in particular, promote increased clade size include the Hawaiian

Drosophila (Speith 1968, Ringo 1977, Carson 1978), the cichlids of the African rift lakes

(Dominey 1984; Meyer et al. 1993), and birds (Raikow 1986; Hoglund 1989; Pierotti & Annett

1993). West-Eberhard (1983) cites several additional examples (see also Marzluff & Dial

199la,b). However, such a listing may be criticized as mere adaptive storytelling (Cracraft 1990).

Ultimately, both ecological/functional and comparative approaches are needed to test evolutionary hypotheses (Heard & Hauser 1995).

COMPARATIVE ANALYSES

The methodological difficulties in testing the relationship between sexual selection, or any other proposed key innovation, and species diversity are not trivial (Mitra et al. 1995; reviewed in Cracraft 1990; Heard & Hauser 1995; Sanderson & Donoghue 1996). First, changes in rates of speciation are likely to be marked by a suite of functionally related intrinsic characters and extrinsic events, and it is difficult to rule out confounding influences (and perhaps biologically shortsighted; see discussion). Second, all degrees of relative diversity are equiprobable and thus large differences in species numbers can be explained solely through stochastic processes (Raup et al. 1973; Guyer & Slowinski 1989; Slowinski & Guyer 1993). Recently, however, two 20

methods have been advocated to test hypotheses of character-diversity; the method of multiple

sister-taxa comparisons (Mitter ef a/. 1988; Zeh et al. 1989; Farrell et al. 1991; Lydeard 1993;

Weigmaim et al. 1993) and the maximum likelihood method (Sanderson & Donoghue 1994).

Studies using these tests have found a significant relationship between sexual selection/sexual

display and species diversity in birds (Barraclough et al. 1996 and Mitra et al. 1996) and plants

(Hodges & Arnold 1995).

Here, I use the method of multiple sister-taxa comparisons to test the prediction that sexual selection is associated with increased species diversity in teleost fishes. Specifically, I test

the prediction that, in sister taxa, the lineage with the greatest sexual dimorphism should be more diverse (see Table 1). My goals in this chapter are threefold: (1) to make these sister taxa comparisons for teleost fishes, (2) briefly to review the evidence for this hj'pothesis from other taxonomic groups, and (3) to discuss patterns that have emerged from this study regarding the evolution of signals used in sexual and social interactions and how they may affect species diversification.

METHODS

This test requires that I identify teleost lineages that have independently evolved sexually dimorphic characters involved with courtship, identify their sister taxa, and compare the diversities of the paired lineages. By definition, sister taxa are the same age (Hennig 1966; but see Weigmann et al. 1993 for possible complications) and any difference between them in diversity, such as the number of species, reflects different rates of diversification (speciation minus extinction, Stanley 1979; following Weigmann et al. 1993). THE DATA SET

Teleost fishes are the most species-rich group of vertebrates. The current estimate, cited

by Nelson (1994), lists 23,637 extant species in 38 orders and 451 families. Teleost fishes are

ideal for this study because of the tremendous diversity in sexual dimorphism that is icnown to exist. However, the sheer number of species renders this a daunting task. The data set used for

this study includes all families (and sometimes subfamilies and tribes) of teleostean fishes following the taxonomic designations of Nelson (1994). I chose the familial level because information on fish is readily accessed in this fashion and because for many families, but certainly not all, mating systems are conserved across species.

For each family, I compiled information on: (1) relationships; (2) species diversity; (3) the intensity of sexual selection, defined here as the relative ability of males to acquire multiple mates and of females to choose their mates; (4) the mating system; (5) sexual dimorphism, for which I used both a "sexual dimorphism record" (a record of the presence/absence of display traits) and a subjective "qualitative score" (see below and Tables 2 and 3); (6) additional reproductive traits that might be correlated with sexual dimorphism, such as the mode of fertilization, egg type, the presence and/or type of nest, the presence and extent of parental care, the presence of brooding and the sex of the brooding parent, the existence of alternative male reproductive strategies, and whether the fish migrate to localized breeding sites; and (7) major ecological and morphological traits that might shed light on the ecological context in which sexual dimorphism arises, such as body size (measured as standard length), habitat (freshwater or marine, coastal or offshore, lake or river-dwelling), depth range, primary food type, and schooling behavior. Clearly, this is a tremendous amount of information and I was by no means able to find the answer to all of these variables for all taxa considered. While I surveyed 451 families of teleosts, I used my best judgement to prioritize my search first to those taxa that 22

looked most likely to yield the above information. There are numerous omissions and this

continues to be a work in progress.

I used a four-tiered and iterative strategy to search for sister taxa comparisons. I began

looking for promising comparisons by reviewing Nelson (1994), Lauder & Liem (1983), Moser

et al. (1984), Johnson & Anderson (1993), and Paxton & Eschmeyer (1994) to obtain information

on higher-level relationships and general biology of teleosts. For general information on mating systems and sexual dimorphism, I used Thresher (1984) and Breder & Rosen (1966). Second, when tentative comparisons were found, I ran electronic library searches with BIOSIS for the years 1989 - September 1996 to obtain more recent information. BIOSIS searches 20,000

journals in the biological sciences. I also ran electronic searches of the abstracts for the 1996 meeting of the American Society of Ichthyologists and Herpetologists (ASIH) provided on the society's website. Third, I turned to the primary literature. Fourth, I contacted specialists to verify the final comparisons.

IDENTINCATION OF SEXUALLY DIMORPHIC TAXA

The first challenge was to define "sexual dimorphism". I used two methods to categorize sexual dimorphism (Tables 2 and 3, Appendices I and 11). The "sexual dimorphism record" records the presence of all sexually dimorphic characters observed for each family (or smaller taxonomic group therein, following the classification of Nelson 1994; Table 2). I included temporarily dimorphic characters (e.g., nuptial coloration) and permanently dimorphic characters.

Based on available information, sexually dimorphic characters were categorized as either "non- display" or "display" characters based on a subjective assessment of those considered most likely to function in courtship displays. Characters that were ambiguous were simply listed under both 23

categories, pending additional information. Each family (or lower taxonomic group) received as

many records as it had sexually dimorphic characters.

The "qualitative" score is based upon that subset of characters subjectively considered

most likely to function in courtship displays from the sexual dimorphism record, and their relative

degree of elaboration. The greater the degree of elaboration of the presumed display trait and/or

the greater the number of characters involved in the courtship display, the higher the score (see

Table 3). Scores ranged from I = monomorphic to V = sexes so dimorphic that they have been

considered separate species. I tried to omit all "non-display" sexually dimorphic characters, i.e.,

those unlikely to function in courtship displays (e.g., sexually dimorphic characters resulting from

niche partitioning, from selection on female fecundity, or that were associated with the transport of sperm or eggs). I tried to assign one qualitative score to each family (or lower taxonomic group). When a taxon contained lineages that dilfered significantly in their qualitative score, I assigned the appropriate score to each subgroup, and the family (or lower taxonomic group) therefore received multiple scores. This qualitative sexual dimorphism score is used in all further analyses in this study.

While the qualitative scoring method describes the relative pattern of sexual dimorphism among families, it undoubtedly falls short for many of them. Certainly, there are numerous species in which sexual dimorphism has not been recorded here, although it exists. Some sexually dimorphic species have simply not been observed, or described, and others may utilize sensory modalities that are not obvious to human investigators. In addition, some sexually dimorphic characters that have no apparent function in courtship display (e.g., chromosomal or meristic differences) may turn out to be important. I also did not score courtship motor patterns, nor include the elaboration or nests, because they were rarely quantified in the literature and were too difficult to compare across taxa. Lastly, I did not integrate into the sexual dimorphism score the intensity of sexual selection acting on females via male choice of female morphology or

behavior. However, these are certainly important aspects of mate choice that may affect

diversification rates. These omissions are priorities for future work.

The second challenge was to identify whether sexual dimorphism evolved through the

action of female choice rather than, or in addition to, intrasexual signaling, niche partitioning,

or phylogenetic constraints. Indeed, my test rests on the validity of this assumption (see

discussion). There is ample evidence to support this assumption. First, sexually dimorphic

characters are often displayed conspicuously during courtship (e.g., color patterns intensify and

fins are flared). Second, sexually dimorphic characters tend to occur in species in which females

are free to choose males and there is a bias in the distribution of matings among males (Robertson

& Hoffman 1977, Thresher 1984, Turner 1993), although it is not true that all sexually selected

species are sexually dimorphic and some monogamous species are sexually dimorphic as well.

Third, female mate choice has been shown to be correlated with aspects of male courtship display

in many teleost species (reviewed in Kodric-Brown 1990).

SISTER-TAXA COMPARISONS

I tallied sister-taxa comparisons using the following procedure (Figure 1). (1) I identified sexually dimorphic taxa from the data set described above that were monophyletic and that showed an unambiguous sexual dimorphism score. (2) I then looked for evidence to identify a definite sister taxon or closely related set of sister taxa. (3) I identified the sexual dimorphism score of the sister taxa from the data set described above. If the qualitative sexual dimorphism scores for the two taxa were the same, I returned to the first step. If the qualitative sexual dimorphism scores differed by one or more categories, I proceeded to the next step. (4) I obtained estimates of species diversity for each of the sister taxa and tallied the difference in 25

diversity between the two taxa, the sign of the difference in diversity, the cumulative probability,

and the relative net rate of diversification (see statistical analyses).

I attempted to control for factors hypothesized to be confounding ones by excluding certain comparisons a priori. I excluded from the analysis comparisons in which the sister taxa differed in major habitat type, egg type, or sensory modality. I did not compare freshwater with marine species, nearshore marine with pelagic species, shallow-dwelling with deep-dwelling species, species that spawn demersal eggs with species that spawn pelagic eggs, or species that court visually with ones that use primarily acoustic displays.

The greatest challenge was to find the most accurate reconstruction of sexual dimorphism on the phylogenetic tree. Often, I could not determine exactly where sexual dimorphism arose and, without this information, it was difficult (or impossible) to assign a sexual dimorphism score to each of the sister taxa. I attempted to establish where the change in dimorphism arose either by moving to shallower or deeper nodes in the tree (e.g., all families within the Ceratoidea share a similar sexual dimorphism and therefore the comparison was made at the superfamily level).

If I could not establish an unambiguous dimorphism score for each of the sister taxa, or if relationships were unresolved, I excluded the comparison from the tally of comparisons pending further information (see discussion of the salmonids and doradoids in Appendix A). In addition, without knowledge of one (and preferably two) outgroups, I frequently was unable to determine character polarity. Thus, while I know that the sister taxa tallied here differ in their sexual dimorphism score, I do not know if I am testing the effect of a gain, or of a loss, of sexual dimorphism on species diversity. The prediction of the effect on species diversity remains the same, regardless, of whether there is a gain or loss of sexual dimorphism.

Sexually dimorphic lineages sometimes contained derived lineages containing lesser or non-dimorphic species (and vice versa). I used three approaches to such interdependent comparisons. First, I choose comparisons on shallower nodes of the tree because nodes in shallow

portions of the tree have a higher probability of accurately reconstructing character evolution

(Maddison 1995). Second, If phylogenetic hypotheses for shallower nodes were unresolved, and

in situations in which the sexually dimorphic lineage contained derived less dimorphic lineages

(Figure 2, node c), I would subtract the diversity of the less dimorphic lineages firom the total

diversity of the sexually dimorphic lineage, because the remaining species represent the degree

of radiation associated with the sexually dimorphic character (I applied this approach to the

myctophid and syngnathid comparisons). In situations in which the less dimorphic Imeage

contained derived sexually dimorphic lineages (Figure 3, node b), I would include the entire

clade, if inclusion of the derived lineage did not affect the higher order comparison (as is the case

in the cichlid comparisons tallied here; following Mitter et al. 1988). In the first approach, the

resolution I gain by an accurate reconstruction of the characters, I lose by being unable to

generalize to the rest of the clade. The results of these comparisons should not be taken to be

representative of the entire clade unless additional sister-taxa comparisons corroborate the pattern.

This approach should be taken as a preliminary test of the hypothesis and awaits fiiture

reconstruction of the evolution of the sexually dimorphic characters. Additional approaches for

dealing with derived lineages are discussed by Mitter et al. (1988) and Barraclough et al. (1995).

In two cases, I have included comparisons comprised of trichotomies (the Pomacentridae

and the Belontidae). In these situations, I resolved the trichotomy in the most conservative

manner relative to the sexual selection-diversity hypothesis. For example, in the Belontidae,

relationships among the Macropodinae (the dimorphic lineage) and the Belontiinae and

Trichogastinae lineages (both less dimorphic) are unresolved. The most conservative resolution is to consider the lesser dimorphic lineages to be sisters themselves, and this lineage as sister to the Macropodinae. Thus, I combined the species diversities of the Belontiinae and the 27

Trichogastinae and compared this sum to the species diversity estimate for the Macropodinae.

DIVERSITY ESTIMATES

Species diversity estimates of clades used in sister-taxa comparisons were taken from

Nelson (1994) unless more recent systematic studies were available.

STATISTICAL ANALYSES

Trends in relative diversity of sexually dimorphic taxa compared to their less dimorphic sister taxa were evaluated with a sign test, Wilcoxon's signed-ranks test, Fisher's randomization test, and Fisher's combined probability test. The sign test is based on a null model of a 0.5 binomial probability of either of the two groups being larger. However, statistical tests based on this null model lack power because the model fails to consider the absolute differences in the diversity estimates of the sister groups (Slowinski & Guyer 1993). For this reason, Wilcoxon's signed-ranks test and Fisher's combined probability test were used to take the magnitude (absolute and proportional, respectively) of the diversity difference into account. Wilcoxon's signed-ranks test compares the test statistic against a normal distribution. The Fisher's randomization test

(Edgington 1980) compares the test statistic against a null distribution created by 10,000 randomizations of the signs of the differences in species diversity. For the Fisher's combined probability test (Sokal & Rohlf 1995), the probabilities for each comparison were calculated according to a model of random speciation and extinction originally formulated by Harding

(1971) and modified by Slowinski & Guyer (1993). Since elevated relative diversities for the sexually dimorphic clades are predicted, the tests are one-tailed, and I report one-tailed probabilities. A measure of the relative net diversification rate (R) between the two sister taxa 28

was estimated by taking the ratio of the logarithms of species diversity (Stanley 1979; modified

by E. Dyreson, pers. comm.):

R = log (# of species in sexually dimorphic clade) / log {ff of species in less dimorphic species).

A ratio of 1 indicates similar diversification rates. Data were analyzed using the SAS statistical package (SAS Institute Inc., Cary, North Carolina).

RESULTS

DESCRIPTIVE PATTERN

Sexual dimorphism is a widespread characteristic of teleost fishes (Figure 2). One hundred and ninety-eight families had sufficient data regarding sexual dimorphism to be analyzed

(Appendix A). Thirty-five of these families contamed both sexually monomorphic and dimorphic lineages. These families were counted under both categories.

Monomorphic families were comprised predominandy of marine fishes (82.9% were marine whereas 17.1% were found in freshwater; Table 4). Most (63%) of the monomorphic families were comprised of fishes that spawn pelagic eggs (18.4% spawn demersal eggs; Table

5). In contrast, sexually dimorphic families were comprised of a greater number of freshwater fishes and a greater number of demersal, or otherwise non-dispersive, spawners (45.6% of sexually dimorphic families are comprised of pelagic spawners whereas 36.7% are non-dispersive spawners).

The six most species-rich families (> 500 species; in descending order: Cyprinidae,

Gobiidae, Cichlidae, Characidae, Labridae, and Loricariidae) each contain extremely sexually dimorphic lineages (categories IV and V), although all of these families also contain less dimorphic lineages as well (Appendix A). Of the extremely dimorphic families for which I have 29

information, all appear subject to strong sexual selection, i.e., they exhibit mating systems in

which males are able to mate with multiple females and females are mobile and able to choose

among males. However, the converse is not true. Many families known for haremic mating

systems, suggesting strong sexual selection, are not necessarily extremely sexually dimorphic.

For example, the Cirrhitidae, some Labridae, some Pomacanthidae, and the Synbranchidae have

haremic mating systems but are sexually monomorphic.

Freshwater and marine species differed in the sensory modality exploited during courtship

(Figure 2). Visual, electrical, acoustical and tactile courtship signals are present in freshwater

systems, whereas only visual (color and/or modiHed morphology), and sometimes acoustical,

courtship signals have been observed in shallow water marine systems. Chemical and luminescent

signals predominated in deep sea species (e.g., Ceratoidea, Myctophidae).

SISTER-TAXA ANALYSIS

In 21 of 27 sister-taxa comparisons extracted from this review of teleost fishes, the

lineage with the greater degree of sexual dimorphism was more diverse than its hypothesized sister taxa by at least one, and sometimes two or three, orders of magnitude (Table 6). The

results were highly significant (p < 0.0025) by all statistical measures. Relative net diversifica­ tion rates of sexually dimorphic lineages vs less dimorphic lineages ranged from O.CX) {Cirriem- blemaria and Emblemariopsis) to 2.92 (Stemopygoidei and Gymnotoidei). One ambiguous

(Simochromis - Tropheus) and five contrary examples {Ancistrus - Chaetostoma clade, Anthiinae

- Epinephelinae, Anisochrominae - Congrogadinae, Ekemblemaria - Acanthemblemaria, and Cir- riemblemaria - Emblemariopsis) were encountered. In the latter, the less dimorphic lineage was more diverse than its hypothesized sister taxa by one order of magnitude or less. I discuss the 30

relationships, mating systems, and the sexual dimorphism of taxa used in the comparisons tallied

here in Appendix B.

Ninety-three percent of examples (14/15) from freshwater systems supported the hj^po-

thesis. The exception was the loricariid comparison involving the genus Ancistrus. Sixty-four

percent (7/11) of the marine comparisons supported the hypothesis. The remaining four contrary examples (Anthiinae-Epinephelinae, Anisochrominae-Congrogadinae, Ekemblemaria-Acanthem- blemaria, and Cirriemblemaria-Emblemariopsis) were found in shallow water habitats and involve visual displays. It is not known whether there is a visual or tactile (or both) component to the sexually dimorphic tentacles found in the loricariid genus Ancistrus (L. Rapp Py-Daniels pers. comm.). All (5/5) comparisons involving non-visual signals (acoustical, electrical, and chemical) supported the hypothesis. Two of the comparisons involved "sex-role reversed" mating systems in which females used displays to attract mates. Both of these examples, the pheromone-emitting and luminescent females of the superfamily Ceratioidea and the sexually dichromatic and dimorphic pipefish of the subfamily Syngnathinae, supported the hypothesis.

In 6/31 comparisons, the sister-taxa showed different mating systems (Table 7, Section

IV; the total number of comparisons tallied here = 31, because some comparisons fall under more than one category). In all six of these comparisons, the lineage exhibiting the greater sexual dimorphism had a mating system characterized by more intense sexual selection. In the remaining

25/31 comparisons, the sister-taxa shared a similar mating system. Thus, in these comparisons,

I was able to decouple sexual selection and sexual dimorphism and, independently, to examine the association between sexual dimorphism and species diversity. In 14/25 (Table 7, Section I), the sister taxa shared a similar mating system and differed in that one lineage was sexually dimorphic. In 12 of these, the sexually dimorphic lineage had more species than the non- dimorphic lineage. In the remaining 12/25 comparisons (Table 7, Sections II-V), the character 31

state change in sexual dimorphism was correlated with a character state change in parental care,

egg type, courtship display, or habitat use. In 11 of these, the sexually dimorphic lineage had

more species than the lesser or non-dimorphic lineage.

DISCUSSION

The consistently greater diversity of sexually dimorphic lineages provides strong support

for the hypothesis that sexual selection, and sexual dimorphism in particular, is correlated with

increased species diversity in teleost fishes. The data suggest the following points:

(1) There is a phylogenetic trend toward increasing elaboration of the sexually selected

traits and this trend is correlated with increasing diversity. In several of the sister-taxa

comparisons, there is a phylogenetic trend toward increasing elaboration of sexually dimorphic

characters within sexually dimorphic lineages, e.g., within the Mormyrinae, Cyprinella, Melano-

taeniidae, Xiphophorus, Anthiinae, doradoids, (Appendix B). This trend is correlated with

increased species diversity, the greatest diversity observed in the lineages with the greatest elab­

oration.

(2) An increase in species diversity is associated with the evolution of sexual dimorphism

in particular — not just the presence of sexual selection. In many of the comparisons tallied here,

the sister-taxa shared a similar mating system but, in one of the lineages, sexually dimorphic

displays evolved. These comparisons enabled me to decouple sexual selection and sexual

dimorphism and, independently, to examine the association between sexual dimorphism and

species diversity. In the majority of these comparisons, the elaboration and diversification of the signal was correlated with an increase in species diversity. This phenomenon, the ability to finely exploit a sensory system by signal and receiver, and its correlation with increased lineage 32

diversification — independent of mating system — was first suggested by Ryan (1986) for

anurans (see below).

Another way to test the idea that sexual dimorphism (independent of sexual selection) is

correlated with increased lineage diversification, is to examine sexually selected clades that have

secondarily lost dimorphism, such as the haremic and mimetic wrasses, and test for a correlated

reduction in diversity. Such tests await the necessary phylogenetic hypotheses.

(3) Shallow-water marine species showed the weakest correlation between sexual

dimorphism and diversity. Of the eleven marine comparisons tallied in this study, nine occur in

nearshore shallow water and have visual courtship displays. Five of these supported the

hypothesis (Syngnathinae - Hippocampinae, Genicanthus clade - Apolemichthys clade, Poma-

centrinae/Chrominae + Lepidozyginae - Amphiprioninae, Coralliozetus - Protemblemaria,

Acanthuridae - Zanclidae) and four did not (Anthiinae - Ephinephalinae, Anisochrominae -

Congrogadinae, Ekemblemaria - Acanthemblemaria, and Cirriemblemaria - Emblemariopsis).

This result may be explained by (a) chance, (b) the ability of larvae to disperse off natal reefs and

to move great distances in some groups {e.g., pomacanthids, chaetodontids and acanthurids;

Brogan 1994), (c) social selection accelerating diversification in the non-sexually dimorphic

lineages, and (d) visual signals being co-opted for a variety of other functions, both intraspecific and interspecific. I would predict these latter conditions to apply in tropical marine systems, as compared to freshwater systems, because of the greater densities of fishes, and of social inter­ actions, that may exist. Perhaps, in these systems, it may be more biologically relevant to ask how the evolution of visual signals (especially bright colors) used in social interactions (both intraspecific and interspecific) affects diversification rates.

(4) Non-visual courtship signals may be less constrained by selection in other contexts and show a tighter correlation with diversity. As a corollary to the point above, perhaps the use of olfactory, electrical, chemical and luminescent courtship signals shows a tighter correlation to

species diversity, as compared to visual signals, because they are not so readily, nor so often,

used for other fiinctions and thus are not so constrained by selection in other contexts. Moreover,

among visual signals, I would predict that morphological signals (e.g., spines and tentacles among

fishes) may show a tighter correlation with species diversity than do color patterns. I do not mean

to imply that the evolution of color is constrained — in fact, the opposite is probably true — but

rather that the correlation with species diversity via sexual selection may not be as tight because

the colors also may be under selection in different contexts.

(5) Pelagic spawning fishes may be extremely sexually dimorphic but were not necessarily

the most species-rich clades of fishes. The greatest opportunity for males to acquire multiple

mates, situations in which I would predict sexual dimorphism to be well-developed, should occur

in species without male parental care but in which the males are territorial and thus must court

to attract females {e.g., labrids). However, these groups often spawn pelagic eggs and may have

a long planktonic dispersal phase. The increased dispersal might swamp out the potential isolating

affects of geographic differences in male display. Thus, pelagic spawning, nearshore marine

fishes may have well-developed sexual dimorphism, but these lineages are not likely to be the

most species rich. These considerations may explain, in part, why the sexual selection-diversity

hypothesis is less well supported in some of the shallow-water marine systems (see below). In contrast, while I expect demersal spawning, sexually selected lineages to be species rich (because of the reduction in the dispersal ability of larvae relative to pelagic spawning lineages), I do not expect them to necessarily be the most sexually dimorphic. Male parental care may (but does not necessarily) reduce the opportunity for males to acquire multiple mates and may thereby reduce

the intensity of sexual selection (Wittenberger 1979). 34

POTENTIAL BIASES IN THE DATA

As noted in similar studies (Mitter et al. 1988), the final tally of comparisons I have

presented here represent a complex series of judgments about often fragmentary evidence. They

"rest on shifting phylogenetic soil" (Guyer & Slowinski 1993), and are vulnerable to errors in

phylogenetic reconstruction. However, such taxonomic error should be random with respect to

the mating display-diversity hypothesis. They also are potentially subject to statistical, taxonomic,

and phylogenetic artifacts (as in similar studies, see discussion in Mitter et al. 1988, Farrell et

al. 1991, Weigmann et al. 1993).

First, interpretation of these results may be biased by a lack of representativeness of the

samples. As mentioned, the 27 comparisons included here are only a small fraction of the many

possible. Future work on the phylogenetic relationships and biology of these fishes will permit

many more contrasts and may modify some of the comparisons made here. And, while I tried

to sample broadly, I am missing examples from some major lineages (e.g., Characidae, Gobiidae)

which could potentially yield different results. However, my sample should not be biased

regarding the hypothesis being tested. Sampling breadth was chosen at the expense of sampling

depth. In only a few lineages (e.g., Poeciliidae, Loricariidae, Chaenopsidae) was I able to make

multiple comparisons. Thus, I am unable to address whether the chosen comparisons are

representative of their lineages. (In the Poeciliidae, all comparisons showed support for the

hypothesis; in the Loricariidae the results were ambiguous; in the Chaenopsidae, two comparisons

were contrary and one supported the hypothesis).

Second, taxonomists might tend to recognize more species in groups that are sexually

dimorphic, and sexually dichromatic, in particular. This remains untested. However, fish

taxonomists traditionally base species descriptions on meristic counts taken from museum specimens, either preserved in ethanol or cleared and stained. In these specimens, color is either 35 not visible or only raelanic pigments remain. While these patterns may be described in taxonomic works, they are rarely used as diagnostic characters in species descriptions. In addition, I would not expect the visual abilities of taxonomists to bias results in non-visually signaling groups of fishes, such as acoustic or electrically signalling fishes.

It is also important to note that the vast majority of the characters used to construct the trees upon which these comparisons were built were not sexually dimorphic; most trees used in this study were based on osteological, muscular, soft-part anatomy, larval, or molecular data. The only exceptions being the loricariid and chaenopsid phylogenies in which a few of the characters involved in tree construction were dimorphic.

Third, the current test of the hypothesis that sexual selection by female choice has promoted speciation rests on the assumption that sexual dimorphism has evolved through female choice, rather than, or in addition to, intrasexual signaling, niche partitioning, and/or phylogenetic constraints. For the vast majority of examples, this remains untested. The ftinction and significance of sexual dimorphic characters are frequently unclear and we often suffer from over-interpretation of limited data (Thresher 1984). In particular, it is difficult to rule out the possibility that sexual dimorphism has not evolved in response to intrasexual signaling, which also has been suggested to increase divergence among populations, although the scenario has a weaker theoretical basis (Barraclough et al. 1995; West-Eberhard 1983; Tanaka 1996). While it may, in fact, be premature to assume that sexual dimorphism has evolved due to sexual selection by female choice, I propose to test its logical evolutionary consequences, by considering the potential accelerating affect sexual dimorphism may have on diversification rates.

Fourth, estimates of tree shape may be biased (Heard 1992; Guyer & Slowinski 1993;

Kirkpatrick & Slatkin 1993; Huelsenbeck & Kirkpatrick 1993). Tree symmetry may be affected by taxon sampling, clade size and the method of phylogenetic reconstruction. Importantly, computer simulations by Huelsenbeck & Kirkpatrick (1993) found that estimates of tree shape

were, on average, more asymmetrical than the true tree, especially when rates of evolution were

high. However, as mentioned above, the sexually dimorphic characters that I predict should evolve rapidly were not used to construct the trees upon which these comparisons are built.

Moreover, despite the potential biases in the reconstruction of phylogenetic hypotheses, these hypotheses still provide the best test of departure firom a null model of equal diversification rates between sister taxa.

Other than artifactual biases, the results reported here could also be due to confounding factors. Geographic range, habitat subdivision, and body size are among the most important ecological and life history correlates of increased species diversity in fish (Zapata 1990; P.

Hastings unpublished data; S. Mesnick unpublished data) and other groups (Marzluff & Dial

1991b). We should not necessarily attempt to factor out these intrinsic characters and extrinsic conditions in diversity comparisons but, rather, to study their interaction and reconstruct the sequence of their evolution.

EVOLUTIONARY IMPLICATIONS

(I) Increased species diversity in teleost fishes is associated with a suite of intrinsic characters and extrinsic conditions. Heterogeneous habitats, life history traits correlated with reduced dispersal, and sexual selection, alone and together, may contribute to population divergence, subsequent speciation and, ultimately, to differential rates of lineage diversification.

These characteristics are interdependent. While sexual selection is correlated with species diversification in the lineages tallied here, it is also likely that ecological divergence was crucial.

A more complete understanding of the evolution of species-rich clades will arise when we reconstruct the sequence of evolution of intrinsic characters and extrinsic conditions on phylogenetic trees. For example, the common ancestor of the haplochromine cichlid species flock

which invaded the isolated lakes of eastern Africa, with their heterogenous rocky shores and

relatively clear waters, with its hj^jothesized polygynous mating system, set the stage, so to speak, for the exploitation of a visual display system. Whether the same radiation would have occurred if the same haplochromine ancestor entered the Nile River, or if it was a substrate spawner, will remain untested. We can, however, reconstruct the evolution of multiple traits on trees and use the multiple sister-taxa comparison method to test the affect of suites of characters, or the sequence of character evolution, on species diversity.

(2) Social selection and species diversity. West-Eberhard (1983) suggested that both sexual signals, and the signals used in non-sexual social interactions, should experience rapid and divergent rates of character evolution. I would thus predict that lineages of monomorphic, but brightly colored animals to show increased rates of lineage diversification because the diversification of these signals may cause the breakdown of social communication among conspecifics. There is theoretical justification to support this hypothesis (Tanaka 1996). In species in which both sexes are colorful but isomorphic, I would expect significant geographic variation in coloration to be less likely to result in reproductive isolation among morphs. In contrast, I would predict that geographic variation in dichromatism among isolated, or semi-isolated, populations of a sexually selected and dimorphic species would be more likely to result in speciation events. The result in sexually selected lineages would be more species per genus.

This pattern, of polymorphic species, but few species per genus in non-dimorphic lineages, is found among cichlids; the sexually monomorphic but colorful Tropheus and

Eretmodini show numerous "subspecies" or "races" per species in contrast to the pattern seen in the sexually dimorphic Simochromis and Haplochromini; see Appendix B). This pattern has been well-documented among birds (Pierotti & Annett 1993). (3) Social/sexual characters evolve rapidly, erasing their pkylogenetic signal as they

evolve. In contrast, abiotic or ecological characters evolve relatively less rapidly and their

phylogenetic signal may be retained deep in trees. Key innovations that open new adaptive zones

occur relatively infrequently in evolution and their signal is likely to be retained deep in trees,

e.g., the radiation of birds ascribed to the acquisition of flight (Heard & Hauser 1995). In

contrast, "specialization" key innovations involve fine-tuning and can occur relatively rapidly

(e.g., social/sexual signals, plant/pollinator system, mimicry). In addition, they increase the rate

of formation of small, isolated populations. These factors are less likely to be retained over time

and will be most evident evolving in the shallow branches of trees. Thus, rates of character

evolution may be evident by their position in phylogenetic trees. Similarly, Jablonski & Bottjer

(1991) discussed how, in invertebrates, abiotic factors define orders (nodes deep in trees) while

ecological factors define genera (nodes in the mid part of trees). Here, I suggest that social

factors, and the social environment, because of its rapid rates of evolution, are most important

in events at the species level.

(4) Implications for conservation. Habitat destruction may accelerate the loss of sexually

selected and dimorphic species disproportionally. Because sexually selected species are predicted

to have small, localized populations and smaller geographic ranges, in any given geographical

area, habitat destruction would take a disproportionate number of these species. Moreover, in any

given geographical area, endemic species are likely to be comprised of a disproportionate number of sexually selected species. This can be tested by analyzing endemic species lists for specific geographic regions {e.g., in the Gulf of California, Thomson & Hastings ms). 39

OTHER TAXA

To evaluate the sexual selection-diversity hypothesis in a broader context, in this section,

I extend the multiple sister-taxa comparison method to other taxa. I review the results of

published sister-taxa comparisons on sexual selection and diversity in birds (Barraclough et al.

1995 and Mitra et al. 1996) and plants (Hodges & Arnold 1996), and I present the results of data

I have compiled on Drosophila, bovids, jumping spiders, and anurans (Table 8). These com­

parisons are but a few of the many that could be investigated. Other radiations that deserve

further investigation include the Anolis lizards, nastalanine moths, fiddler crabs, ephipid flies,

fireflies, green lacewings, ostracods, and primates.

Birds. In birds, where we perhaps have the best information available on mating systems,

sexual dimorphism and species diversity, sexual selection has often been implicated by several

authors as a factor in diversification (Raikow 1986; Hoglund 1989; Pierotti & Annett 1993). Two

recent studies have used multiple sister-taxa comparisons to test the hypothesis that sexual selec­

tion is correlated with increased species diversity. Barraclough et al. (1995) used sexual

dichromatism as a proxy for sexual selection. This study had the advantage of being able to

quantify sexual dichromatism with relative objectivity for virtually all species, based on field guides. They tallied 31 sister-taxa comparisons and found a positive correlation between the

proportion of sexually dichromatic species within a tribe and the number of species in those tribes. However, by considering only visual signals in their analysis, and not acoustical signals or other aspects of courtship displays, this study was biased in its representation of the sexual selection process in many groups. Mitra et al. (1996) tested how the intensity of sexual selection affects species diversity by comparing avian taxa with promiscuous mating systems to taxa exhibiting other (mostly monogamous) mating systems. They compiled 14 sister-taxa comparisons and found that taxa with promiscuous mating systems tended to be more species-rich. In both 40 studies, statistical significance was sometimes marginal depending on the test used and the taxa included.

Drosophila. The Hawaiian Drosophila have long been a classic example of an unusually diverse radiation in which sexual selection appears to play a role (Speith 1966; Ringo 1977;

Carson 1978; Kaneshiro 1989). The most widely accepted reconstruction of drosophilid relation­ ships puts the Hawaiian Drosophila as sister to a clade comprised of the Hawaiian Scaptomyza andEngiscaptomyza (Throckmorton 1962; DeSalle 1992; B. Heed pers. comm.; E. Dyresonpers. comm.; reviewed in Thomas & Hunt 1992; DeSalle & Grimaldi 1993). The outgroup of these two clades is thought to be some clade among the continental genus Drosophila. Both Hawaiian clades share the small, isolated and ephemeral environment of the island chain and have been isolated for about 40 million years (Lewin 1985). They differ in ecological habitat and mating behavior (Heed 1971; Speith 1974; Kambysellis et al. 1995). The Hawaiian DroJopMa inhabit montane rain forests. They display a complex courtship behavior that involves elaborate wing displays and volatile pheromones. The great majority of males are ornamented in morphology, size, and pigmentation, and the ornamentation is involved in the male's courtship display (Speith

1974). Most are lekking and the lek sites are species-specific (Heed 1971). Speith (1974) suggests that lekking behavior is a result of high predation by birds and other flies in the montane habitat.

Mating experiments confirm that females discriminate among males on the basis of the sexually dimorphic traits and that this reinforces the reproductive isolation among species (Kaneshiro &

Giddings 1987; Kyriacou et al. 1991). Their labile genetic system has been well-studied (Carson

& Templeton 1984). The Hawaiian Scaptomyza do not lek. There is no courtship, per se: males find females and mount them. They have diverse genitalia and sexual selection may be operating at this level (see Eberhard 1985), although this has not been investigated. There also may be many cryptic species not yet identified. Their genetic system remains to be studied. The relative 41

species diversities of the two clades support the sexual selection-diversity hypothesis (the

Hawaiiancontain about 484-1000 species whereas the Scaptomyza + Engiscaptomyza

contain about 230-300 species; Thomas & Hunt 1991; Heed pers. comm).

An alternative reconstruction (Grimaldi 1990) places the Hawaiian Drosophila in a genus

called Idiomya which is sister to two other Drosophila species and these are sister to the

Zygothrica genus complex (about 353 species). The mating system of Zygothrica species is

unknown, but they are sexually dimorphic, males having enlarged heads (and evidence of intense

male-male interactions).

Mammals: bovids. Most of the ruminating ungulates have sexually dimorphic horns or antlers. Vrba (1984) provides a tree of extant and extinct bovids with which I can compare the diversity of the Aepycerotini (impala) lineage, which have sexually dimorphic horns, with that of the Alcelaphini (wildebeest and hartebeest) lineage, which are monomorphic in horn shape.

Impala inhabit woodlands. They tend to be territorial and relatively sedentary. In contrast, the wildebeest and hartebeest inhabit open grasslands and are migratory. Both the social system and the pattern of sexual dimorphism predict that the impala lineage should be more species-rich than the wildebeest and hartebeest lineage. However, the opposite is true: the Aepycerotini contain 3 species whereas the Alcelaphini contain 32 species. However, these results represent an example of how a socially selected trait — the horns are used by males and females in social interactions in the large, mobile herds — may be expected to diverge via social selection and may facilitate speciation. The habitats, forage, social organization, and the evolution of horns in bovids and cervids would be especially interesting to study in the context of the sexual/social selection- diversity hypothesis (see Janis 1990).

Jumping spiders. Jumping spiders of the genus Habronattus are astoundingly sexually dimorphic and dichromatic in the body regions that males use to display to females during courtship (Peckham & Peckham 1889, 1890; Richraan 1982; Griswold 1987; Maddison &

Stratton 1988). Habronattus is sister to a subgroup of the genus Pellenes (Griswold 1987).

Species of this Pellenes ignifrons group are drab in color and sexually monomorphic, except

perhaps for a little red wash of color in some males (Maddison pers. comm.). Similarly, the

outgroup, another subgroup of the genus Pellenes, is drab in color. In both genera, species are

ground dwelling and inhabit open and arid habitats. Although males are thought to be more

mobile than females, little else is known about their mating behavior in the wild. There are no

obvious differences in the mating system of the two groups (Maddison pers. comm.). The relative

diversities of the two clades support the sexual selection-diversity hypothesis: the sexually

dimorphic genus Habronattus contains 95 described species and the relatively drab Pellenes ignifrons subgroup contains 10-15 species.

Anurans. In frogs, males call to females in ponds, females are attracted to the calls and search among males, usually for the individual with the lowest call frequency, and mate. The

mating system is basically consistent across taxa (Ryan & Rand 1993). No two species have the same call and experimental results show that the mating call is an important behavioral isolating

mechanism (Ryan 1986, Ryan & Rand 1993). Ryan (1986) mapped the structural components of

the ear on an anuran phylogeny constructed by Dowling & Duellman (1973). His analysis showed

a tight correlation between the development of the inner ear, and thus the ability to exploit the acoustical range, and species diversity, as predicted by the sexual selection-diversity hypothesis.

The order Urodela (salamanders), the outgroup to the anurans, and primitive anurans (three families with four species) possess one patch of sensory epithelium. The Discoglossidae (9 species) and the Pipidae + Pelobatidae (66 species) possess simple two-patch papillae of varying lengths. The Pipidae Pelobatidae are sister to the clade containing the modem anurans (2,489 species) which possess an elongate and recurved two-patch papillae (relationships modified from Dowling & Duellman 1973 and Ford & Cannatella 1993). Ryan suggests that the great diversity

of the modem frogs is due to changes in their inner ear that have given this group a greater range

of variation over which the calls can diverge from one another and over which evolution can

occur.

Plants. Hodges & Arnold (1995) expand the idea of sexual dimorphism and sexual

selection to the ways in which plants attract pollinators. In columbines, the nectar spur, a tubular

outgrowth of the flower, is intimately tied to reproduction. Relatively simple differences in the

length, shape, orientation, and color of the spur are associated with different pollinators.

Differences in the nectar spur among closely related species potentially can facilitate reproductive

isolation and possibly lead to enhanced rates of speciation. In columbines, the most parsimonious

reconstruction of the evolution of nectar spurs places it on the lineage leading to the diversifica­

tion of the genus Aguilegia (14 species). The sister taxa, the genus Semiaquilegia, lacks nectar

spurs (1 species). Using the maximum likelihood test of Sanderson & Donoghue (1994), the

authors found support for the sexual selection-diversity hypothesis by showing that the origin of

nectar spurs and an enhanced rate of speciation were correlated on the columbine tree. In

addition, using the multiple sister-taxa comparison method, they found significantly greater

diversity than expected in either three or four, out of five additional groups, that independently

evolved nectar spurs (the correlation was in the expected direction with the Fumariaceae,

Tropaclaceae, and Lentibulariaceae; was in the opposite direction with Pelargonium-, and the

relation was equivocal for Delphinium and Aconitum depending on the sister group identified).

The multiple sister-taxa comparisons were nearly significant using a Wilcoxon's signed-ranks test and were highly significant using Fisher's combined probability test. 44

PRIORITIES FOR FUTURE WORK

(1) Determine the relationships among female choice, intrasexual competition, the intensity of sexual selection, and the elaboration of sexually dimorphic traits for specific popu­ lations. The sexual selection-diversity hypothesis rests upon many untested assumptions regarding

these processes.

(2) Finer reconstruaion of sexually selected traits onto phylogenetic trees and better resolution of the timing of changes in diversification rate. What multiple sister-taxa comparison tests gain in breadth, they lose in depth. Because they are essentially two-taxon trees, sister-taxa comparisons take into account minimal information present in a tree (Sanderson & Donoghue

1994) and minimal information regarding the origin and subsequent development of the trait. The inclusion of at least one outgroup taxon (preferably two) and/or information on changes in character states should permit finer resolution of the timing of changes in diversification rate, which can then be tested against null models of random speciation and extinction {e.g., the maximum likelihood test developed by Sanderson & Donoghue 1994).

(3) Sexual selection and the rate of molecular evolution. Because sexual selection is predicted to accelerate population subdivision, I would expect accelerated rates of molecular divergence among populations or related species. I know of no study that has addressed this topic directly. However, two classic empirical studies show enhanced rates of chromosomal evolution in social mammals (Bush et al. 1977; Wilson et al. 1975). However, preliminary data collected by Mesnick (unpublished data) showed no correlation between the intensity of sexual selection and the amount of genetic divergence using allozyme electrophoresis. Comparative molecular studies of population subdivision based on studies using more discriminating techniques, such as mtDNA or microsatellites, may prove rewarding (Mesnick & Peterson in prep.).

(5) Extend the multiple sister-taxa comparison method to test the social selection-diversity hypothesis. The multiple sister-taxa comparison method could be used to test for a correlation 45

between the elaboration of social signals {e.g., bright colors in coral reef fishes, tropical birds)

and species diversity. It would be especially rewarding to test this hypothesis, for example, in

the forest-dwelling guenons of Africa, where brightly colored faces peaking out from perches in

tropical forest trees signal information about sex, age, species and motivation (Kingdon 1989;

Gautier et al. 1988).

CONCLUSIONS

The consistently greater diversity of sexually dimorphic lineages when compared to sister

lineages with lesser sexual dimorphism provides strong support for the hypothesis that sexual

selection, and sexual dimorphism in particular, is correlated with increased species diversification

rates in teleost fishes. The pattern holds across taxonomic levels, sensory modalities, and whether

the male, or the female, is emitting the signal. Evidence for the sexual selection-diversity

hypothesis is also found in taxonomic groups as diverse as birds, frogs, spiders, Hawaiian

Drosophila and plants. Future work will seek to understand the processes of diversification at the specific level and expand the analysis to socially selected traits.

•• •

This study was inspired by Donald A. Thomson, who originally suggested that I examine the association between sexual dimorphism and diversity. This study would not have been possible without the extraordinarily generous contributions of many investigators. For sharing their knowledge, time, and enthusiasm for their fish with me, I extend my sincere gratitude to

Carole Baldwin, Alex Basolo, Andy Cohen, James Farr, Tony Gill, Phil Hastings, Carl Hopkins,

Ingrid Kaatz, Alex Kerstitch, John Lundberg, Paula Mabee, Richard Mayden, Axel Meyer,

Randall Mooi, Lynne Parenti, Lucia Rapp Py-Daniel, Peter Reinthal, Donald Thomson, Eric

Verheyen, and Amanda Vincent. I thank Donald Thomson, Phil Hastings, Wayne Maddison, Judie Bronstein, Bob Smith, and John Lundberg for critical reviews of an earlier draft of this

chapter. I thank Eric Dyreson for his patient statistical assistance.

SUMMARY

The multiple sister-taxa comparison method was used to test the hypothesis that sexual

selection, and sexual dimorphism in particular, is correlated with increased species diversity in

teleost fishes. In 21 of 27 sister-group comparisons, the lineage with the greater degree of sexual

dimorphism was more species-rich than its hypothesized sister taxa by at least one, and sometimes

two to diree, orders of magnitude. The pattern holds across taxonomic levels and sensory

modalities, and whether the male, or the female, is the displaying sex. Additional data supporting

the sexual selection-diversity hypothesis were found in taxonomic groups as diverse as birds,

frogs, spiders, Hawaiian Drosophila and plants. The results suggest the following for the

evolution of teleost fishes: (1) In some sexually dimorphic lineages, there is a phylogenetic trend

toward increasing elaboration of the sexually selected trait, and this trend is correlated with

increasing diversity. (2) An increase in species diversity is associated with the evolution of sexual

dimorphism in particular — not just with the evolution of a greater intensity of sexual selection.

(3) Shallow-water marine fishes show the weakest association between sexual dimorphism and

species diversity. (4) Non-visual signals (acoustic, electrical, pheromonal) show the tightest

association with increased species diversity. (5) Pelagic spawning fishes may be extremely sexually dimorphic but were not necessarily the most species-rich clades of fishes. In addition,

the data suggest the following evolutionary implications, applicable to a wide variety of sexually selected and dimorphic organisms: (1) A suite of correlated social and ecological characters and historical events spur diversification. (2) Sexually selected lineages show relatively more species/genus whereas socially selected lineages show more "subspecies"/species. (3) Sexually 47

selected characters are expected to evolve rapidly, and thus are more likely to be observed at the

tips of phylogenetic trees, whereas naturally selected characters evolve relatively less rapidly and

thus are more likely to retain their signal deep in trees. (4) Habitat destruction may accelerate the loss of sexually selected and dimorphic species disproportionally. Sexual selection, and the diversification of the signals used to attract mates in particular, are factors that should be considered in explaining patterns of species diversity in teleosts and other animal and plant groups. 48

FIGURE 1. The sister-taxa comparison method. Taxa were included in this tally of comparisons only if (1) they showed an unambiguous character state for sexual dimorphism, (2) there was evidence for their monophyiy, and (3) there was evidence to identify a definite sister group (or closely group of closely related taxa). Comparisons of species diversity between the sexually dimorphic clade, and its less dimorphic sister clade, would be made at "node a" [e.g., 13 species in the dimorphic clade would be compared to 11 species in the less dimorphic clade), unless either clade contained derived lineages with another character state, as is shown here, and thus violating (1) above. In this situation, I would move to shallower nodes in the tree, e.g., "node b" and "node c", and make the comparison/s at this level. If, however, relationships at shallower nodes were unresolved, and a derived less dimorphic lineage was contained within the sexually dimorphic clade {e.g., "node c"), I would subtract the species diversity of the derived lineage from the total species diversity of the sexually dimorphic clade, because the remaining species diversity represents the degree of radiation associated with the sexually dimorphic characters(s). In the example shown here, the new species diversity for the sexually dimorphic clade would be 13-3 = 10. If a derived dimorphic lineage was contained within the less dimorphic clade {e.g., "node b"), I would include the species diversity of the derived lineage, if inclusion of the derived lineage did not affect the results of the higher order comparison (at "node a" in this example), a conservative approach relative to the sexual selection-diversity hypothesis. In the example shown here, inclusions of the derived lineage at "node b" (n = 2) has no bearing on the result of the higher order comparison (13 compared to 11 as noted above); the less dimorphic clade is less species rich, regardless of the inclusions of the derived lineage at "node b". FIGURE 1.

NODEB NODEC

Sexual Dimorphism NODE A sexually dimorphic non-dimorphic or less dimorphic equivocal n II n II ^ " II •[•••••••• Osteoglossiformes •n O ••••••••• Elopiformes G isdii" "Si ?0 ••••••••• Albulifomnes w S) • '"Ss? ••••••••• Anguillifomnes ••••••••O m o < Saccopharyngiformes 2. ••••••••• Clupeiformes ? ••••••••• Gonorhynchiformes c OCDCDaoaOHBi Cypriniformes •••••••••Characifomnes Via OOOOOaOMHI Silurifomnes cX ••••aaaizia Gymnotiformes •••••••aa Esocifomnes £Lrt •••aaaaaa Osmeriformes n o Salmoniformes CL •••••cuanDizi Ateleopodifomnes us Stomiifomnes 69 Aulopifomnes 3o Mycotophiformes OQ3 Lampridiformes n o •••••••••Polymixiiformes Vi n ••aaaaaaizi Ophidiiformes C/3 •••••••••Percopsiformes Gadiformes a •-! ••aaanciz]* Batrachoidiformes Vi in Lophiiformes •o oCD •••••••••Mugilifomnes n' ••••••••• Atheriniformes Vi ••••••••• Beloniformes J? •••••••an Cv^Drinodontiformes •••••••••Stephanoberyciformes c/> z? ••••••••• Beryciformes S "o ® •o ••••••••• Zeiformes (39) 3 3 81 ••••••••• Gasterosteiformes s Z (D § 3-(P CD ^ ••••••••• Synbranchiformes ViO 5^ Q- z ••••••••• Scorpaeniformes Vi § < "D J 0 CO ••••••••• Perciformes ^ Q ^ 3 ••••••••• Pleuronectiformes O •••••••••Tetraodontiformes

OS ZQ 51

TABLE I. Predicted association between the intensity of sexual selection (defined here as the relative opportunity among males to acquire multiple mates and the relative ability of females to choose their mates), mating system, development of sexually dimorphic display characters, and species diversity in teleost fishes.

Predicted Intensity of Sexual Mating system species sexual selection dimorphism diversity "polyandrous" (group spawning) or low long term bonds which may be monomorphic low monogamous or haremic

polygynandrous ("promiscuous", moderate prefered mate pairbonding, moderate moderate temporary pair bonds)

high polygynous extreme high 52

TABLE 2. Categories of sexual dimorphism used in this study. The "sexual dimorphism record" records the presence of any observations of a sexually dimorphic trait.

Sexual Dimorphism Record

I. Absent. Monomorphic. n. Present. A. Non-display 1. Gamete transport. Sexually dimorphic morphology associated with the transport of sperm or eggs. 2. Fecundity. Dimorphic traits associated with selection on female fecun­ dity, e.g., females larger than males. 3. Ecological. Sexual dimorphic morphology associated with niche differen­ ces. 4. Internal. Chromosomal or vertebral count differences between the sexes. B. Display * 1. nuptial coloration 2. males larger than females 3. visual a. color b. egg spots 4. acoustical 5. electrical 6. tactile (pearl organs, tubercles) 7. chemical 8. visual - morphological a. fin extensions b. head shape (jaw size, lips, crests, etc.) c. eye position and size d. opercular modifications e. scalation f. dentition g. odontodes, spines (may be tactile) h. fleshy head extensions (barbels, papillae,etc.) i. body shape (keels, adipose flaps, tail, etc.) j. gonopodium k. cirri (e.g., blennies) 1. flesh swells (e.g., daners) 9. visual - structural (bowers, nests)

* For most species, it is unclear to what extent, if at all, these characters are displayed during courtship or are evaluated by females during mate choice decisions. They are included in the data set in the following categoires pending specific infomation on their function. 53

TABLE 3. Qualitative sexual dimorphism scores used in this study. The qualitative score is my assessment of the degree of elaboration of characters displayed during courtship by males (or by females in sex-role reversed species). I = monomorphic or the dimorphic character is not used in courtship display; II = slight (e.g., small differences between the sexes in color, fin extensions, or size); in = moderate dimorphism (distinct differences bewteen the sexes in one or two characters); FV == extreme (sexes very different in two or more characters); V = different species (sexes so different that they were once thought to be different species).

Sexual Dimorphism Score Description

Sexes similar or the sexually mono­ morphic dimorphic characters are not displayed during courtship

n small differences between the sexes slight in color, fin extensions, or male size

III distinct differences between the sexes moderate in one or two characters; moderate elaboration of characters

rv sexes very different in two or more extreme characters; extreme elaboration of characters

V sexes so different that they were once "different species" thought to be different species 54

TABLE 4. Sexual dimorphism and habitat of families of teleost fishes. "Monomorphic" refers to category I in Table 3; "dimorphic" refers to categories II - V in Table 3. Some families contain both sexually monomorphic and dimorphic species (see Appendix I). These are entered under both applicable categories.

Sexual Dimorphism Monomorphic Dimorphic (n = 111 families) (n = 132 families)

Marine 92 (82.9%) 79(59.8%) Freshwater 19 (17.1%) 53 (40.2%) 55

TABLE 5. Sexual dimorphism and egg type in families of marine teleosts. "Monomorphic" refers to category I in Table 3; "dimorphic" refers to categories II - V in Table 3. Some families contain both sexually monomorphic and dimorphic species (see Appendix I). These are entered under both applicable categories.

Sexual Dimorphism Monomorphic Dimorphic (n = 92 families) (n = 79 families)

Dispersive 58 (63.0%) 36 (45.6%) (pelagic spawners)

Non-dispersive (demersal spawners 17 (18.4%) 29 (36.7%) and brooders)

Mixed (family contains both 7 (7.6%) 7 (8.9%) dispersive and non- dispersive egg types)

unknown 10 (10.9%) 7 (8.9%) TABLE 6. Examples of sister-group species diversity comparisons on sexually dimorphic lineages of teleost fishes. The most evident sensory modalities used during courtship are indicated in parentheses. In 21 of 27 sister-taxa comparisons, the lineage with the greater degree of sexual dimorphism was more species rich than its hypothesized sister taxa. For sources and discussion see Appendix 11.

direction of relative > Dimorphic lineage < Dimorphic lineage difference difference net in species in species cumulative divers, taxon spp. taxon spp. diversity' diversity^ probability^ rate (R)

Osteoglosiformes (electrical, sound) Mormyrinae 165 Petrocephalinae 26 + 139 0.14 1.57

Cypriniformes (visual - color, morphology; acoustical, tactile) Cyprinella 28 Pimephales + + 22 0.18 1.86 Opsopoeodus -h Codoma Siluriformes Loricariidae Ancistrinae (fleshy tentacles - visual? tactile?) Ancistrus 55 Chaetostoma clade 68 -13 0.56 0.95

Loricariinae (odontodes - visual?) Rineloricaria 45 Harttia 13 + 32 0.23 1.48

Callichthyidae (acoustical) Corydoradinae 120 Callichthyinae + 112 0.06 2.30

Gynmotiformes (electrical) Sternopygoidei 57 + 53 0.07 2.92 Gymnotoidei U* Myctophiformes (visual - luminescence) Myctophidae (117)^ Neoscopelldae + + 111 0.05 2.66 TABLE 6 - Continued

direction of relative > Dimorphic lineage < Dimorphic lineage difference difference net in species in species cumulative divers. taxon spp. taxon spp. diversity' diversity^ probability^ rate (R)

Lophidiformes (chemical; female display) Ceratioidea 149 Ogocephalioidea 62 + +87 0.30 1.21

Atheriniformes (visual - color and morphology) Melanotaenidae + 85 Bedotioidei 9 + +76 0.10 2.02 Pseudomugilidae 4- Telmatherinidae

Cyprinidontiformes (visual - color, morphology) Poecilidae Poecilia (high fm clade) 40 Poecilia (low fin clade) 9 + +31 0.19 1.68

Xiphhophorus 23 Priapella 3 + +20 0.12 2.85

Goodeidae Goodeinae 36 Empetrichthyinae 4 + +32 0.10 2.58

Aplocheilidae Aplocheilinae Aphyosemion clade 225 Aplocheilus clade 92 + + 133 0.29 1.20

Gasterosteiformes (visual - color, morphology; female display) Syngnathinae (193)^ Hippocampinae 35 + + 158 0.15 1.48 TABLE 6 - Continued

direction of relative > Dimoqjhic lineage < Dimorphic lineage difference difference net in species in species cumulative divers, taxon spp. taxon spp. diversity' diversity^ probability^ rate (R)

Perciformes Percoidei Serranidae (visual - color, morphology) Anthiinae 175 Epinephalinae 203 -28 0.54 0.97

Pseudochromidae (visual - color, morphology)'* Anisochrominae 2/3? Congrogadinae 22 -20 0.96 0.22

Centrarchidae (visual - color, acoustical) Lepomis 11 Enneacanthus + + 8 0.23 2.18

Percidae (visual - color, morphology) Etheostoma 103 Percina 39 -f +64 0.28 1.27

Pomacanthidae (visual - color, morphology) Genicanthus + 37 Apolemichihys + 15 +22 0.29 1.33 Centropyge Pygoplites + Holacanthus

Labroidei Pomacentridae (visual - color and morphology, acoustial)'' Pomacentrinae 199 Amphiprioninae 28 Chrominae + 88 +60 0.24 1.34 S Lepidozyginae TABLE 6 - Continued

direction of relative > Dimorphic lineage < Dimorphic lineage difference difference net in species in species cumulative divers. taxon spp. taxon spp. diversity' diversity- probability^ rate (R)

Cichlidae (visual - color and morphology)^ Haplochromini 800-1300 Tropheini 12 + -f-788-1288 0.02 2.69

Simochromis 6 Tropheus 5-6 -1-/= -t-1/0 0,54 1.00

Blennioidei Chaenopsidae (visual - color and morphology) Ekemblemaria 3 Acanthemblemaria 17 -14 0.90 0.39 Cirriemblemaria 1 Emblemariopsis 9 -8 1.00 0.00 Coralliozetiis 6 Protemblemaria 2 + +4 0.29 2.58

Acanthuroidei (visual - color and morphology) Acanthuridae 72 Zanclidae 1 + +71 O.Ol

Anabantoidei Belontidae (visual - color and morphology, acoustical)'* Macropodinae 32 Belontiinae 2 + -his 0.31 1.31 Trichogastinae 12

' paired sign test: S+ = 21, d.f. = 26, p = 0.0025 2 Wilcoxon paired sign rank test: T+ = 145.5, d.f. = 26, p = 0.0001; Fisher's randomization test, p < 0.(XX)1 3 Fisher's combined probability test; = 89.34, d.f. = 54, p = 0.0018 '* For the most conservative estimate, relative to the sexual selection-diversity hypothesis, the following were used in the statistical calcuations (see Appendix I for discussion): species diversity in Anisochrominae = 2; Chrominae + Lepidozyginae used as siter to the Amphiprionae; species diversity in Tropheus = 6; and Belontiinae and Trichgastinae combined as sister to Macropodinae. ^ Species diversity estimates were adjusted by subtracting out lesser or non-dimorphic species (see Appendix 1 for discussion) TABLE 7. Mating system correlates of character state change in sexual dimorphism. Polygynandrous mating systems have varying potential for polygyny among males. By convention, the lineage with the greater degree of sexual dimorphism is listed first. Some comparisons fall under more than one category. "PC" = parental care. For sources and discussion see Appendix 11.

Direction of difference Sister-taxa comparison in species diversity Mating system

I. SISTER TAXA WITH SIMILAR MATING SYSTEMS Mormyridae • Petrocephalinae both lineages nesting w/cS PC and probably polygynandrous Ancistrus • Chaetostoma clade both lineages probably polygynandrous w/6 PC Rineloricaria • Harttia + both lineages probably nest in the open & are polygynandrous Sternopygoidei • Gymnotoidei + species spawn repeatedly over several months; polygynandrous ? Myctophidae • Neoscopelidae + mating unknown Melanotaenidae clade • Bedotiidae + both lay eggs in aquatic vegetation; polygynandrous ? Xiphophorus • Priapella + courtship display & gonopodial thrusting • unknown; polygnandrous Anisochrominae • Congrogadinae both with long term pair bonds and egg guarding Lepomis • Enneacanthus + both nest, w/d PC, polygynandrous some Etheostoma • Percina + egg buriers, dumpers and clusterers • egg buriers; polygynandrous ? Centropyge clade • Apolmichthys clade + variable mating systems, polygynous? Acanthuridae • Zanclidae + variable mating system • reproduction unknown Macropodinae • Belontiinae/Trichogastinae + bubblenesters; polygynandrous Cirriemblemaria • Emblemariopsis + resource defense polygyny II. SISTER TAXA WITH SIMILAR MATING SYSTEMS BUT WITH DIFFERERENCES IN THE PRESENCE OF PARENTAL CARE Cyprinella • Pimephales clade + crevice spawners w/o <5 PC • egg clusters w/d PC Corydoradinae • Callichthyinae + no nest, w/o d PC • bubblenest w/d PC some Etheostoma • Percina + egg buriers; dumpers and clusterers w/d PC • egg buriers w/o d PC III. SISTER TAXA WITH SIMILAR MATING SYSTEMS BUT WITH DIFFERENCES IN LIFE HISTORY TRAITS Goodeinae • Empetrichthyinae + viviparous • oviparous Aphyosemion • Aplocheilus clade + annual & nonannual • annual TABLE 7 - Continued

Direction of difference Sister-taxa comparison in species diversity Mating system

IV. SISTER TAXA WITH SIMILAR MATING SYSTEMS BUT WITH DIFFERENCES IN THE FORM OF THE COURTSHIP DISPLAY high fin Poecilia • low fin Poeciiia + courtship display • gonopodial thrusting ? Xiphophorus • Priapella + courtship display & gonopodial thrusting • unknown V. SISTER-TAXA HAVE SIMILAR MATING SYSTEMS BUT DIFFER IN TERRITORIALITY/HABITAT USE some Haplochromini • Tropheini + only dominant males territorial • both sexes territorial Simochromis • Tropheus =/-f only dominant males territorial • both sexes territorial some Etheostoma • Percina + egg buriers; dumpers and clusterers territorial • egg buriers not territorial Coralliozetus* Protentblemaha + females out of shelters • both sexes in shelters VI. SISTER TAXA HAVE DIFFERENT MATING SYSTEMS Ceratioidea • Ogocephalioidea + parasitic (permanent monogamy/polyandry) • mating unknown Syngnathinae • Hippocampinae + sex role reversed/polygamy • conventional sex roles/monogamy Anthiinae • Epinephelinae protogynandry • group spawning/protogynandry Pomacentrinae • Amphiprionae or Chrominae + polygynandry • monogamy some Haplochromini • Tropheini + polygyny • polygynandry Simochromis • Tropheus = /+ polygyny • polygynandry TABLE 8. Examples of sister-group species diversity comparisons on sexually dimorphic lineages of unusually diverse taxa. Sources are cited in the text.

direction of relative > Dimorphic lineage < Dimorphic lineage difference difference net in species in species cumulative divers, taxon spp. taxon spp. diversity diversity probability rate (R)

Mammals - bovids Aepycerotini Alcelaphini 32 +29 0.09 0.32

Reptiles - anolis lizards' Anoies 170 Para-anoles 5 + + 165 0.03 1.71 Leiosaurus 20 + 150 0.11

Amphibians - frogs Leptodactylidae 2489 Pipidae + 66 -1-2440 0.03 1.87 Pelobatidae

Spiders - jumping spiders Habronattus 95 Pellenes iRnifrons 15 + 4-80 0.14 1.68 subgroup

Insects - Drosophila Hawaiian —484-1000 Hawaiian — 230-300 -f- 4-700 0.23 1.21 Drosophila Scaptomyza + Engiscaptornyza

' Etheridge & DeQueiroz 1988; Schwartz & Henderson 1991; P. Holm pers. comm. TABLE 9. Cichlid radiation and correlates of species diversity. The Madagascar flock is sister to the remaining groups. The neotropical lineage is sister to the African lineages, and the haplochromines are sister to the Tropheini, one of the 12 Tanganyikan tribes. In genera) (there are exceptions), substrate spawners tend to be pair-bonded with bi-parental care and mouthbrooders tend to be polygynous. Mating system and sexual dimorphism are not necessarily correlated, ie., there are monomorphic mouthbrooders (e.g., many South American genera). However, it is important to note that the haplochromines are generally sexually dimorphic and polygynous mouthbrooders.

Pleisiomorphic Haplochromines of Lakes Lake Tanganyika Madagascar Neotropical African Malawi, Victoria, satelite (12 tribes) (Helerochromis) lakes 3.5-4 million years Age of lake 9-12 million years (Malawi) and 700,000 - 800,000 years (Victoria) 50,000 - 150,000 years Age of flock 9-12 million years (Malawi) and 14,000 years (Victoria) Habitat rivers and lakes rivers rivers lakes lakes

Water clarity low low low high high Colorful no no some yes yes

substrate substrate substrate substrate Mating behavior spawners and spawners and mouthbrooders spawners spawners mouthbrooders mouthbrooders none to low Sexual none to low none to low (some in dwarf (none) to high (none) to high dimorphism species) Species diversity 9 I 350 171 800-1300+

Sources; relationships, Stiassny 1992, Meyer et al.l994; mating behavior. Barlow 1991; age of lakes and cichlid flocks, Cohen et al. 1993, Nelson et al. 1996; general, P. Reinthal pers. comm., A. Cohen pers. comm. 64

CHAPTER n

GEOGRAPHIC VARIATION IN COLOR IN THE BROWNCHEEK BLENNY, ACANTHEMBLEMARIA CROCKERI (TELEOSTEI: CHAENOPSIDAE): CAN THE DIVERGENCE OF SIGNALS USED IN SEXUAL INTERACTIONS PROMOTE REPRODUCTIVE ISOLATION?

INTRODUCTION

Signals used in sexual interactions are expected to be particularly labile and to evolve rapidly (West-Eberhard 1983). They are expected to experience accelerated rates of evolution because of their importance in determining access to critical resources (mates), the absence of a limit to change (except by selection in other contexts), the large number of factors that can initiate trends {e.g., selection operating under different social or ecological conditions, drift, selection for novelty, and others), and the potential for mutually accelerating evolution (West-Eberhard

1983). Intraspecific variation in sexual signals should be particularly effective at facilitating reproductive isolation because the divergent characters are directly involved in the mating process. However, whether naturally occurring variation in sexual signals affects the mating decisions of individuals has only rarely been tested (Andersson 1984).

Chaenopsins are small inquiline fishes that inhabit empty invertebrate tubes and tests. The

17 species in the genus Acanthemblemaria (Blennioidei: Chaenopsidae) are distributed throughout the tropical western Atlantic and the eastern Pacific Ocean (Stephens 1963, Hastings 1990). The species occurring in the Gulf of California have different but overlapping habitat preferences, and are nearly identical in feeding (Kotrschal & Thomson 1986, Lindquist 1985). Morphologically, closely related species in the genus differ most informatively in cranial osteology, especially spination, supra-orbital cirri, cephalic sensory pores and, perhaps most dramatically to human 65

observers, in coloration (Stephens 1963; Smith-Vaniz & Palacio 1974; Lindquist 1975; Hastings

1990; Almany & Baldwin 1996; Hastings & Robertson in press).

Color variation among species is especially evident on the anterior third of the body, and

in the anterior portion of the dorsal fin, in particular (Smith-Vaniz & Palacio 1974; Lindquist

1975; Hastings & Robertson in press). This region of the body is important as a "signal organ"

and is displayed during social interactions (Lindquist 1975). In both courtship and agonistic

interactions, individuals lunge out of their tubes, flare then: median fins and extend their branchiostegal membranes. That color evolves especially rapidly in this body region is particularly clear among the closely related members of the "^hancocki^ species group, which has undergone a rapid radiation in the tropical Eastern Pacific (Hastings 1990; Hastings & Robertson in press).

The browncheek blenny, Acanthemblemaria crocked Beebe and Tee-Van, is sister to the

""hancockr species group, and is the most sexually dichromatic species in the genus (Stephens

1963; Hastings 1990). Males are speckled, while females have large lateral spots. The species is also polymorphic in coloration (Stephens 1963; Lindquist 1980). There are two color morphs, a dark "Gulf form and a red "Cape" form. The Cape form lacks the marked sexual dimorphism of the Gulf form; both males and females have large lateral red spots. Based on these marked color differences, Stephens (1963) regarded the forms as so different that he considered whether they should have subspecific or even specific status. These geographical differences in color raise the question of whether the fish themselves recognize and/or respond to the observed variation.

My goals in this chapter are two-fold: (I) to more fully describe geographic variation in color and (2) to test the effect of this color variation on social interactions between conspecifics. To achieve the latter goal, I use a combination of laboratory and field experiments to test how color variation affects male courtship responses to females and female spawning behavior. 66

Three aspects of these experiments are unusual. First, this study is unique in that it tests the effect of color variation in blennies on the behavior of the fish themselves. Second, I was able to test the behavioral responses of both males and of females. Finally, I was able to conduct the courtship experiments under natural conditions in the field. Thus, I was able to provide an especially robust test of the hypothesis that the divergence of sexual signals should promote reproductive isolation among populations.

METHODS

STUDY SPECIES

Acanthemblemaria crockeri is endemic to the Gulf of California, where it is the third most common rocky shore species (Thomson & Gilligan 1983). The species ranges from Puertocitos to Cabo San Lucas along the Baja California coast, and from Puerto Lobos to Isla San Ignacio de Farallon along the Sonoran and Sinaloan coasts of mainland Mexico (Thomson et al. 1987;

Figure 1.). On rocky outcrops, A. crockeri primarily inhabits vacant vermetid gastropod tubes

(Serpulorbis margaritaceus, Vermetidae) or sometimes barnacle tests {Megabalanus califomicus) in the southern region. In coral heads (Porites califomica), A. crockeri inhabits vacated bur­ rowing mussel {Lithophaga spp., Mytilidae) or clam (Pholadidae) valves. Rarely, the species inhabits vacated polychaete worm tubes (Lindquist 1985; Thomson et al. 1987, pers. obs.). The species feeds primarily on mobile planktonic crustaceans (Kotrschal & Thomson 1986).

Reproduction occurs during the spring and summer (Thomson et al. 1987). Males court females from their shelters by alternately lunging out of and withdrawing into the shelter while holding their dorsal fin erect, expanding their branchiostegal membranes, and flushing a jet black color on their head, anterior body and median fins (Hastings 1988). A receptive females enters the male's tube where spawning and fertilization occur. After depositing the adhesive eggs on the 67

tube walls, the female departs, leaving the male to aerate and protect the eggs until they hatch,

about 3-5 days later (Hastings 1988, Thomson et al. 1987). Brogan (1994) showed that the

planktonic larvae of this species may be retained near their natal reefs.

GEOGRAPHIC VARIATION

Six study sites were chosen to represent the full geographic range of A. crockeri (Figure

1), two from the northern region, Puerto Lobos and Puerto Refugio ("Roca Blanca"); two from

the central region, Isla San Pedro Nolasco ("Bobby's Cove") and Isla Coronado (northwest

comer): and two from the southern region, Isla San Ignacio de Farallon (northeast comer) and

Cabo San Lucas (Chileno Reef). Data were collected during June - August 1992 (all sites but Isla

San Pedro Nolasco) and March 1993 (Isla San Pedro Nolasco). At each site, I collected data that

would enable me to characterize A. crockeri habitat, catalogue their general behavior, and note

their basic morphological characters, and color patterns. I recorded depth, temperamre, and

substrate characteristics at each site. Multiple three-minute predator surveys were conducted to

identity and estimate the abundance of potential predators. Every potential predator to pass within

1 m and within 3 m of prime blenny habitat was recorded, and later combined in the analyses.

Both horizontal (0.3 m x 2 m) and vertical (0.5 m x depth) surveys were conducted to estimate shelter availability, shelter occupancy, and the identity and abundance of potential shelter competitors. All A. crockeri individuals observed outside of shelters were counted.

To characterize the behavior of A. crockeri at the six sites, three-minute focal periods were conducted on each of 20 individuals, 10 females and 10 males. Al Puerto Refugio, an additional 20 focal periods were collected on fish outside of shelters. Data were collected on the average distance (measured in bodylengths) that an individual extended from its shelter when at

"idle" (i.e., not foraging or engaging in social interactions), foraging rates, rates of intraspecific interactions, and the presence of eggs in the shelters of males (determined by observing brief

retreats into the shelter, presumably to fan eggs and confirmed by opening the shelter after the

fish were collected). The intensity of male nuptial coloration was scored in one of the following

color intensity categories, following Hastings (1988): 1 = pale; 2 = brown markings on head

and body somewhat distinct, no yellow on head or pelvic fins; 3 = brown markings on head and

body distinct, yellow on branchiostegal membranes and pelvic fin; 4 = head, especially the

branchiostegal membranes and lower jaw, gray; 5 = head, especially the lower portion, back,

body gray to black. Male courtship behavior was quantified by presenting females enclosed in a clear plastic "whirl-pac" ~ 12 cm from each of 10 resident males for 30 seconds. The time to respond, number of courtship lunges, the distance covered during lunges (measured in bodylengths), and the vertical and horizontal direction of each lunge were recorded. Use of the whirl-pac, an 11 cm x 22.5 cm clear plastic bag, ensures that visual cues from the presentees are available to the resident males. It eliminates out chemical cues, but does not rule out auditory ones, although the latter have never been postulated to occur during mating in blermioids.

At the end of the observation period, all 20 individuals were collected alive. Each fish was immobilized by putting it first in a dilute solution of quinaldine and then transferring it to

50% ethanol. Twenty-one body regions were then immediately scored for color by eye and with the aid of a dissecting scope under sunlight (Figure 2). At each body region, the presence/absence of structural (iridescent) or pigment (melanin and red) colors as well as color pattern (the distribution of color, e.g., stripes, spots, etc.) were recorded. Descriptions of color and pattern character states are described in Appendix B.

Standard length (SL), head length (HL), and head width (HW) were measured with digital calipers. Counts were made of dorsal, anal, and pectoral fin elements and the largest head spine was identified. Each individual was dissected and its reproductive condition identified following Hastings (1991): 0 = thin, accessory organ not evident in males and eggs not evident in females

— ribbon like ovaries; 1 = moderately thick accessory organ evident in males and previtellogenic

eggs evident in females; 2 = thick testes and well-developed accessory organ present in males

and yolky eggs present in females. Each fish was then gutted, and the remainder of the body

chopped into approximately 3mm sized pieces, leaving the head intact. The pieces were washed

three times in 100% ethanol and preserved in 100% ethanol for further analyses of variation in

head spination and for studies of mitochondrial DNA sequence divergence (both smdies are

currently underway). Two additional fish from each site were collected as vouchers; they were

preserved in 10% formalin and later transferred to 70% ethanol.

MALE COURTSHIP DISCRIMINATION EXPERIMENTS

In these experiments, the responses of test males to "native" (same site), "semi-native"

(regional), and "foreign" (different region) conspecifics of both sexes, and "heterospecific"

(another species of chaenopsid) were observed. At the beginning of each series of trials, presentees were put in individual clear plastic whirl-pacs and presented to resident males in a randomized order for 30 seconds at a distance of -12 cm. Trials were conducted both in the field and in the laboratory (on an as available basis between spawning trials, see general laboratory conditions described below) and were conducted as 2-way, 3-way, or 5-way presentations (detailed in each experiment, see table and figure captions).

Native presentees were collected at the same study site as the test males. They were not his immediate neighbors and were collected at least 15 m away from test males. This, however, does not eliminate the possibility that the experimental individuals were familiar with each other.

Semi-native individuals were collected in the central region but not on the same island or mainland site as test males. Foreign individuals were collected at various sites throughout the 70

Gulf of California (detailed in each experiment, see table and figure captions). They were

transponed, by air, car or boat, to Tucson, and then later to the field test site.

Responses of resident males to the bagged fish were categorized as: court = rapid lunges

in and out of the tube with median fins held erect, branchiostegal membranes flared, and usually

accompanied by darkening of the anterior portion of the body; retreat = male retreats back into

the shelter; attack = gaping, extended lunges with mouth agape, and/or biting at the bagged fish;

no response = remaining motionless, alert, at the shelter entrance, neither moving in or out of

the shelter; and mixed = any two or more of the previous behaviors. Each time a male was

presented with a test fish, one of the above scores was recorded.

In each experiment, I controlled for size, breeding condition, and movement among the

presentees. In the field, I controlled for size as closely as possible by eye. However, I was

constrained by the sizes of those fish I had available from each site. I controlled for breeding

condition by collecting and testing fish only when they were actively breeding at their natal sites.

I controlled for motor patterns of presentees by scoring their movement in the bag as 1 =

motionless; 2 = moderate movements, stop and go, swimming back and forth; and 3 = energetic

movement. I excluded from the final tally of presentations any in which the fish were motionless,

and any in which presentees used in a trial sequence differed in their motor pattern score.

Intrapopulation Field Experiment

Three-wav presentations — Isla Coronado. This experiment was conducted on July 20

1992 at Isla Coronado. Three fish — a native female, a native male, and another tube-dwelling chaenopsid — were presented to each of 10 different resident males. In nine tests, the heter- ospecific individual was Protemblemaria bicirrus, and in one test, Acanthemblemaria macrospilus. 71

Interpopulation Field Experiment

Five-wav presentations — Bahfa de los Angeles. This experiment was conducted on 16

July 1994 at Isla Ventana in Bahi'a de los Angeles. Five fish — a native female, a foreign female,

a native male, a foreign male, and another local mbe-dwelling chaenopsin — were presented to

each of 16 different resident males. The foreign fish were collected 29 June 1994 at Chileno reef,

Cabo San Lucas, and paired as closely as possible in size at Bahia de los Angeles with the native

fish chosen for the trials. Although the Chileno fish were some of the largest I could obtain, they

were less robust than the native test fish. The male presentees are shown in Figure 12. The other

tube dweller was a male Coralliozetus micropes.

Interpopulation Laboratory Experiment

Two, three, and five-wav presentations — Laboratory. These presentations were

preformed on an "as available" basis during the course of the laboratory spawning experiments,

25 April - 19 May 1992. Fish were used in these trials between spawning trials and thus the

number of fish involved in a presentation was variable as was the availability of novel males.

Sixteen different males were used. Thirteen were tested once, 2 were tested twice, and one was

tested four times, for a total of 19 trials. Nine trials were performed as 2-way presentations, 4

were preformed as 3-way presentations, and 6 were performed as 5-way presentations. One test

male was from Cabo San Lucas, the remaining 15 males were from Isla Tiburon or San Carlos.

Presentees were from Isla Tiburon, San Carlos, or Cabo San Lucas. Isla Tiburon fish were

collected 10-12 March 1992, San Carlos fish were collected 17 March 1992 at Martini Cove and

on the east side of San Carlos Harbor, and Cabo San Lucas fish were collected 11-13 April

1992. Discrimination trials were mn between native individuals (Tiburon - Tiburon or San Carlos

- San Carlos), "semi-native" individuals (Tiburon - San Carlos or San Carlos - Tiburon), or 72 foreign individuals (Tiburon - Cabo San Lucas or San Carlos - Cabo San Lucas). Acanthem- blemaria macrospilus was used as the heterospecific presentee. Because of the variable nature of

these presentations, they are presented here as a heuristic, rather than a statistical comparison.

FEMALE SPAWNING EXPERIMENTS

General Laboratory Conditions

Ten experimental 20-liter aquaria with a flow-through water circulation system, and four holding tanks, were maintained in the laboratory under natural lighting (Figure 3). Each experimental tank was divided with a permeable plastic partition. Males and females readily inhabited clear glass 1.5 dram vials as shelters and were fed a mixture of flake fish food and live brine shrimp daily.

To ascertain female spawning behavior, I put single females in tanks with varying combinations of males (detailed in each experiment, see table and figure captions). A female's spawning behavior was easy to observe because a receptive female enters a male's shelter and deposits a single layer of eggs within it. I controlled for shelter quality by providing identical 1.5 dram vials. One additional shelter was added to each experimental tank so that shelters were not a limiting resource. Vials were checked daily for the presence of eggs. Once a female laid a batch of eggs, I recorded which male was guarding them, pulled diat vial out of the aquarium and replaced it with a new vial, and the trial was over. I then replaced the female and another trial began. Most experimental females laid eggs approximately every 2-10 days. Females were removed from tanks after 10 days if no eggs were laid. Trials in which vial residency was not settled were omitted from the analyses. 73

Single Female - Single Male Experiment

In these trials, each female was placed in an experimental tank with one male, either a native, semi-native, or a foreign individual. Here, I tested the spawning behavior of females when paired with native (n = 43), semi-native (n = 9), or foreign males (n = 19). Trials were conducted during 23 April - 4 May 1992 (n = I), 13 June - 30 August 1993 (n = 56), and 11

July - 7 August 1994 (n = 14). Twenty-one males (10 from Cabo San Lucas and 11 from the

Guaymas area) and 22 females (6 from Cabo San Lucas and 16 from Caleta Venecia) were used.

Most frsh were used multiple times but always in unique combinations.

Choice Experiment

In the choice trials, each female was placed in an experimental tank with two males. As such, these trials do not nothing to control for the effect of male-male interactions on female spawning and the interpretation of the results from these trials should be made in conjunction with those from the single female - single male trials described above. I ran three types of choice experiments as partial controls: (1) the female and both males from the same site, (2) both males from the same site but the female from a different site, and (3) males and females from the same site but the males differed in size by 1-4 mm (see below). In the experimental trials, the males were from different sites. One male was from the same site as the female, and the other male was from a different site than the female. Most fish were used multiple times. Females and the male pairs were used repeatedly but always and unique combinations.

Size was controlled as closely as possible. Each male was measured at the beginning of the experimental period by placing them in a whirl-pac with a small amount of water and measuring standard length three times with digital calipers to the nearest 0.1 mm. The standard length of each male was considered to be the mean value of the three measurements. Standard lengths of males ranged from 34.0 mm to 44.2 mm. The difference in size between the two males 74 in each choice experiment was generally less than 1.0 mm, and usually less than 0.5 (about 1.5% of SL; analogous to testing the ability of human females to discriminate 1.1" in height of 6' tall men).

These trials were preformed with novel, but experienced (i.e., non-virgin) females, given a choice of males who were permanent residents of the tank. Females and male pairs were used repeatedly but always in unique combinations. A total of 42 trials were conducted. Thirty-seven of these trials were conducted between 13 June and 11 August 1993 and five trials were conducted from 11 July - 30 July 1994. The fish were from Caleta Venecia or Cabo San Lucas.

Nineteen females and 12 pairs of males were used in the trials (15 females and 10 male pairs in

1993 and 4 females and 2 male pairs in 1994). Five females were from Cabo San Lucas and 14 females were from Caleta Venecia. Most fish were used multiple times.

RESULTS

GEOGRAPHIC VARIATION

The six geographic sites differed in physical and ecological characteristics (Table 1).

There was a clear trend, showing an increase from north to south, in water depth, shelter availability, number and color of encrusting organisms, number of potential predators, and the abundance and diversity of potential shelter competitors. At the northern sites, A. crockeri was first encountered in very shallow water, 1 meter below the surface, and was the only common tube-dwelling species. There were relatively few predators; predators were sighted in only one of nine predator watches. Rock cover was not diverse, and tended to be a dull Sargassum brown in color. There were few Serpulorbis tubes present as potential shelters. At Puerto Lobos, A. crockeri commonly inhabited Lithophaga/Pholas burrows in heads of Porites coral. At the central sites, A. crockeri was also first encountered in shallow water. There were up to seven other tube- 75 dwelling species observed. There were more predators at Isia Coronado and Isia San Pedro

Nolasco (x = 0.8 ± 0.5 and 8.3 ± 2.3 per three minute focal period, respectively). Predators were sighted in six of sixteen predator watches. The encrusters on the rocics was more colorful at these central sites with the addition of a number of invertebrate species. At the southern sites,

A. crockeri was first encountered at about 13 m below the surface. At Cabo San Lucas, six other potential competitors for shelters were observed. Potential predators were consistently observed.

Predators were sighted in nine of ten surveys; x = 3.4 ± 1.0 potential predators observed per three minute focal period. Rock cover at these sites was the most tropical in species composition and was the most colorful with an abundant and diverse set of encrusting invertebrates. Shelters were especially abundant at Cabo San Lucas and there were many unoccupied shelters available.

There difference in number of potential predators observed among the northern sites, central sites, and soudiem sites together was not statistically significant (ANOVA, d.f. = 34, F = 1.52, p = 0.2338. Student's t multiple comparisons test. Group A = all sites; however, this is primarily due to the large number of potential predators observed as Isia San Pedro Nolasco, otherwise, there is an increasing trend in predation risk from north to south).

There were striking geographic differences in the behavior of A. crockeri associated with these environmental differences (Table 2). Especially in the northern, but also in the central, pans of its range, A. crockeri was easily observed. Individuals extended far out of their shelters at rest

(1/3 - 3/4 body length) and were sometimes sighted outside of shelters. As a result, there were more conspecific interactions recorded during focal periods, at Puerto Refugio in particular. In contrast, in the southern parts of its range, A. crockeri was much more difficult to observe.

Ninety- percent of the focal individuals at Cabo San Lucas had only their heads protruding firom their shelters. All movements of individuals appeared to be relatively fast, short and furtive. Especially interesting was the population at Puerto Refugio. At this site, there were few

Serpulorbis observed as potential shelters and little Porites either. Barnacles were abundant but

were not occupied by A. crockeri. An additional transect, 2.5 m wide x 3.5m long showed that

64% (86/134) of the population resided in shelters while 36% (48/134) did not. Fifty-five percent

of those fish outside of shelters were female. Those males that occupied shelters but were not the

largest individuals observed in the population and there were females inside shelters. When a fish

in a shelter was approached, instead of retreating, it would often abandon the shelter altogether.

Those outside of shelters perched on small rock promontories and maintained these as territories,

defending them against conspecifics and returning to the same place after feeding lunges (very

similar in appearance to the behavior of triplefins). Individuals outside of shelters took more

feeding bites (x =6.5 ± 1.1) than individuals inside of shelters (x = 1.1 ± 0.3; Mann-Whitney

U test, U = 249, n, = 20, Uj = 20, p = 0.0000). This population, visited in August, appeared

to be late in its breeding cycle relative to other populations. Few males were in nuptial coloration, and those males that were not especially dark (nuptial color scores of 3-4) did not court bagged females placed near the shelter. I saw no evidence of eggs in the territories of males that did not occupy shelters unsheltered males did not court. I revisited this site a year later and found males in shelters defending eggs but found no evidence of eggs, nor of males in nuptial coloration outside of shelters. A large proportion of the males in this population thus appear not to breed.

Breeding was not synchronous among sites (Table 3). Blennies at the northern sites began earlier and ended earlier in the year than those at the southern sites. In general, the courtship behavior of males was similar among sites (small samples sizes preclude statistical treatment of these data; Table 4). When presented with a bagged female, all males lunged repeatedly directly at the female (perpendicular to her body) and at a slight upward angle. Males at Cabo San Lucas, and to a lesser extent those males at Isla San Ignacio de Farallon, tended not to develop the

intense nuptial coloration of the northern sites, nor did they appear to lunge as far, or as often,

or as quickly, out of their tubes during courtship (pers. obs.).

In general, mean size (SL) increased from south to north. For example, at Cabo San

Lucas, adult size ranged from 22.4 - 36.7 mm. In contrast, at Isla San Pedro Nolasco, adult size

ranged from 30.2 - 51.4 mm and at Puerto Lobos, the range of adult sizes was 29.0 - 41.2 mm.

(It is important to note, however, that these data do not represent an unbiased sample of each

population, e.g., the largest individuals were outside of shelters at Puerto Refugio and were not

measured, and thus these standard lengths should not be considered a complete characterization

of the population). Dorsal and anal fin counts increased from north to south (Table 5.). Pectoral

fm counts ranged from 12 - 14 (x = 13) but did not differ statistically among sites (ANOVA,

d.f. = 64, F = 0.94, p = 0.4615).

COLOR

The anterior ponion of the body, and on the anterior dorsal fin, in particular, was the

most variable in color states (Figure 4, Appendix B). Seventeen color states (16 in females) were

recorded for the anterior portion of the dorsal fm alone. Variation included differences presence/absence of iridescent spots, the shape of the pigmented area on the anterior dorsal fm, the pattern at the pectoral-fin base, and the body midline color (Figures 5-8). Individuals differed in the mean number of dorsal fm iridescent spots (ANOVA, d.f. = 37, F = 17.1, p =

0.0000; multiple comparisons based on Tukey's test. Group A = Puerto Lobos, Isla San Pedro

Nolasco, Isla Coronado; Group B = Puerto Refugio; Figure 5). Individuals from Isla San Ignacio de Farallon and Cabo San Lucas lacked spots entirely whereas individuals at Puerto Refugio commonly had, on average 59 iridescent spots, and sometimes over 100. Only in the Guaymas area, from San Carlos to Caleta Venecia, did the majority of individuals have a large melanic spot on the anterior dorsal fin. A few individuals on midriff islands and Isla San Pedro Nolasco also had this spot. Individuals differed in the mean color score for dorsal fin pigmented area, measured in mean number of dorsal fin elements taken up by the pigmented area (ANOVA, d.f.

= 62, F = 5.28, p = 0.0005; multiple comparisons based on Tukey's test. Group A = Cabo

San Lucas, Group AB = San Ignacio de Farallon, Group B = Puerto Refugio, Puerto Lobos,

Isla Coronado and Isla San Pedro Nolasco; Figure 6.). The color and pattern at the base of the pectoral fin (Figure 7) and the posterior portion of the operculum were also variable, and more so in females than in males. The color and pattern of the anterior part of the body midline reflected the geographical polymorphism and sexual dichromatism described earlier by Stephens

(1960) and Lindquist (1980; male midline color scores were consistent within sites and no

ANOVA was calculated; multiple comparisons based on Tukey's test. Group A = Cabo San

Lucas; Group B = Puerto Refugio, Isla San Pedro Nolasco, Isla Coronado. Isla San Ignacio de

Farallon; Group C = Puerto Lobos; midline color scores for females differed within and among sites (ANOVA, d.f. = 35, F = 17.66, p = 0.0000; multiple comparisons based on Tukey's test.

Group A = Cabo San Lucas; Group B = Isla San Ignacio, Isla Coronado, and Isla San Pedro

Nolasco; Group C = Puerto Refugio and Puerto Lobos; Figure 8). The face and head, i.e., the color and pattern of the face and cirri, the presence and overall gross shape of the cheek spot, and the presence of a white tip on the lower jaw — did not vary among sites. The posterior portion of the body was moderately variable. Variation occurred mostly in number of stripes on the posterior portion of the anal and dorsal fins. Males had an additional color state on the pectoral and caudal fins in association with increased melanism expressed during courtship.

Fish from the six geographical sites were identifiable by color states in each of the indicated body regions. The anterior portion of the body, and the anterior portion of the dorsal fin in particular, was not only the most variable in color and pattern, it was also the most

geographically informative. Fish from five of the six geographic sites were identifiable by color

states in this body region (Figure 9, Table 6). Individuals from Puerto Refugio, Puerto Lobos,

Cabo San Lucas and San Ignacio de Farallon showed unique combinations of color states.

Blennies from Isla Coronado and Isla San Pedro Nolasco, the two central sites, had similar color

scores and individuals from these sites were not distinguishable. The face and head, were

monomorphic and geographically uninformative. The color states in the posterior portion of the

body, distinguished three geographic groups. Puerto Lobos was uniquely identifiable, Cabo San

Lucas was uniquely identifiable, and the four remaining states fell out together. Although there

were a number of states recorded in this body region, most populations were polymorphic and

therefore this region was only moderately geographically informative.

MALE COURTSHIP DISCRIMINATION EXPERIMENTS

Intrapopulation Field Experiment

Three-way presentations — Isla Coronado. When presented with a native female, all

resident males responded by courting (Figure 10, Table 7). When presented with a native male,

the most common responses of resident males were either aggression or "no response". One male showed a mixed response, he both displayed aggression and "courted" the male. The most common response of resident males to the heterospecific individual was "no response". One male

"courted" the heterospecific individual and two males showed a mixed response, including both

"no response" and "courtship". When resident males courted native males or heterospecific chaenopsids, they did so with less vigor compared to their courtship of females (Table 7.). They preformed fewer courtship lunges and showed a tendency not to extend as far out of their tube during those lunges. 80

Interpopulation Field Experiment

Five-way presentations — Bahfa de los Angeles. Males from Bahiade los Angeles showed

no difference in their behavioral responses to native and foreign females (Fisher's Exact Test, p

= 0.292; Figure IIa). However, when these males courted foreign females, they did not court

them with the same vigor with which they courted native females (Table 8). They took

significantly longer to respond to foreign females, performed fewer courtship lunges, and did not

extend as far out of their mbes when courting.

Resident males showed different behavioral responses to native and foreign males

(Fisher's Exact Test, p = 0.039; Figure lib; males used in the experiment are shown in Figure

12). The most common response to a native male was aggression. Resident males never

"courted" native males. To foreign males, the most common responses of resident males were either aggression or "counship". The mean number of courtship lunges, and the mean extension during the lunges, were similar to those displaying to foreign females, and less than those displaying to native females (Table 8). The primary response of Bahia de los Angeles males to a heterospecific was "no response".

Interpopulation Laboratory Experiment

Two, three, and five-wav presentation — Laboratory. Laboratory presentations are combined and reported here as a heuristic, rather than a statistical, comparison (Figure 13.). For both males and females, these trials show the ability to discriminate among native, semi-native, and foreign individuals by resident males. The most common response of test males to females from native, semi-native, or foreign populations was to court them. The second most common response to foreign females was to show aggression. Test males never showed aggressive responses to native or semi-native females. To semi-native females, males showed a greater frequency of retreats into their shelters than for females from either native or foreign populations.

In parallel, the most common response of test males to males from native, semi-native or foreign

populations was aggression. The second most common response to foreign males was courtship.

Test males never courted native or semi-native males. The most common responses of test males

to heterospecifics was "no response" or to retreat into their shelter.

FEMALE SPAWNING EXPERIMENTS

Single Male - Single Female Experiment

Females spawned readily with native males, but showed a strong aversion to depositing

eggs in vials occupied by foreign males (Fisher's exact test, p < 0.0001; Table 9.). Ninety-four

percent (49/52) of females paired with native males deposited their eggs in the vial occupied by

the male. In contrast, only 2/19 (10%) of females paired with foreign males deposited their eggs in the vial occupied by the male. One female split a clutch between the male's vial and an

unoccupied vial. The remaining females deposited eggs in their own vials (n = 16) or in an unoccupied vial (n = I). Females deposited a greater number of eggs during viable spawnings

(spawning in the vials of males; mean = 26.14 ± 2.4) than in non-viable spawnings (spawnings in their own, or in unoccupied vials; mean = 14.8 ± 2.4, Mann-Whitney rank sum test, U =

2003, n, = 51, n, = 19, p = 0.0114).

Females from the two sites differed in their pattern of egg deposition. When paired only with a Cabo San Lucas male, 100% (16/16) of the Caleta Venecia females deposited their eggs in their own vial, or in an empty vial, rather than in the vial occupied by a Cabo San Lucas male.

In contrast, when paired only with a Caleta Venecia male, two Cabo San Lucas females deposited eggs in the vials of these males, and one deposited eggs in her own vial. Some of the Cabo San

Lucas males never received eggs when paired with Caleta Venecia females. However, some of 82

these males received eggs within days when paired with native females (e.g., one male received

eggs firom a Cabo San Lucas female on 23 June 1993, but on 28 June 1993, the Caleta Venecia

female with which he was paired deposited eggs in her own vial).

Choice Experiment

There was a highly significant tendency of females to deposit eggs in vials occupied by

native, compared to foreign, males (binomial exact test; p = 0.0005; Table 10). Seventy-one

percent (30/42) of females deposited eggs in vials occupied by native males, 21.4% (9/42) deposited eggs in vials occupied by foreign males, and 7.1% (3/42) in an unoccupied vial or the

female's own vial. There was no difference in the mean number of eggs deposited in the vials of native (25.4 ± 2.89, R = 2 - 60) and foreign males (28.33 ± 5.9, R = 4 - 52; Mann-

Whitney rank sum test, U = 597.0, n, = 30, nj = 9, p = 0.9336). Females from the two sites differed in their pattern of egg deposition. Forty-three percent (4/7) of the Cabo San Lucas females deposited their eggs in the vials of native males whereas 82.9% (29/35) of the Venecia females deposited their eggs in the vials of native males.

Individual Spawning Histories

Females from Caleta Venecia showed consistent preferences for native males and against foreign males over the experimental period. One representative spawning history is illustrated in

Table 11. In choice trials, female "Venecia 38.78" deposited eggs in vials occupied by native males 4 of 5 times. When paired with a single native male, she deposited eggs in the native male's vial 6 of 6 times, yet when paired with a single foreign male, she deposited eggs in her own vial 2 of 2 times. Fewer Cabo San Lucas females were available for these trials, and these females spawned less frequently, and therefore their spawning preferences were more difficult 83

to characterize. One representative history is illustrated in Table 12. In choice experiments,

female "Cabo 34.5" deposited eggs in vials occupied by foreign males in 2 of 2 times. In single

female - single male trials, she deposited eggs in vials of native males 4 of 4 times.

DISCUSSION

Acanthemblemaria crockerishows considerable geographic variation in ecology, behavior,

size, meristics and color. A dine exists from north to south such that individuals at Puerto

Refugio and Puerto Lobos tend to be relatively larger in body size and bolder in behavior (less likely to be found in shelters and engaging in a greater number of intraspecific interactions).

These individuals are strikingly dichromatic. They have the greatest abundance of melanin pigments, and the signal region of the dorsal fin is covered with numerous small iridescent spots.

At the southern sites, individuals tend to be smaller in size. They are shy and retiring in behavior

(less likely to emerge from or leave their shelters and engaging in fewer intraspecific inter­ actions). These individuals have the greatest abundance of red pigments. Individuals firom Cabo

San Lucas occur exclusively in the red-phase color pattern, and exhibit little or no sexual dimorphism in color. The signal area of the anterior dorsal contains no iridescent spots, and differs in the shape of the pigmented area, and the pattern of pigmentation. Individuals in the central Gulf are intermittent in these characters. The pattern of geographic variation is correlated with the number of potential predators, the number of confamilial competitors for shelters, and the availability of shelters, all of which are higher in the central and lower Gulf regions.

Individuals from five of the six sites used in this study were identifiable by unique combinations of color states. Individuals from Puerto Refugio, Pueno Lobos, Cabo San Lucas and San Ignacio de Farallon are identifiable by color states primarily on the anterior portion of the body, and the anterior portion of the dorsal fin, in particular. Individuals from Isla Coronado and Isia San Pedro Nolasco share similar color states, cluster together, and are not distinguish­

able. The posterior portion of the body is only moderately variable. That the anterior portion of

the body is the most variable, and the most geographically informative, is especially interesting

in light of how A. crockeri and most other chaenopsids use this portion of their bodies. This

region of the body, the "signal organ", is displayed when individuals lunge out and in their

shelters, flare their median fins, and extend their branchiostegal membranes during social

interactions.

Variation in color states, such as the number of iridescent spots in the anterior dorsal fin,

the color pattern at the pectoral-fin base, the shape of the pigmented area on the dorsal fin, and

the pattern on the anterior body midline, show a clinal pattern. For many of these body sites,

individuals from northern, central or southern regions share color states, i.e., individuals from sites across the Gulf are more likely to share color states than are individuals from sites along the same shore. Individuals from Puerto Refugio often share color states with individuals from the central Gulf sites, as did mdividuals from Isla San Ignacio de Farallon.

The geographic pattern of character states suggests dispersal by the three, or four, posmlated current gyres in the Gulf of California (the northernmost gulf, an area bounded to the north by the midriff islands and to the south by Loreto and Huatabampo, an area bounded to the north by Loreto and Huatabampo and to the south by Isla San Jose and Topolobampo, and the southernmost gulf; Sverdrup 1941, Brinton et al. 1986, Bray 1988), rather than along shore dispersal. Funher tests of this hypothesis await the results of molecular analyses (currently underway).

Variation in color appears to be achieved by changes in the distribution and abundance of structural (iridescent) and pigment (melanin and red) colors, rather than the occurrence of new pigments or structures. For example, the "green" appearance of the anal fin in individuals from Puerto Lobos appears to be produced by very pale red pigment, appearing almost yellow, being

masked by melanin. Whether this pale red is qualitatively or quantitatively different from the red-

orange visible in the same position on the anal fin of individuals from central sites, or from the

red visible in individuals from the southern sites, requires fiimre biochemical analysis.

The courtship responses of males and the spawning behavior of females were not

uniformly distributed in the field or laboratory. Native females were courted more often by males

and native males received more eggs than foreign males. The results from both field and

laboratory presentations show that resident males are conflicted when presented with unfamiliar

individuals. They court foreign males, and did not court foreign females with characteristic vigor.

The difference in male responses to native and foreign males was stronger than the difference in

their responses to native and foreign females, which is to be expected as selection should favor

males that attempt to mate with females whenever possible. Subtle differences in the behavior of

males to native and to foreign females were evident, however. Males took longer to respond,

performed fewer courtship lunges, and extended shoner distances out of their tubes when courting

foreign females. Moreover, males showed different responses to native, semi-native, and foreign females, suggesting their ability to discriminate. It is important to note, however, that all but one of the males used in these discrimination trials were from central or northern sites (Isla Tiburon,

San Carlos, and Puerto Refugio). Repeating these trials with more males from the southern sites will be reveal whether this is a general trend.

Females showed a strong tendency to deposit their eggs in the vials occupied by native males in both choice and single male trials. The trend is due primarily to Caleta Venecia females who discriminated against Cabo San Lucas males in both choice and single male trials. Moreover, individual Caleta Venecia females varied their response to males at each spawning event. When paired sequentially with native and foreign males, they deposited eggs in vials occupied by native males, and then deposited eggs in unoccupied vials, or ones they themselves occupied, when

paired with foreign males. The spawning behavior of Cabo San Lucas females does not show this

discrimination against foreign males, although sample sizes are smaller. In both choice and single

male trials, Cabo San Lucas females deposited eggs in vials occupied by Caleta Venecia males.

In the choice trials, they deposited eggs in Caleta Venecia male vials more often than with native

males.

Four interrelated explanations for the spawning patterns of females are possible. First,

although I controlled for standard length, males from the central sites appeared to be more robust,

with wider heads and bodies, than males from the southern sites. These trials may simply show

that females are choosing the larger male, regardless of his color, confirming the general results

of Hastings (1988). However, Hastings found that standard length was the most important

predictor of reproductive success, and that condition (the value of the residual from the least

squares regression line of SL and head width) was almost negatively correlated with reproductive

success. Second, males from the southern sites were less active overall than males from the

central sites. They did not develop as dark a nuptial coloration and tended to be less active in the

aquaria (these differences have yet to be quantified from the laboratory data). Male behavior in

aquaria mimicked what I observed in the field. I ensured that fish from all populations used in

the laboratory experiments were in full breeding condition in the field before collecting them.

These may simply be inherent differences between males from these sites. Third, as mentioned

above, the choice experiments, do not control for male - male interactions and females may not

be choosing a mate based on color, but rather choosing the winner of male contests, which may

be decided by size. Male - male interactions may have also affected some of the males in the single male trials. I used some of these males previously in choice trials, and their behavior may

have been affected by their earlier exposure to other male fish. Four, females may show a 87

"sensory bias" for darkly pigmented males, thus both explaining the preference of females from

northern and central sites for native males and the preference of females from southern sites for

foreign males.

In conclusion, distinct geographic differences in color exist among A. crockeri

individuals, especially in the signal organ. In the context of the experiments conducted here, the

behavioral responses of males and females from northern and central sites reinforce these color

differences. However, it is not entirely clear what that discrimination is based upon. These results suggest that the divergence of signals displayed during social/sexual interactions in this species

may be a factor promoting reproductive isolation among geographically distant populations, and may facilitate subsequent speciation. Fumre studies will investigate how intraspecific processes in signal divergence can be used to better understand patterns of diversity at the species level.

• • •

This project was made possible by the generous contributions of many. In particular, I extend a deep debt of gratitude to Phil Hastings for sharing his knowledge, enthusiasm, and insights into blenny behavior with me. I thank D.A. Thomson for introducing me to the Gulf of

California and inspiring a project that would enable me to spend summers exploring the islands.

In the laboratory, I thank Michael Brogan for masterminding the aquarium design and Theresa

Friend and Susan Crowell for assistance during the spawning experiments. In the field, I thank many dive buddies and travel companions, Keith Meldahl for sharing months in the field, and

Tad Pfister, Andy Cohen, Debbie Gevirtzman, and Melonie Stringer. I thank the owners and staff of the Baja Treasure, Naviera Guaymas, for comfort and company during the field discrimination tests. Chris Jaffe provided his photographic skills and patience in the field. Alex Kerstitch was a frequent sounding board for questions. In the molecular laboratory, I greatly appreciate the ongoing assistance of Sonja Peterson. During the final data analysis, I thank Eric Dyreson for 88

his statistical help. Financial support was provided by the National Science Foundation funded

Research Training Grant in the Analysis of Biological Diversification, the Department of Ecology

and Evolutionary Biology and the Graduate College of the University of Arizona, and the Lamer-

Gray Fund for Marine Research of the American Museum of Natural History, New York. This

work was carried out under the stipulations of Instituto Nacional de Ecologia permit No. AOO.-

700."(2). I thank Phil Hastings, Donald Thomson, Wayne Maddison, Judie Bronstein, and Bob

Smith for critical reviews of an earlier draft of this chapter.

SUMMARY

This snidy documents variation in color among six populations of the browncheek blenny,

Acanthemblemaria crockeri, in the Gulf of California, Mexico, and tests the ability of individuals to discriminate among conspecifics on the basis of color. A combination of laboratory and field experiments was used to investigate how color variation affects both male courtship responses to females and female spawning behavior. Fish firom five of the six geographic sites were identifiable by unique combinations of color characters. The anterior portion of the body

(excluding the face and head) were not only the most variable but were also the most geographically informative. This region of the body, the "signal organ", is displayed during social interactions. The behavioral responses of the fish themselves reinforce these geographical differences. In courtship discrimination experiments, males responded aggressively more often to foreign females than to native females, and they courted foreign males. When courting foreign females, they took longer to respond, performed fewer courtship lunges, and extended less out of their shelters during those lunges. In both choice and single male spawning experiments, females deposited eggs in the shelters occupied by native males more often than in the shelters occupied by foreign males. These behavioral responses were strongest in individuals from 89 northern and central sites. These results suggest that variation and divergence in the signal organ, a socially selected trait, may accelerate reproductive isolation among geographically distant populations, and facilitate subsequent speciation. Future studies will investigate how intraspecific processes in signal divergence can be used to better understand patterns of diversity at the species level. 90

FIGURE 1. Study sites. The six main sites used in this study to collect data on geographic variation are shown as circles. The location of specimen collection or field discrimination tests are shown as triangles.

U.S.A. • Tucson, AZ

MEXICO

• Hermosilio

EAST 0 PACIFIC OCEAN A

2 Tropic of Cancer ja a

o Puerto Lobos o Isia San Pedro Nolasco o Puerto Refugio A San Carlos A Bahia de ios Angeles O Isia Coronado A Isia Tiburon o Isia San Ignacio de Farallon A Isia San Esteban A Isia Espiritu Santo A Caleta Venecia La Paz A Punta San Antonio O Cabo San Lucas FIGURE 2. Body regions scored for color and pattern.

"face" "head" "anterior body" "posterior body" 92 FIGURE 3. Laboratory aquaria setup, (a) Flow-through aquaria system; (b) Experimental tank close-up.

B FIGURE 4. The total number of different color states in males (right of the arrow) and females (left of the arrow) recorded at the indicated body region summed over the six geographic sites. If no alternative states were observed, the region was considered monomor- phic and scored a " 1

16,17

2'3

u> FIGURE 5. (a) Mean number of dorsal fin iridescent spots, (b) Mean number of dorsal fin iridescent spots over the species range

23.4 S9.1 59.1

21.3

12.0 20.2

21.7- 18.6 '5^ 0.0

6.8-

0.0'

VO -P". 95

FIGURE 6. Mean color score for dorsal fin pigmented area, measured in mean number of dorsal fin elements taken up by the pigmented area. The general color pattern of the anterior dorsal fin area is indicated in color. 96

FIGURE 7. Mean color score for pectoral-fin base. Males and females share pattern indicated at Puerto Refugio, San Ignacio de Farallon, and Cabo San Lucas. At the remaining sites, this body region is sexually dimorphic. Males show a uniform melanic speckling. Females are variable, some uniform, some with a red spot or outline. FIGURE 8. Mean color score for body midline (1 = faint outline, thin melanic ring around careotenoid center; 2 = reddish- orange/brown, erythrophores covered uniformly with melanophores; 3 = heavy outline, thick melanic ring around careotenoid center; 4 = brownish/reddish-orange erythrophores with very dense melanophore; 5 = brown/pure melanophores). FIGURE 9. Geographically informative body regions. The anterior portion of the body (excluding the head and face) is the most geographically informative; individuals from five geographic locations could be identified by knowledge of the color states in this body region. The fece and head, being monomorphic, were not geographically informative. The posterior portion of the body enabled identification of individuals from three regions. See text for discussion.

vO 00 FIGURE 10. Male courtship discrimination trials: intrapopulation; 3-way field presentations female

• court • retreat E9 attack B rw response • mixed response

male

• court El retreat B3 attack 0 no response • mixed response

heterospedtic

• court • retreat B attack • no response • mixed response 101

FIGURE 11. Male courtship discrimination trials: interpopulation; 5-way field presentations, (a) Responses of males to native and foreign females; (b) Responses of males to native and foreign males; (c) Responses of males to heterospecific individuals. 12 102

Figure Ua 10

8

6

4

2

0 - native female

• court 0 retreat ^attack ^ no response • mixed response

12

10

8

6

4

2

0 - foreign female

• court • retreat ^ attack ^ no response • mixed response native male

• court •retreat @ attack ^no response • mixed response

8

foreign male

• court • retreat ^ attack ^ no response • mixed response 10

Figure 11c 8

0 heterospecific

• court • retreat attack no response • mixed response 105 FIGURE 12. Presentees used in the Bahia de los Angeles field courtship discrimination trials, (a) Bahia de los Angeles male and Cabo San Lucas male; (b) Bahia de los Angeles male (same male as above) and Balua de los Angeles female. Cabo San Lucas female is essentially indistin­ guishable from the Cabo San Lucas male.

A

6 106

FIGURE 13. Male courtship discrimination trials: interpopulation; 2-, 3-, and 5-way laboratory presentations, (a) Responses of males to native, semi-native, and foreign females; (b) Responses of males to native, semi-native, and foreign males; (c) Responses of males to heterospecific individuals. native female

Icourt • retreat Q attack • no response • mixed response

semi-native female

I court • retreat B attack f3 no response • mixed response

foreign female

Icourt • retreat B attack • no response • mixed response native male

I court • retreat Q attack • no response • mixed response

semi-native male

Icourt • retreat B attack • no response • mixed response

foreign male

Icourt • retreat Q attack • no response • mixed response Figure 13c

•-SIiIM! • \ .. . '-V , ,• •

heterospecific court • retreat ^ attack ^ no response • mixed response o VO 110

TABLE 1. Habitat characteristics of study sites.

NORTHERN SITES CENTRAL SITES SoiTTHERN SITES

Isla San Isla San Cabo Puerto Puerto Isla Ignacio Pedro San Lobos Refugio Coronado de Nolasco Lucas Farallon

Depth (m) of quadrats 4.3 2.0 5.0 3.7 12.2 14.8

Shelters occupied (S = Serpulorbis, L = Lithophaga/Pholas, B S, L S S S,C S. L,B S = Megabalanus, C = Chama)

Number of unoccupied shelters available in 4 3 1 2 1 12 2m X .5m quadrat and (L) (L) (S) (S) (S) (S) the type of shelter (S, L, B, C; as above)

Representative number of encrusters (gross measure of algae & 5 6 7-8 7-8 6 6-9 invertebrates) in a 0.5 (n = I) (n = 1) (n = 2) (n = 4) (n = 1) (n = 6) X 0.5m area (number of transects)

Mean number of 0.0 ± 0.2 ± 8.3 ± 0.8 ± 3.4 predators, 3 minute 0.0 0.2 2.3 0.5 ±1.0 focal periods, (number (n = 3) (n = 6) (n = 6) (n = 13) (n = 10) of focal periods)'

Number of other tube dwelling fish species in 1 2 3 7 6 6 area that are potential shelter competitors'

Number of A. crockeri individuals sighted outside of shelters/hour 8.5 258 2.4 1.8 0.3 1.1 (extrapolated) and the (29%) (57%) (79%) (73%) (0%) (89%) percent of these that were female

' Sightings of other potential shelter competitors were estimated from transects and from species list compiled for each site, all dives combined: Protemblemaria bicirris, Acanthemblemaria macrospilus, Coralliozetus micropes, Plagiotremus azaleus, Coralliozetus angelica, Entromaarodus chiostictus, Acan­ themblemaria balanorum, Chanopsis a. alepidota, Hypsoblennius jen/dnsi Ill

TABLE 2. Behavior of focal individuals.

NORTHERN SITES CENTRAL SITES SOUTHERN SITES

Isla San Isla San Cabo Puerto Puerto Isla Ignacio Pedro San Lobos Refugio Coronado de Nolasco Lucas Farallon

Number of focal 20 20 20 20 11 20 individuals

Proportion of focal individuals with only 0.55 0.3 0.7 0.75 0.64 0.90 their heads protruding from shelter

Proportion of time out of shelter (other than 0.0 O.ll 0.0 0.0 0.0 0.0 for feeding)

Proportion of focal periods w/conspecific 0.05 0.7 0.0 0.0 0.0 0.0 interactions

Mean number of 1.1 ± 1.2 ± 0.2 ± 1.5 ± 1.1 2.3 ± 1.6 feeding bites 1.0 1.2 0.4 1.0 ±1.0

Proportion of males 0.7 0.0 1.0 0.6 0.2 0.6 guarding eggs TABLE 3. Preliminary observations on the monthly reproductive condition of A. crockeri at six sites in the Gulf of California, Mexico. Data on reproductive condition were compiled from personal observations in the field, from dissection of specimens in the Fish Collection at the University of Arizona, from dissection of the specimens collected during this study, and from the personal observations of Alex Kerstitch. Within each square, the first symbol indicates whether there was active breeding based on adult condition, and the second symbol indicates whether newly settled juveniles were observed. " + " = yes (adults in active breeding condition or juveniles present); = no (adults not in breeding condition or newly settled juveniles not observed); "?" = no data; "0" = ambiguous {e.g., male acessory organs in breeding condition but ovaries not mature). Data on temperature were compiled from Robinson (1973) and from data recorded in the field.

Temp., oC; yearly range & Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec range during observed breeding Bahfa de 14.4 - 29 los Angeles . ? + - + - + ? + ? + - - 7 . 7 area (14-17) - 26.7

Puerto + + 16.1 -30.0 ? ? ? ? + - + ? + ? ? ? 7 7 ? ? Lobos (19-25) - 26.7 ? ? 17.5 - 30.6 Loreto area ? ? ? ? . 7 + - + ? + + + + + ? - 7 . 7 (20-25.6) - 30.5

Guaymas + 15.8-31 - ? + - + - + ? + + + + + + + ? - 7 area + (15-19) - 31

Cabo San 20.3 - 29.4 + ? . 7 . 7 - 7 + ? + + + + + ? + ? + ? + ? Lucas (20.6 - 27) Isla San 18.3 - 30.3 Ignacio de ? ? 7 7 . 7 + - + ? + + + ? + ? + ? + ? + ? + ? ? - 28 - ? Farallon 113

TABLE 4. Courtship behavior of males during 30 second focal periods.

ISLA SAN PUERTO ISLA CABO SAN IGNACIO DE LOBOS CORONADO LUCAS FARALLON (10-12 June 1992) (12-20 July 1992) (9-11 July 1992) (22-23 June 1992)

Number of focal males 5 10 3 9

Time to respond, 1-4 ± 1.1 4.9 ± 16.0 ± 6.9 9.9 ± 6.7 seconds (n = 5) (n = 10) (n = 3) (n = 8)

Proportion of 100% 100% 100% 75% courtship responses

Mean score for 4.6 ± 0.2 4.5 ± 0.2 4.5 ± 0.0 3.8 ± 0.3 intensity of nuptial (n = 5) (n = 9) (n = 2) (a = 9) color

Mean extension during courtship lunges, 0.4 ± 0.1 0.7 ± 0.0 0.3 ± 0.0 0.5 ± 0.0 body lengths, (number (n = 73) (n = 125) (n=13) (n = 66) of lunges)

Horizontal direction of 3.2 ± 0.2 3.1 ± 0.2 2.9 ± 0.5 2.8 ± 0.2 courtship lunge (see (n = 44) (n = 120) (n = 14) (n = 57) below)

Vertical direction of 4.9 ± 0.1 4.4 ± 0.1 4.3 ± 0.5 4.3 ± 0.1 courtship lunge (n = 69) (n = 144) (n = 66) (n = 14) (see below)

Lenth of courtship <1 <1 <1 <1 lunge, seconds

Total number of 13.6 ± 5.3 14.5 ± 6.4 4.3 ± 2.1 9.4 ± 5.1 courtship lunges/30 (n = 5) (n = 10) (n = 3) (n = 7) seconds

horizontal vertical 114

TABLE 5. Number of dorsal fin and anal fin elements in focal individuals.

ISLA SAN ISLA SAN ISLA IGNACIO CABO PUERTO PUERTO PEDRO CORONAD DE SAN LOBOS REFUGIO NOLASCO 0 FARALLO LUCAS N Mean number 39.3+0. 38.3±0.3 38.6±0.1 38.7±0.2 38.7±0.2 39.4±0.2 of dorsal fin 2 (n=ll) (n=9) (n=15) (n=19) (n=10) elements' (n=20)

Mean number 28.5±0. 27.3+0.3 27.1+0.2 27.7±0.3 27.8±0.2 28.3 ±0.2 of anal fin 1 (n=12) (n=9) (n=15) (n=191) (n=8) elements^ (n=20)

' ANOVA, d.f. = 83, F = 2.85, p = 0.0206; Student-Newman-Keuls multiple comparisons test. Group A = Cabo San Lucas, San Ignacio de Farallon, Isla Coronado, Isla San Pedro Nolasco, and Puerto Refugio; Group B = San Ignacio de Farallon, Isla Coronado, Isla San Pedro Nolasco, Puerto Refugio, and Puerto Lobos. 2 ANOVA, d.f. = 74, F = 2.79, p = 0.0237; Tukey's multiple comparisons test. Group A = Cabo San Lucas, San Ignacio de Farallon, Isla Coronado, Isla San Pedro Nolasco, and Puerto Refugio; Group B = San Ignacio de Farallon, Isla Coronado, Isla San Pedro Nolasco, Puerto Refugio, and Puerto Lobos 115

TABLE 6. Geographically informative and non-informative color states (n = 102 characters). The number of color characters found at only one geographic site, or shared by a group of geographic sites, is indicated. Geographically distant sites that share color characters are indicated by a See Appendix II and text for discussion.

I. Number of geographically informative color characters; 43 A. Number of characters exclusively shared by two or more geographic sites: 27

Cabo + Ignacio 9 Lobos + Coronado + Nolasco + Ignacio + Cabo 8 Refugio + Lobos + Coronado + Nolasco + Ignacio 5 Refugio + Lobos + Coronado + Nolasco + Cabo 3 Refugio + Coronado + Nolasco + Ignacio + Cabo 2 Refugio + Coronado + Nolasco + Ignacio 2 Refugio + Lobos + Coronado + Nolasco 2 Refugio + Ignacio (?) 2 Lobos + Coronado + Nolasco 2 Lobos + Coronado + Cabo 2 Nolasco + Cabo (?) 2 Refugio + Lobos + Coronado + Cabo Refiigio + Lobos + Coronado Refugio + Nolasco Refugio + Lobos Refugio + Cabo (?) Lobos + Coronado + Ignacio Lobos + Coronado Lobos + Cabo (?) Coronado + Cabo Nolasco + Ignacio

B. Autapomorphies (color states supporting, or found only at one site): 16

Refiigio 6 Cabo 5 Ignacio 3 Lobos 2 Nolasco 0 Coronado 0

II. Non-varying color characters (geographically uniform and thus uninformative): 59 116

TABLE 7. Male courtship discrimination trials: intrapopulation; 3-way field presentations (n = 10). This experiment was conducted on 20 July 1992 at Isla Coronado. Three fish — a native female, a native male, and another tube-dwelling chaenopsin — were placed in whirl pacs and presented in a random order for 30 seconds to each of 10 different resident males. In nine tests, the other species was Protemblemaria bicirrus, and in one test, Acanthemblermria macrospilus. Kruskal-Wallis tests were used to compare medians. The p value for this test statistic is based on the chi-square distribution, "n" = number resident males responding.

PRESENTEE

female male heterospecific p

Mean time to respond, seconds' 4.9 ± 0.4 4.0 ;+• 0.3 18.3± 1.0 0.04222 (n = 10) (n = 9) (n = 3)

Mean number aggressive displays 0.0 1.8 :t 0.1 O.C) (n = 0) (n = 7) (n = 0)

Mean number courtship lunges 14.5± 0.6 5.0± 0.0 4.0 ± 1.3 0.031 P (n = 10) (n = 1) (n = 3)

Mean extension during courtship, 0.7 ± 0.8 0.3 ± 0.0 0.7 ± 1.2 0.2892" bodylengths (n = 10) (n = 1) (n = 3)

' "No response" responses were omitted from the statistical calculations. 2 Kruskal-Wallis test, chi-square = 7,449, d.f. = 2 ^ Kruskal-Wallis test, chi-square = 5.951, d.f. = 2 * Kruskal-Wallis test, chi-square = 2.486, d.f. = 2 TABLE 8. Male courtship discrimination trials; interpopulation; 3-way field presentations (n = 16). This experiment was conducted on 16 July 1994 at Isla Ventana in Bahfa de los Angeles. Five fish — a native female, a foreign female, a native male, a foreign male, and another tube-dwelling chaenopsid species — were placed in whirl pacs and presented in a random order for 30 seconds to each of 16 different resident males. The foreign fish were collected 29 June 1994 at Chileno Reef, Cabo San Lucas, and paired as closely as possible in size with the native fish chosen for the experiment. Although the Chileno fish were some of the largest I could obtain, they were nonetheless slightly smaller than the native test fish. The presentees are shown in Figure 12. The other tube dweller was a male Coralliozetus micropes. The categorical responses of resident males to each of the bagged fish is shown in Figure 11.

FEMALE MALE HETERO- SPECIFIC

native foreign P native foreign P

Mean time to respond, 1.5 ± 1.1 6.0 ± 4.6 2.9 ± 2.9 4.1 ± 5.4 0.0041' N.S.2 20.4 ±11.9 seconds (n = 13) (n = 11) (n = 12) (n = 14) Mean number aggressive 1.3 ± 0.6 1.9 ± 1.2 2.1 ± 1.3 0.78153 1.6 ± 0.7 moves (n = 3) (n = 11) (n = 8) (n = 6)

Mean number of courtship 10.1 ± 4.2 5.8 ± 3.8 0.0239^ 3.6 ± 2.7 lunges (It = 13) (n = 11) (n = 6)

Mean extension during 0.6 ± O.l 0.4 ± 0.2 0.4 ± 0.2 0.0489' courtship, bodylengths (n = 13) (n = 11) (n = 6)

'•5 Mann-Whitney U Test 118

TABLE 9. Summary of laboratory no-choice spawning experiments (one male and one female in each trial). "Viable" spawnings refer to eggs deposited in a vial occupied by a male. "Non­ viable" spawnings refer to eggs deposited in a vial not occupied by a male (empty or inhabited by the female). These experiments were conducted during 23 April - 4 May 1992 (n = 1), 13 June - 30 August 1993 (n =56), and 11 July - 7 August 1994 (n = 14). Twenty-one males (10 from Cabo San Lucas and 11 from the Guaymas area) and 22 females (6 from Cabo San Lucas and 16 from Caleta Venecia) were used. Males and females were used multiple times.

NATIVE FOREIGN

Cabo? - Cabod Cabo 2 - Venecia 6 (n = 9) (n = 3) Venecia 9 - Venecia 6 Venecia 9 - Cabo 6 (n = 34) (n = 16) Venecia 2 - Antonio or Nolasco cJ (n = 9)

Number of trials 52 19

Number of "viable" spawnings 49.5 2 Mean number of eggs deposited in 25.4 ± 2.4 45.5 ± 6.5 viable spawnings Number of "non-viable" 1.5 17 spawnings

Mean number of eggs deposited in 6.0 ± 3.0 15.8 ± 2.5 non- viable spawnings 119

TABLE 10. Results of laboratory choice spawning experiments (two males and one female in each trial). "Same" size indicates that the two males differed in standard length by no more than 1mm (and usually less than 0.5mm). "Different" sized males differed in standard length between 1-4 nam.

Male site same same same same Male size same same same different Female site same different same as one same

Number of trials 8 3 42 7

Number "viable" 7 3 39 7 spawnings

Site of mated male, relative to female native foreign 30 native native 9 foreign

Size of mated male, relative to the other = = = 6 larger male 1 smaller

Mean + SE number of 27.0± 13.4 8.3 ± 4.5 native: 386 ±a4 eggs deposited' 25.4 ± 2.9

foreign: 28.3 ± 5.9

Number of "non-viable" 1 0 3 0 matings

Mean number of 11 26.7 ± 13.9 "non-viable" eggs

Experimental fish 7 different 9, 2 different 9, 19 different 9, 7 different?, and year 3 pairs of S; 2 pairs of 6; 12 pairs of cJ; 3 pairs of 6; 1991, 1992 1991 1993, 1994 1991

' Kruskal Wallis test, d.f. = 4, chi-squarc = 9.562, p = 0.0486 120

TABLE 11. Spawning history of female "Venecia 38.78", 13 June - 11 August 1993. Names indicate the geographical site at which the fish were collected and SL, in millimeters.

Date Mated male Unmated male Number of eggs Comments

13 June aquaria established

17 June Cabo 39.8 Venecia 39.9 4

20 June Venecia 38,8 28

22 June Venecia 40.4 Cabo 40.4 23

28 June Venecia 38.8 33 repeat w/eJof 20 June

1 July Venecia 44.08 55

4 July Venecia 37.5 Cabo 37.8 54

7 July Venecia 38.1 2

13 July Cabo 34.5 16 eggs in female's tube

20 July Venecia 41.0 Cabo 41.0 17

24 July Venecia 41.08 40 repeat w/cJof IJuly

26 July Venecia 36.0 Cabo 35.7 22

2 August Cabo 34.8 27

5 August Venecia 38.1 11 121

TABLE 12. Spawning history of female "Cabo 34.5", 13 June - 11 August 1993. Names indicate the geographical site at which the fish were collected and SL, in millimeters.

Date Mated male Unmated male Number of eggs Comments

13 June aquariae stablished

22 June Venecia 37.9 Cabo 37.9 61

24 July Venecia 40.4 Cabo 40.4 18

8 August Cabo 37.9 32

10 August Cabo41.0 10

20 August Cabo 39.8 27

26 August Cabo 37.9 21 repeat w/dof 8 Aug 122

CHAPTER ffl

SEXUAL COERCION AND SEXUAL ALLIANCES: IMPLICATIONS FOR THE EVOLUTION OF ANIMAL MATING SYSTEMS

INTRODUCTION

We need [men] sometimes if only to protect us from other men.

Allison Lurie 1974, The War Between the Tales (cited in Hrdy 1977)

For many species of animals, mating serves more than a procreative fiinction and much more than gametes are exchanged between panners (Wilson 1978). Females are expected to be discriminating among males on the basis of a wide variety of properties, including resources that males actually or potentially hold, their abilities as parents and their genotype (Halliday 1983; reviewed in Andersson 1994). In some animal species, particularly internally fertilized insects and venebrates, aggressive male mating behaviors impose costs on females (Hiruki et al. 1993b;

Amqvist 1995; Campagna et al. 1988; Thomhill 1980, McKinney et al. 1983; Le Boeuf &

Mesnick 1991; Smuts & Smuts 1993) and protection may be a valuable resource that particular males can broker for matings; females that choose to allocate matings to these males effectively exchange sex for protection (Brownmiller 1975; Wrangham 1979; Smith 1984b; Trivers 1985,

Wrangham & Rubenstein 1986; Mesnick & Le Boeuf 1991). Alliances with protective males can be an effective female behavior that reduces vulnerability to aggression from other, conspecific males. It also is a factor to consider in explaining: (1) patterns of female mate choice, and (2) the evolution of a diversity of animal mating systems, including mate guarding, female gregariousness and breeding synchrony, leks, "harems", monogamy, polygyny, and pair-bonding in humans. 123

A female's choice of mates is influenced by environmental, social, physiological, and

phylogenetic constraints (Wilson & Hedrick 1982; Parker 1984; Ahnesjo et al. 1993; Hedrick

& Dill 1993; Gowaty, this volume). However, these constraints have not been systematically examined. This paper suggests that, in some species, sexual aggression is also an important factor constraining female behavior and that, in such simations, protection may be a primary criterion of female mate choice; I call this the "bodyguard" hypothesis of female mate choice. Because protective males defend their own reproductive interests as well as augment a female's ability to survive and reproduce, protective mating alliances may be the best way for certain individuals of both sexes to maximize their fitness, given the prevailing constraints. The goal of this paper is three-fold: (1) to synthesize examples from the literature that are consistent with elements of the bodyguard hypothesis and to suggest that protective mating alliances are widespread among animals, (2) to present data illustrating the effectiveness of protective mating alliances in reducing the rates of aggression against females, and (3) to suggest that protection from male aggression is an important factor to consider in the evolution of animal mating systems.

I begin by reviewing female interests during mating, information that puts the bodyguard hypothesis in context. I explain why the interests of males and females can be asymmetrical and discuss the concept of sexual coercion {sensu Smuts 1992; Smuts & Smuts 1993) which suggests why males may use force against females during mating. I review the costs to females of male aggression and outline the forms of female resistance. I introduce the bodyguard hypothesis in the second section of this paper and explain why protective males can be an especially effective means of reducing female vulnerability to aggression from other males under certain circum­ stances. I detail the assumptions of the hypothesis, present a series of predictions, and suggest critical tests of the hypothesis. In the final section, I review examples consistent with elements 124

of the bodyguard hypothesis and suggest the importance of protective mating alliances in the

evolution of a diversity of animal mating systems.

FEMALE INTERESTS DURING MATING

ASYMMETRICAL INTERESTS DURING REPRODUCTION

In general, the primary limitation on female reproductive success is the production of eggs, and importantly, relatively undisturbed periods of time in which to channel resources into those eggs or young (Darwin 1871; Bateman 1948; Trivers 1972; Gowaty, this volume). Females of many species can store sperm (Smith 1984a) and for others with a long gestation, lactation or incubation period, the time between necessary matings may be months or years. In contrast, males of most species require no such interludes between matings. Males can increase their reproductive success by mating with many females because each additional mating increases a male's probability of siring young (Darwin 1871; Bateman 1948; Trivers 1972). In general, the primary limitation on male reproductive success is access to females.

Asymmetrical interests in mating have two important consequences for females. First, in encounters between males and females, males may be under selection to mate and females may be under selection not to mate. Asymmetrical interests can lead to conflict between the sexes over mating (Trivers 1972; Parker 1979; Hammerstein «& Parker 1987; Clutton-Brock & Parker 1995).

Second, because the number of copulations is generally more important to males, and because males often control access to resources valuable to females, a system of "resource brokering" can emerge (Gowaty, this volume). Females in many species can obtain access to male-controlled resources by copulating with them {e.g., for food, purple-throated Carib hummingbird. Wolf

1975; soldier beetle, McLain 1981; brown capuchin monkey, Janson 1986). 125

BEYOND DARWIN: SEXUAL COERAON AND RESOURCE BROKERING

Darwin (1871) recognized that males can increase their mating success by competing

against other males for access to females and/or by biasing female mating decisions in their favor.

Smuts & Smuts (1993) suggested that one way males can bias female mating decisions is through

the use of force. The authors defined sexual coercion as "the use by a male of force, or threat

of force, that ftmctions to increase the chances that a female will mate with him at a time when she is likely to be fertile, and to decrease the chances that she will mate with other males, at some cost to the female" (Smuts & Smuts 1993:2). The use of force may be directed at females

(behaviors such as forced copulation, harassment and aggressive conditioning) or at their young

(infanticide, in which death of the infant can bring the mother into estrus sooner than would occur otherwise and the infanticidal male may subsequently mate with the female; Hrdy 1974, 1979;

Sherman 1981).

Gowaty (this volume) represents the behavioral mechanisms by which males can bias female mating decisions as a continuum, defined in terms of the consequences for female survival. At one end of the continuum are mechanisms that work directly on females' bodies, or on their young, and that are detrimental to survival (sexual coercion). And, at the other end of the continuum, are mechanisms that bias female mating decisions indirectly (e.g., by exploiting female sensory biases or by brokering female access to limiting resources), mechanisms that may be neutral or beneficial to female survival. Interestingly, if some males in a population force females to mate with them by physical means of coercion, protection can become a valuable resource that other males can use to attract females.

Although I have chosen to focus on male aggression against females during mating in this paper, it is important to note that this is but one aspect of a wide range of affiliative, neutral and conflictive relationships that can be observed between the sexes. Male aggression during mating 126

is not ubiquitous in nature. On the contrary, in many species, male and female interactions during

mating are peaceful and the use of force against females has never been documented. In

populations in which sexual aggression is known to occur, many males never show these

behaviors (Frederick 1987; Hiruki et al. 1993a; Smuts & Smuts 1993; Tang-Martinez, this

volume). Nor is aggression during mating solely the domain of males, for example, mating can

be mutually aggressive (carnivores, Ewer 1973). Female aggression against males during mating,

and other female behaviors that may bias male mating decisions, has received little attention in

the literature and the dynamics of these systems deserve fiirther investigation (see Appendix E).

The use of force by males against females is also not necessarily sexual in nature. Sexual

coercion is a subset of the aggressive behaviors that males may direct at females, for example,

in the context of competition for food or the defense of territory (Smuts & Smuts 1993). Adult

females and young of both sexes can exhibit aggression toward other individuals in these contexts

as well.

TERMINOLOGY

It is difficult to avoid loaded terminology when describing aggressive interactions between

the sexes (see Gowaty 1982). Until the functional significance of an interaction between the sexes

can be determined, I will use the term male "aggression" rather than "sexual coercion".

Preferably, interactions should be described operationally, and I do so below when discussing

case studies. I offer the following definitions of terms:

Forced Copulation — the physical restraint for mating of a non-receptive female. Forced copulation involves actions, such as biting or striking, in excess of that necessary to position a receptive female for copulation and which physically overpower female resistance. The use of force may result in physical injury or death to the female. However, forced copulation also can 127

occur without apparent, or with minimal, injury to the female (e.g., orangutans, Mitani 1985;

scorpionflies, Thomhill 1980; water striders, Amqvist 1995). By definition, females physically

resist attempted forced copulation (but see caveats below).

Harassment — copulation attempts directed at non-receptive females that cause the loss

of biologically meaningful time and energy and may result in physical injury. By definition,

females physically resist attempted harassment. The frequency and the intensity of the disruptions are important for determining whether a male's behavior can be described as harassment. A continuum exists between clear cases of non-harassment and clear cases of harassment and the biologist must make a judgment call to categorize an act of aggression between the sexes. To make that call as accurately as possible, the rate, intensity, subsequent behavior and reproductive consequences of the interaction for both sexes should be taken into consideration. These are difficult data to obtain but they accurately reflect the complexity of interactions between the sexes

(Smuts & Smuts 1993).

Resistance — fleeing and/or struggling to escape male restraint by a non-receptive female.

The functional significance of female resistance is especially difficult to interpret for two reasons.

First, female resistance does not necessarily represent a female that is unreceptive or unwilling to mate. Struggling may represent an aggressive response to another individual in close proximity

{e.g., carnivores. Ewer 1973), a means of attracting other males (e.g., elephant seals. Cox & Le

Boeuf 1977) or a means of mate assessment (although these are less probable in situations in which females risk serious injury; Thomhill 1980). Second, a female may not struggle, despite non-receptivity, in order to reduce the risk of injury (sensu "convenience polyandry"; Thomhill

& Alcock 1983; Amqvist 1995). Thus, resistance by a female may not necessarily indicate a conflict over mating and a conflict over mating may not necessarily cause females to resist physically. In order to distinguish among alternative hypotheses for the function of female 128

resistance, experiments can be designed that, for example, manipulate the levels of male

aggression and test for changes in levels of female resistance (Amqvist 1992).

COSTS OF SEXUAL COERCION FOR FEMALES

Mating requires orchestrating the activities of two different individuals and even in the

most harmonious of encounters there are costs involved in locating mates, in courtship and in the

act of mating (Daly 1978; Sivinski 1980; Sheldon 1993), including the risk of incidental injury and death for females. Females can be killed by males attempting to mate with them at densely

populated breeding sites (e.g., anurans, Davies & Halliday 1979, Howard 1980; dung fiies,

Parker 1970a, 1979; dragonflies, Jacobs 1955) or during the prolonged and mutually aggressive mating observed in some species of well-armed carnivores (Enders 1952; Ewer 1973; Siniff et al. 1979) or dasyurid marsupials and opposum (Y. Cruz, pers. comm. regarding individuals in captive colonies).

In addition to the potential risks involved in matings between males and receptive females mentioned above, aggressive male mating behavior can impose several additional costs on non- receptive females (Table 1). To females, the evolutionary significance of male aggression during mating hinges on the frequency and intensity of aggression as well as the condition of the female.

However, for the vast majority of species, we lack any information on the presence or absence of male aggression during mating and its significance for male or female fitness therefore is unclear (Smuts & Smuts 1993; but see Smuts 1985; Mesnick & Le Boeuf 1991; Amqvist 1989,

1992; Smuts & Smuts 1993; Hiruki et al. 1993b; Sorenson 1994). At present, we are limited to those few studies that explicitly state incidence rates or that explicitly state die absence of these behaviors. 129

The loss of young directly, through infanticide, or indirectly, through disruption of

maternal care, can be a significant cost in terms of female fimess, especially in species with low

reproductive rates (reviewed in Hrdy 1979; Hausfater & Hrdy 1984; Smuts & Smuts 1993;

Hiraiwa-Hasegawa & Hasegawa 1994). The frequency of loss of young due to male aggression

ranges from anecdotal reports to being the primary cause of infant mortality during the study

period. Sixty-seven percent (30/45) of southern sea lions pups at the Punta Norte rookery that do not survive their first season are killed either directly by males, or indirectly, due to mother-

pup separation and subsequent starvation (Campagna etal. 1992). Infanticide by invading males accounts for 27% of cub mortality in lions in the Serengeti National Park (Packer et al. 1990).

In mountain gorillas, 37% of infant mortality is due to infanticide in the Virungas population

(Watts 1989). In grey langurs, 40% of infants present at the time of group take-over were killed by a new male and an additional 35% were killed shortly thereafter (12 different troops in

Jodhpur, Rajasthan, India, Sommer 1994; see Boggess (1984) for alternative explanations of infanticide in this population and Sommer (1994) for discussion).

Female fatalities that are attributable to male aggression during mating also range from anecdotal reports to being the primary cause of adult female monality documented during the study period (reviewed in Le Boeuf & Mesnick 1991; Smuts & Smuts 1993; Hiruki et al. 1993b).

The frequency of female fatalities attributable to male aggression during mating in wild populations have been calculated for only four species of which I am aware. When considered as a function of the aduh female population, documented fatality rates are 0.1% (11/18,837) in northern elephant seals (20 breeding seasons; Le Boeuf & Mesnick 1991), 0.1% (19/-20,000) in California sea otters (21 years; Staedler & Reidman 1994, pers. comm), 5% (1/22) in eastern gray squirrels (1 breeding season; Koprowski 1993, pers. comm) and 14% (8/55) in the endangered Hawaiian monk seal (6 breeding seasons; Hiruki et al. 1993b). These figures are 130 conservative in that they do not take into account females that have been mjured and may die elsewhere or later. When considered as a function of adult female mortality, the si;-^ficance of male aggression relative to other causes of female mortality during the smdy period becomes clearer; rates are 3% (19/706) in California sea otters, 85% (11/13) in northern elephant seals,

86% (14/16) in Hawaiian monk seals and 100% (1/1) in eastern gray squirrels. From these studies and other reports (reviewed in Le Boeuf & Mesnick 1991; Smuts & Smuts 1993; and

Hiruki et al. 1993b) it appears that females may be especially susceptible to serious injury and death by males during mating when the sex ratio is male biased (e.g., during "mobbings"); in sexually dimorphic species; and at high population density. These and other factors hypothesized to increase the risk to females are discussed in Le Boeuf & Mesnick (1991), Smuts & Smuts

(1993), Starfield etal. (1995), and Gowaty (this volume).

It is important to note that some of the records mentioned above and in Table 1 are from studies of captive, urban and endangered species. These smdies suggest even more strongly the potentially negative consequences of unusually high population densities and/or unusually biased sex ratios on females, as well as the potentially negative consequences of reduced access to natural habitat into which wild females could normally escape (e.g., urban waterfowl, McKinney pers. comm.). In one instance, male aggression against females has serious consequences for an entire species. In the endangered Hawaiian monk seal, mobbings, in which adult males injure and often kill adult females and immature seals of both sexes during mating attempts, appear to be limiting population growth (Hiruki et al. 1993a, 1993b; Johanos et al. 1994; Starfield et al.

1995). 131

FEMALE COUNTERSTRATEGIES TO SEXUAL COERCION

An array of behaviors and morphological structures have been hypothesized to ftmction

as mechanisms of female resistance to male aggression during mating (reviewed in Mesnick &

Le Boeuf 1991; Smuts & Smuts 1993; CIutton-Brock & Parker 1995). Few studies, however, have quantified the effect this resistance has on rates of male aggression. Similarly, few studies have tested the proposed fimctional significance of these behaviors and morphologies against alternative hypotheses for their existence (but see Mesnick & Le Boeuf 1991; Amqvist 1992;

Amqvist & Rowe 1995). In this section, my interest is to compare the proposed forms of female resistance and, in particular, to determine those conditions in which protection from mates may be the most effective and/or efficient way for females to reduce the risk of male aggression during mating.

Avoidance/Resistance — The most straightforward mechanism of resistance to male aggression is to avoid interactions with males. Females have been observed to avoid males by hiding, fleeing and struggling (e.g., orangutan, MacKirmon 1971; water strider, Amqvist 1992; tree squirrels, Koprowski 1993; bison, Berger 1994; white-cheeked pintail, Sorenson 1994). Hrdy

(1977) and Smuts & Smuts (1993) suggest that female primates may attempt to avoid potentially infanticidal males by emigrating. Such behaviors can be costly to females in terms of time and energy, the risk of physical retaliation by the male, and the loss of social stams. Avoidance mechanisms are most likely to be effective when the sexes are similar in size, or females are larger, when the female is mobile, and when the female is confronted with only a single male.

When the environment constrains females in their habitat use {e.g., by limiting females to particular oviposition, foraging, or lactation sites), females are predictable in time and space and the ability of females to avoid males is reduced (Amqvist 1995).

Behavioral/Physiological — At present, relatively little is known about a female's ability to control the fate of sperm once it is in her reproductive tract. However, females of many 132 species can selectively destroy, store, transport and reject sperm (insects, Eberhard 1985; birds,

Birkhead & Mailer 1992). In addition, synchronous ovulation, pseudo-estrus, situation-dependant ovulation or abortion may occur as a response to male aggression (primates, Hrdy 1977, Smuts

& Smuts 1993; mountain zebras, Penzhom 1985; lions. Packer & Pusey 1983).

Morphological — Male aggression may have important consequences for the evolution of female morphology (Parker 1979; Clutton-Brock & Parker 1995). Female morphologies suggested to have evolved as adaptations to reduce the costs of aggressive male mating behavior include: the genital spines of female water striders that enable females to repel males more effectively (Amqvist & Rowe 1995); the thicker skin in some species of female sharks and rays that can protect them against male biting behavior during mating (Pratt 1978, Nordell 1994); andromorphic color patterns in a dragonfly and African swallowtail butterfly that reduce the rate of aerial chases and mounts by males (Robertson 1985; Cook etal. 1994); and increased female size relative to males in some species of primates, birds and hyenas (Smuts & Smuts 1993;

Clutton-Brock & Parker 1995; Gowaty, this volume).

Female Coalitions — Females that form coalitions with other females may be able to collectively defend themselves and their young from males. Berger (1986), Smuts (1987a, 1992),

Connor et al. (1992), Smuts & Smuts (1993) and de Waal (1995) discuss the importance of female coalitions in bottlenose dolphins, horses and many species of primates. Female coalitions can mobilize quickly, will attack males that are aggressive toward females or their young and have been observed to kill males (Starin 1981; Rowell 1974). Female coalitions are most likely to evolve in species that live in groups and are long-lived so that benefits can be reciprocated among coalition members.

Alliances with Male Non-mates or "Friends" — In savannah baboons, males may protect their female "friends" and their young from aggression by other males (Smuts 1985). However, 133

there are only rare examples of affiliative alliances in which the females does not subsequently

mate with the male (B. Smuts pers. comm.).

Convenience Polyandry — When females cannot avoid males effectively, females may

respond receptively to male mating attempts (Parker 1979; Walker 1980; Smuts & Smuts 1993;

Amqvist 1995). "Convenience polyandry" (sensu Thomhill and Alcock 1983) represents a trade­

off between the costs of rejecting persistent and/or aggressive males and the costs of mating.

Convenience polyandry describes the behavior of female dung flies (Parker 1979) and predicts

the behavior of female water striders in varying male densities (modeled by Amqvist 1992). It

also has been suggested that females will mate to prevent injury to themselves (e.g., chimpanzee,

Goodall 1986; Hawaiian monk seals, Johnson & Johnson 1981) and, in birds, to prevent injury

to eggs as they sit on their nests (Mineau & Cooke 1979; Fujioka & Yamagishi 1981; Werschkul

1982).

Copulation Solicitation — In lions, tree swallows and a number of primate species,

females are receptive to or solicit copulations from a number of different males (Packer & Pusey

1983; Altmann 1990; Smuts & Smuts 1993). Such situation-dependent sexual receptivity may

reduce the likelihood of male aggression toward females and their young in two ways: by mating with many males in a population, or by mating with invading or replacement males, females might confuse paternity and thereby reduce the threat of infanticide (Hrdy 1977, 1979;

Wrangham 1980, but see Sommer 1994; Robertson 1989) or by inciting male-male competition, and thereby inducing takeover by the strongest male (Packer & Pusey 1983). Subsequently, these males would have the greatest probability of being able to defend the female and her young.

Sexual Alliances — Females that choose to mate with a particular male based on the male's ability to protect the female and her/their young from aggression by other, conspecific males, reduces the probability of male aggression because of the dual effect on male behavior. 134

First, the female reduces potential aggression from her mate by submitting to his mating attempts

(similar to the discussion of convenience polyandry above; but see caveats, below). Second, as

he defends his own reproductive interests, her mate deflects additional males thus enabling the female to forage and/or provide maternal care without disturbance.

Wrangham (1979), Wrangham & Rubenstein (1986), and Rubenstein (1986) suggested the importance of protection from male aggression in the evolution of animal social systems and termed protective males "hired guns". The bodyguard hypothesis that I develop here formalizes the relationship between female mate choice and protective males and expands the concept to include examples from a wide variety of taxa.

THE BODYGUARD HYPOTHESIS

BASIC TENETS

The bodyguard hypothesis proposes that, in those systems in which sexual aggression constrains female activities during reproduction, protection from male aggression: (1) is an important — and, under certain circumstances, perhaps the primary — criterion in female mate choice decisions, and (2) is a factor to consider in the evolution of animal mating systems. I define the bodyguard hypothesis of female mate choice as the following: in those systems in which sexual aggression constrains a female's activities during reproduction, a female may choose to mate with a particular male based on the male's ability to defend her, or her young, from sexual aggression by other, conspecific males. The resulting protective mating alliance is a more- or-less long-term period of interaction between the male and the female during which the female is receptive to mating with the protective male and the male protects his mate (and their young) from other males. The association may last hours (mate-guarding in insects), days (consortships in orangutans), weeks (pinniped "harems") or years (pair-bonding in birds). A male may be able 135 to guard one female (monogamy) or many (polygyny). The guarding occurs during a time critical to the female, for example, during lactation, incubation, nest-building or oviposition, when alternative means of female resistance are infeasible or ineffective.

The bodyguard hypothesis of female mate choice is not purely a behavioral concept but involves a combination of behavioral description and fimctional explanation (Smuts & Smuts

1993). Protective mating alliances cannot be identified solely by the mate choice decisions of females or by observing males guarding their mates. Rather, identifying females that choose mates based on their ability to protect them requires data on the risks to females of male aggression and the consequences that protection has for the reproductive success of fen\ales. It also requires that protection from male aggression be distinguished from the other potential benefits females can derive by their choice of mates and/or from their extended associations with particular males, such as paternal care, access to male-controlled resources and/or the possibility of increasing the genetic quality of offspring. These are difficult distinctions to make but they accurately reflect the multi-fimctional namre of sexual relationships in animals.

If sexual aggression constrains females activities during reproduction, mates are likely to make especially effective protectors because: a) males in many species are better equipped in size and weaponry and have greater strength and fighting ability than females and thus are better suited for combat with other males; b) mates have a larger genetic stake in the offspring com­ pared to other potential allies, such as unrelated females or other males (van Schaik & Dunbar

1990); and c) unlike potential female allies, males are not occupied in reproductive activities such as lactation, oviposition or incubation and, therefore, are available to guard.

Among the males available as mates within a population, females should prefer the naales that offer the greatest benefits (e.g., paternal care; resources, including protection; and/or "good genes"), that impose the least costs on her (Wrangham 1979; Amqvist 1995) and that can 136

minimize the costs imposed by others (Wrangham 1979). Wrangham predicts that this may lead females to prefer males that are dominant over others. Female preference for dominant males can lead to selection for increased size, strength and fighting ability among males, as well as to the evolution of traits that might advertise a male's ability to protect females. FenuJe preference for dominant males can also lead to increased female group size, because the most powerful males may be able attract many females. The situation may be less than ideal, however. Increased male size and strength, and increased female group size, can potentially increase the costs of mating for females either directly, during mating encounters with large and aggressive males, or indirectly, due to disruptive mating attempts by excluded males. Nonetheless, females may prefer an aggressive male as a mate because of the implication that he is an aggressor capable of protecting her and her young subsequently (Wrangham 1979; Packer & Pusey 1983).

Traditionally, the association of mates beyond the time required to fertilize ova have been explained in terms of ecological constraints, for example, the need to acquire resources for the young, to defend the territory or to guard against predators. However, in some systems, intraspecific interactions, and male aggression in particular, may be the primary factor promoting the extended associations of mates (Wrangham & Rubenstein 1986). In these situations, protective mating alliances may represent the most effective way for females to decrease die costs of mating, and to increase the probability of mating and raising young successfully, given the prevailing constraints.

COSTS AND BENEFITS OF PROTECTION

Predicting the evolution of protective mating alliances requires investigating the consequences that protection has on the fitness of both males and females. During reproduction, an individual must decide with whom to mate, as well as how long to remain in association with 137 that mate. These decisions will depend on the individual's physiological condition, the strategies adopted by other individuals in the population, prevailing ecological conditions and phylogenetic constraints. For females, protective mating alliances entail a number of potential costs, such as

(1) the costs of sharing a territory and resources with another individual (and additional females if the male is guarding polygynously, Wrangham 1979); (2) reduced opportunity for free mate choice (Gowaty 1995, this volume); (3) the energetic costs of mating (e.g., water striders,

Fairbaim 1993); and (4) the need to be sexually available and interesting lest the male desert her for other females (B. Le Boeuf pers. comm.). All else being equal, females may be bener off without these extended associations with males (they may be better able to forage on their own for instance, e.g. apes, Wrangham 1979; water striders, Amqvist 1995). However, all else is not always equal. When sexual aggression constrains the activities of females during reproduction, protective mating alliances may represent the "best of a bad situation" for females; an inflicted harmony (sensu Amqvist 1992, 1995).

Protective males can enhance female fitness in a number of ways. The reduced rates of disturbance from other males increases the amount of time and energy a female can channel into young and reduces the probability of potentially dangerous encounters with other males; additional time and energy are also saved because the sexual demands of one male are less than that of several (B. Le Boeuf pers. comm). Protective males may also defend their mates from predators and from disturbances by other individuals of the same species attempting access to sites or resources. If the male is dominant over others, females may also gain access to other male-controlled resources and, to the extent that the traits that confer dominance (e.g., health, size, strength) are heritable, she benefits through enhanced survival of her offspring (at present, there is little empirical support for this assumption, and there are theoretical objections to it, e.g., 138

Fisher 1930, although there is reason to believe that fitness in natural populations has some

heritability; reviewed in Andersson 1994, see also Burt 1995).

By deterring competitors, protective males can enhance their own fitness through

increased opportimities for mating, increased probability of paternity and increased care and

survival of their young. However, for males, protective mating alliances entail a number of

potential costs as well. Protective males have reduced opportunities to seek other females as

mates, and protection can be costly in terms of time, energy and the risk of physical injury during encounters with conspecific males. In populations m which the probability of male aggression

against females is high, protection may benefit female fimess as much as, or even more than, it

benefits male fitness. It is possible that in some situations, males may be forced to modify their

behavior and provide protection because it is the only way to attract mates. It is also possible that there will be situations in which females attempt to deceive males into guarding them and in which males attempt to resist the costs of guarding. At present, I have no direct evidence for these latter speculations (but see Waage 1979; Lumpkin 1981, 1983).

Although males and females (as well as individuals within each sex) may have asymmetrical, or opposing interests in protection, for a certain fraction of males and females, protective mating alliances may be the best strategy for maximizing fitness, given the prevailing constraints (a condition dependent mixed evolutionarily stable strategy, or ESS; Maynard Smith

& Price 1973; Maynard Smith 1978). While my focus in this paper is on female interests in protection, in order to predict the evolution of protective mating alliances in any system, it is necessary to investigate the costs and benefits of protection, to both males and females, within the relevant population parameters. 139

ASSXJMPTIONS AND PREDICTIONS

The bodyguard hypothesis proposes that, in those systems in which male aggression constrains female activities during reproduction, protection from male aggression is: (1) an important criterion of female mate choice and (2) a factor to consider in the evolution of animal social systems. This hypothesis assumes:

1. Sexual aggression is costly to females. Thus, this hypothesis is relevant only to that subset of species in which costly male aggression against females or their young has been demonstrated.

2. Females are guarded by their mates. Thus, this hypothesis is relevant only to that subset of systems in which males guard their mates. The question I address here is not whether males guard their mates but why males guard their mates. And, specifically, whether selection acting on females to reduce the probability of sexual aggression from other, conspecific males can be useful in explaining the existence of mate guarding.

The hypothesis predicts:

1. Females with mates are less vulnerable to sexual aggression from other males. This is the key prediction of the bodyguard hypothesis.

2. The frequency with which females choose mates based on their ability to protect them from conspecific males, and/or the duration of the alliance, will increase as a function of the frequency of encounters with aggressive males. When females are simultaneously exposed to many males while they are engaged in other activities such as incubating, lactating or foraging, they may not have sufficient time or energy both to deflect suitors and attend to their activities.

Thus, protective mating alliances are more likely to evolve in species in which breeding occurs in dense mixed-sex assemblages, when males are mobile and when the environment offers few refuges or hiding places for females (Gowaty, this volume). Likewise, when population density 140

increases or the sex ratio becomes more male biased, protective mating alliances are expected to

increase in frequency and/or duration.

3. The frequency with which females choose mates based on their ability to protect them

from conspecific males will increase as the degree of sexual dimorphism increases. In species in

which male-male competition has led to die evolution of dimorphism in size and weaponry, males

potentially become more dangerous to females. In addition, males also become better suited for

combat with other males and, at the same time, females become less suited to deflect male suitors

themselves. As the physical disparity between males and females increases in magnitude,

protective mating alliances are expected to increase in frequency.

4. The frequency with which females copulate with males based on their ability to protect them and/or the duration of the alliance will increase when other mechanisms of resistance are unavailable or inefficient. A female in good condition is more likely to be able to defend herself from sexual aggression than a female in poor condition. Likewise, when potential female allies are occupied {e.g., lactating or incubating), females may need to turn elsewhere for assistance to deter males. When the condition of the female, or the availability of potential female allies decreases, protective mating alliances are predicted to increase in frequency and/or duration

(see Gowaty 1995, this volume).

5. The occurrence and duration of protective mating alliances will be proportional to the duration of the female's critical time. Because sharing space and resources with a male can be costly for females, females are expected to minimize the duration of their association with protective males to critical times, the time during which she is otherwise occupied and thus is unable to deter males herself. As the duration of the female's critical time increases, protective mating alliances are expected to increase in duration (i.e., from short to long or from temporary to permanent). 141

CRITICAL TESTS OF THE HYPOTHESIS

It is difficult to derive competing predictions that can distinguish the bodyguard

hypothesis firom other hypotheses that attempt to explain why females preferentially mate with

dominant males or from other hypotheses that attempt to e5cplain why males sometimes guard

their mates. This is because the hypotheses need not be mutually exclusive and because at least

some of the predictions can be derived from more than one of the hypotheses (see also Balmford

& Read 1991). Furthermore, different circumstances will motivate individuals differently.

Clearly, female preferences for dominant males and mate-guarding can arise, and be maintained,

by more than one contributing selection pressure; the value of these behaviors can be pluralistic.

The challenge is to determine those factors that contribute to the evolution of these behaviors and

to take into account both male and female interests.

For example, both the bodyguard hypothesis and the male paternity assurance hypothesis

(reviewed by Birkhead & Ntoller 1992) for the evolution of mate-guarding predict that guarding

will increase as population density increases (Table 2). However, the hypotheses differ in

predicting which sex will initiate guarding and tests of this prediction could be used to distinguish

between them (Lumpkin 1981; data that addresses this prediction, although not in species in

which male aggression against females has been documented, is reviewed in Birkhead & Mailer

1992). The important point is that mating traits that have traditionally been interpreted in terms of male benefit may be shaped by female interests, as well.

Likewise, both the bodyguard hypothesis and the "good genes" hypothesis (Trivers 1972;

Zahavi 1975; Hamilton & Zuk 1982; Kodric-Brown & Brown 1984) predict that females will prefer to mate and/or associate with males that are dominant over others (Table 3). At present, it is difficult to assess the "good genes" hypothesis because we have little data on the heritability of components of male fitness (but see Boake 1994). However, in some systems, competing 142 predictions to distinguish between the two hypotheses can be derived by altering the risk of aggression to females and observing subsequent female mate choice decisions (e.g., Amqvist

1992) or by documentation of cheaters (females that associate with protective males but mate with other males; e.g., female dragonflies, Waage 1979).

Protection from sexual aggression has been proposed as a hypothesis and tested against alternatives to explain the evolution of monogamy in gibbons and the evolution of bower-building in birds. Van Schaik and Dunbar (1990) derived competing predictions from four hypotheses to explain the evolution of monogamy in gibbons — male monopolization, reduced predation risk, resource defense and guarding against infanticide. The authors evaluated predictions of the hypotheses by exanaining patterns of male and female home range size, by examining patterns of duetting and by observations of the behavior of widowed females. The authors found that the guarding against infanticide hypothesis was most consistent with their data. The results of their research are described in greater detail below.

Borgia (1995, in press) evaluated six alternative hypotheses to explain the evolution of bower-building (decorated male courtship strucnires comprised of twigs, straw or saplings) in bowerbirds — symbolic nests used to stimulate female reproduction, indicators of male quality

("good genes"), runaway selection for exaggerated male displays, protection from predation, protection from forced copulations by intruding males interrupting courtship at bowers, and pro­ tection from forced copulation by the bower owner himself. Field observations of different bowerbird species, knowledge of their evolutionary relationships (based on a phylogeny derived from mitochondrial DNA sequences; Kusmierski et al. 1993), and experimental manipulations of bowers were used to discriminate among the hypotheses.

Results were not consistent with the hypothesis of protection from forced copulation by

Intruding males (analogous to the bodyguard hypothesis). Bowers do not protect the rear of 143 females and thus fail to discourage attacks by intruding males. In species that have lost bower- building, there was no evidence of adaptations for defense against males attempting to interrupt courtship. Protection from forced copulation by the bower owner himself was the only hypothesis consistently supported by the design of major bower types, by the design of the putative ancestral bower, by observations of male display across species indicating that even highly divergent bower types force the male to run around a wall or maypole (thereby allowing the female an opportunity to leave if she is not ready to mate), and by the compensatory behavior of the two non-bower building species. There was some evidence in favor and more against the remaining alternatives hypotheses (see text for discussion).

In an experiment designed to discriminate between the two forced copulation hypotheses,

Borgia (1995) randomly destroyed one of the two walls in the avenue bowers of spotted bowerbirds. He predicted that to gain protection from forced copulation by intruding males, females should orient with the standing wall behind them. Whereas, to gain protection from forced copulation by the bower owner himself, females should stand facing the wall with the male on the other side. The second hypothesis (protection from bower owners themselves) was supported by two results. First, in 25 of 26 courtships females spent most time facing the wall with the male on the other side. Second, displaying males showed a higher rate of aggressive behaviors when displaying outside the standing wall than outside the destroyed wall. This later result supported the prediction that males adjusted the intensity of their display in relation to the protection available to the female. Borgia (1995, in press) concluded that bowers benefited females by protection from forced copulation by bower owners while bower owners benefited from increased female visitation and thus, from increased opportunities for mating. 144

IMPLICATIONS FOR THE EVOLUTION OF ANIMAL MATING SYSTEMS

This section reviews examples from the literature that are consistent with elements of the bodyguard hypothesis. These examples cover a wide range of taxa (insects, birds, imgulates, lions, pinnipeds, primates and humans) and a diversity of mating systems (mate guarding, female gregariousness and breeding synchrony, leks, "harems", monogamy, polygyny and pair-bonding in humans). My objective in proposing that protection from male aggression is an alternative to consider in the evolution of these mating systems is to focus attention on the similarities among them. In each, male aggression constrains females activities during reproduction and females appear to preferentially associate with, and to allocate matings to, protective males. Protection reduces the probability of aggression from other males, protection increases the female's probability of successfully reproducing, and protection increases female safety during times critical to the female. While I propose that the following systems are similar in fimction for females, they differ greatly in form. The association may vary in duration and, depending on the degree of disparity among males, a male may be able to guard one female or many. By compiling the following examples, I hope to demonstrate the generality of the bodyguard hypothesis across taxa and to encourage tests of its predictions in future studies that seek to explain patterns of female mate choice and the evolution of animal mating systems. All differences in data summarized below are significant at p < 0.05.

EXAMPLES

Ungulate Leks — Most theories for the evolution of non-resource based leks propose that females visit leks to choose among the displaying males and that, as a result, they may gain

(indirect) genetic benefits to the fitness of their progeny (Bradbury 1981; Kirkpatrick & Ryan

1991; Johnsgard 1994). It has also been suggested that female choice of particular males on leks may benefit females directly by reducing the risk of predation or the risk of contraction of disease 145

or parasites (Balmford 1991; Kirkpatrick & Ryan 1991; Clutton-Brock et al. 1993; Andersson

1994). However, there is little unequivocal evidence that lekking females benefit firom discrimina­

ting among potential mates (Balmford 1991; Clutton-Brock etal. 1993; Andersson 1994). Yet,

choosing among potential mates is not necessarily the initial, or the only, benefit of lek-breeding

for females. Wrangham (1980), Clutton-Brock et al. (1988, 1992, 1993), Bradbury & Davies

(1987), and Nefdt (1995) have suggested that in lek-breeding species such as sage grouse,

hammer-headed bats, Uganda kob, Kafue lewche and fallow deer, females in estrus leave densely-

populated mixed-sex foraging grounds to avoid sexual harassment and collect on leks to mate in an area where they can be effectively defended by the dominant males assembled there.

In lek-breeding ungulate species, mixed-sex grazing herds typically lack stable dominance hierarchies and estrous females are frequently chased and courted by several males at the same time (Clutton-Brock etal. 1988, 1992, 1993). Attempts to mate are commonly disrupted and the female's ability to forage and rest at a time when she especially needs the resources for reproduction may be reduced. Infrequently, females are injured or killed. In these species, females migrate to known lek sites only when they are in estrus and spend one or a few days there and, as a consequence, are able to mate relatively undisturbed.

In Kafue lechwe antelope, Nefdt (1995) observed estrous females on leks and in mixed- sex herds. Compared to estrous females on leks, estrous females in herds were chased five times as often (0.5 vs 2.5 chases per hour) and were chased twice as far (4 vs 8 m). Thirty-nine percent of mating bouts were disrupted in herds compared to 18% on leks. Consequently, mean rates of successful mating on leks were elevated compared to the mean rate in herds (0.5 vs 0.17 matings per hour).

In a population of fallow deer, Clutton-Brock et al. (1992) quantified the reduction in disturbance on leks experimentally. The authors observed estrous females on a lek that had begun 146

to allow males to momit them and then gently moved these females off the lek and into the

nearest mix-sex herd. On the lek, the mean chase rate of estrous females was 3 times per hour

and, because of the clustering of territories on the lek, chases never exceeded 50 m in length and

averaged less than 10 m. Off the lek, the estrous females immediately attracted the attention of

nonterritorial bucks. They were chased 12 times per hour. Over half of the chases exceeded 50

m in length and averaged 187 m. Does that were chased immediately ran to the nearest territorial

buck. In over half of the experiments, the does herded off the lek ran in a circle and returned to

the lek. In 4 of 20 trials, does that were being chased by young bucks came to a halt and mated

with one of the juveniles chasing them, an event never observed previously.

Using namrally occurring variation in population density within species of ungulates,

Clutton-Brock et al. (1993) found that lek breeding is observed in populations that occur at high

local density and in which the females have large home ranges, unpredictable movements and do

not live in stable groups. The authors suggested that leks have evolved in ungulate species in

which males cannot economically defend females or resources and where local female densities

are high. In these situations, male disruption of the activity of estrous females increases in

frequency. Males may maximize their mating rate by defending territories in clusters because lek

territories both attracted and retained more receptive females. Females that moved to leks to

breed reduced the rates of male dismrbance and enhanced their ability to survive and reproduce.

Mate-guarding in Birds — In a recent review of the evolution of mate-guarding in birds,

Birkhead and Meller (1992) emphasized the potential reproductive benefits males receive by

reducing sperm competition and gave little weight to the role of females in the evolution of mate- guarding. Although guarding can be costly to females in terms of sharing resources with another

individual and reducing the opportunity for mate choice (Gowaty 1995, this volume; Birkhead 147

& Mailer 1992), it may contribute essential support for female reproduction (Wittenberger &

Tillson 1980; Lumpkin 1981, 1983; McKinney etal. 1984).

In white-fronted bee-eaters, clans live in large colonies of nest holes along African stream

beds and maintain foraging areas that may be located some distance away. Emlen & Wrege

(1986) found that when a female exited her nest chamber alone, she had to run a gauntlet of the

assembled males. Chases were dramatic and frequent events and the female was sometimes

pursued by as many as 12 males. The chases sometimes ended with the female being forced to

the ground and mounted by as many as 6 males. The average female was involved in 6.0 to 6.7

chases, forcibly mounted 1.2 to 1.8 times and forcibly copulated 0.15 to 0.23 times during her

7-day receptive period. It appears that these frequencies would have been much greater were it

not for the behavior of male mates who defended their partners. Before leaving the nest chamber,

females actively solicited this guarding behavior from their mates by uttering vocalizations to

which their mates responded. Females were escorted by their mates on 60% (88/147) of their

travels to and from the colony. Seven percent of escorted females (6/88) were chased compared

to 70% (41/59) of unescorted females; escorts reduced the frequency of sexual chases by 90%.

Similar results were observed in smdies of the common murre (35.2% reduction in chases

when the mate is present, Birkhead et al. 1985) and bam swallows (78.6% reduction in chases

when the mate is present. Mailer 1987). In waterfowl, the dramatic chases and forced copulation

attempts occur most frequently when females are outside the protection of their mates as they fly

to and from the nesting site (McKinney et al. 1983, pers. comm.). Females in other species also solicit guarding by calling to their mates (waterfowl, McKinney 1986; great tits, Bjorklund et al.

1992; cattle egrets, Fujioka & Yamagishi 1981). The risk of chases and forced copulation attempts can train females not to leave without their mates; this may result in constraining a female's behavior with her pair mate (Gowaty 1995). 148

Lumpkin (1981,1983) suggested that female ring doves and female purple martins control

the onset of guarding by soliciting copulations from their mates when it becomes advantageous

to the female to be guarded. In these species, the onset of guarding occurs days before the

female's fenile period, and females may deceive males into guarding them because they benefit

from enhanced protection against predation or by protection from the time-consuming and

potentially harmful courtship of other males (see Birkhead 1981, Davies 1992 and Petrie 1992

for alternative explanations).

Female Gregariousness and Breeding Synchrony in Pinnipeds — Bartholomew (1970)

suggested that the evolution of female grouping, or gregariousness, ui pinnipeds can be explained

by females choosing dominant or territorial males as mates and avoiding copulations with

excluded males. In doing so, females that mate with dominant males presumably increase their

probability of bearing young with attributes indicative of "good genes" because males able to

dominate others are of demonstrated phenotypic quality (but see caveats above regarding the

heritability of components of fitness). Le Boeuf (1972), Le Boeuf & Petrinovich (1974), and

Trillmich & Trillmich (1984) proposed an alternative explanation. In most polygynous species,

females away from the territories of dominant males, whether in estrus or not, are frequently disnirbed by excluded males that attempt to mate with them. The disruptions may be costly to females in terms of time and energy loss, disruption of maternal care, injury or death. In contrast, females who choose to associate with dominant males gain protection from copulation attempts by marginal males. This benefit will act to concentrate females into areas claimed by dominant males. It also may result in selection for gregariousness in species where females otherwise do not derive direct benefits from association with one another and in competition among females for access to dominant males. 149

Female gregariousness can increase female reproductive success. Campagna et al. (1992)

found that in colonies of southern sea lions, dominant adult males keep other males away from

their territories, and diereby indirectly protect pups. Most females of this species breed

gregariously in large colonies with numerous territorial males but some consort with a single

male, forming either small isolated groups or solitary pairs (Campagna et al. 1988). These

solitary breeders formed the basis for a comparison of the relative advantages and disadvantages

of reproducing away from traditional colonies. In contrast to the main colony, only 9% (6/67)

of solitary pair breeding males were large adults. The rest were medium-sized adult males or

subadult males. Females benefited from gregariousness through increased survival of their pups;

only 1.7% (3/172) of pups bom to gregarious females died before the end of the breeding season

(due to infanticide by male abductors), whereas 43.8% (25/57) of pups bom to females in solitary

pairs died before the end of the breeding season.(12 due to starvation after failing to reunite with

their mothers and 13 due to infanticide by male abductors). Both gregarious and solitary females

were exposed to group raids by subordinate males (Campagna et al. 1988) but solitary breeders

faced two additional complications. Solo females bred with subordinate males and the individual

risks from male disruptions were higher because exposure was not reduced by the dilution effect

of female climiping (Campagna et al. 1992).

Boness et al. (1995) found that the frequency of disturbances by males was significantly

greater for female grey seals that bred later in the season than for ones that gave birth at peak season (1.4 v.y 1.9 disturbances per hour). At peak season, the sex ratio was female-biased with

2-4 females per male while late in the season the sex ratio was male-biased with 1 female per

2 males. The authors controlled for possible confounding affects, such as maternal age and size, and found that females that bred late in the season spent 22% less time suckling (5.1 4.0 percent of observation time), had 30% slower growing pups (2.4 vj 1.7 kg/day) and weaned pups 150

that were 16% lighter (54.0 vs 45.6 kg). They concluded that the reduced maternal performance

was likely the result of increased male dismrbances and suggested that this may act to further

synchronize female breeding temporally.

Dominance and Territoriality in Horses — Rubenstein (1986) observed that female horses

that resided with dominant and territorial males suffered fewer disruptions caused directly by

male mating attempts, or caused indirectly by females disturbed by males, than females that

resided with non-territorial males (1.7 V5 5.3 interruptions per hour). The implications for female

fimess were significant: territorial females grazed about nine percent more per hour than non-

territorial females. Summed over the 20-22 hours horses grazed per day, this difference becomes

a feeding gain of about two hours per day. Correlated with the increase in foraging, females that

resided with territorial males had a higher per capita probability of raising foals to one year of age, the age of independence. The maintenance of the mating system benefits both males and females because both benefit ft-om guarding. Males effectively defended their own reproductive

interests and in doing so also augmented the foraging and reproductive success of their mates.

Post-insemination Guarding in Insects — Mates in many species of insects associate well past the time required for fertilization. During the post-insemination period, or passive phase, the male deters the approach of conspecific males through either contact or non-contact guarding. The period of post-insemination guarding varies among species and may last minutes to several days

(Thomhill & Alcock 1983). In a recent review of the evolution of post-insemination guarding in insects, Alcock (1994) emphasized the potential reproductive benefits males receive by reducing sperm competition and also mentioned briefly that little attention had been given to ±e role of female interests in the evolution of guarding. Foster (1967) and Parker (1970b, 1970c) suggested that post-insemination guarding may also be a product of selection on the female because mates deflected interruptions by other males. Post-insemination guardmg enables females to forage 151

longer (water strider, Rubenstein 1984; Wilcox 1984) and to oviposit without disturbance (dung

fly, Parker 1970b 1970c; daraselfly, Waage 1979; water strider, Spence & Wilcox 1986). These

behaviors benefit male interests as well if the eggs she is laying are his or if the food she is

acquiring will nourish his offspring.

In the dung fly, Parker (1970b, 1970c) found that when females ovipositing on dung pies

deflected approaching males themselves, they were involved in an average rejection delay of 2.7

minutes per encounter. At the average density of searching males present on the dung (n = 15),

this rejection delay would involve the female in much more time wasted than full receptivity

because after mating the passive male undertakes the rejection of other males during oviposition.

A fiilly receptive female would save about 50 minutes per oviposition cycle compared to one showing rejection (Parker 1970b). After oviposition, the female initiated termination of the

passive phase by swaying reactions which caused the male to dismount. Parker (1970c) calculated

that males that guarded females after mating gained a 400% selection advantage over males that did not guard their mates. The selection differential of females that were guarded over females that were not guarded was 0.5%. Although the strength of selection is far smaller for females, selection acts in the same direction, favoring the evolution of the passive phase for both sexes.

These figures do not, however, take into account the other potential costs to females of male harassment, such as possible injury to wings (K. Schultz pers. comm.) or being drowned in the liquid dung during mobbings (Parker 1970a, 1979).

Waage (1979) found that territorial male damselflies displayed to and chased conspeciflc males attempting takeovers while their mates oviposited. Especially interesting, however, were

Waage's observations of the behavior of females who had mated previously, either with other territorial males or with non-territorial males. These females sometimes alighted on the territories of males who were guarding their ovipositing mates, resulting in the male guarding the these 152

females as well. The non-mate female then proceeded to oviposit eggs fertilized by rivals on the

male's territory. Constrained by the risk of losing his mate and by the physiological limits to

mating repeatedly, there is little that the territorial male can do to exclude or to attempt matings

with arriving non-mates. Waage concluded that non-mates exploited the guarding behavior of

territorial males without paying the costs of copulating.

Sociality in Non-human Primates and Lions — The social system in some species of non-

human primates and in lions may be explained by the signiflcant measure of protection that

females gain by traveling alone or in groups with males who dominate others and who are able

to protect them and their offspring (Wrangham 1986; Wrangham & Rubenstein 1986; Smuts

1985, 1987b; Packer etal. 1990; van Schaik & Dunbar 1990; Smuts & Smuts 1993; van Schaik,

in press).

Among the non-human primates, orangutans are the only species in which forced

copulations are commonly observed. The orangutan is sexually dimorphic and the most solitary

of the great apes (Galdikas 1981). Birth intervals between successive offspring of individual

females range from 5-7 years. Among adults, the only common form of sociality is sexual

consortship. Females that travel with high-ranking adult males experience reduced rates of forced

copulation by subadult and low-ranking adult males, which otherwise occur at high rates, despite

intense female resistance (Mitani 1985).

Infanticide, documented in lions and in a number of non-human primate species,

represents a significant cost in terms of lifetime reproductive effort for females (Hrdy 1979;

Packer & Pusey 1983; Hrdy & Hausfater 1984; Watts 1989; Sommer 1994). In many species, females can reduce the probability of infanticide by associating with dominant males that are able to maintain high rank throughout the breeding season. Although the most dominant males should attract the most females, feeding competition is expected to limit group size (Wrangham 1979). 153

Monogamy in gibbons (van Schaik & Dunbar 1990) and polygyny in gorillas (Wrangham 1982,

1987; Stewart & Harcourt 1987; Watts 1989), langurs (Hrdy 1974, 1977; but see Boggess 1984),

lions (Packer et al. 1990) and others (reviewed in Smuts & Smuts 1993; van Schaik, in press)

can be better understood by considering the protection females receive when residing with

dominant males that protect their young fi-om infanticide. Within multi-male groups, close female

association with particular males, ("friends"), may also be explained by the protection these

males provide to females and their offspring {e.g.. Smuts 1985; reviewed in Smuts & Smuts

1993).

Van Schaik & Dunbar (1990) tested four competing hypotheses to explain the evolution

of monogamy in gibbons. Traditionally, monogamy has been explained in terms of constraints on the ability of males to monopolize access to more than one female (Emlen & Oring 1977).

Van Schaik & Dunbar were able to reject this hypothesis based on calculations that showed males were able to defend the ranges of (and hence sexual access to) several females. For males, therefore, monogamy must be related to services which substantially increase the female's reproductive output by a factor equivalent to the number of females they could otherwise inseminate. The magnitude of the difference indicated that the service must be essential for the female to rear surviving offspring, making it advantageous for her to be monogamous, as well.

Patterns of duetting and observations of the behavior of widowed females toward new males were not consistent with predictions generated from the "reduced predation risk" hypothesis or the

"defending an exclusive resource" (enhanced foraging) hypothesis but did support predictions of the "guarding against infanticide" hypothesis. To the extent that the predictions could be tested with the data currently available, they concluded that the service provided by males in protecting their young against infanticide was the primary factor promoting the evolution of monogamy in 154

gibbons. Van Schaik & Dunbar (1990) suggested that infanticide avoidance is responsible for the

near-universal occurrence among primates of male-female bonds.

In mountain gorillas. Watts (1989) found that infant mortality is 38% in the first three

years (n = 50 infants) and infanticide accounted for at least 37% of these infant deaths.

Infanticide of "protected" infants (those females and their young that are accompanied by males)

is rare while "vulnerable" infants (infants of unaccompanied females) are almost certain to

become infanticide victims. Vulnerable infants have little chance to escape infanticide unless they

die of disease first or are close to being weaned. Most infanticides (9 of 12 well-documented

"strong cases") occurred when the infants' mothers were not accompanied by their group's

mamre male, because he had died (8 cases), or because the mother had become separated from

him (1 case). The remaining three infanticides occurred when an outside male killed an infant

during encounters between social units that each contained a mature male. Active defense of

mountain gorilla infants by their mothers is ineffective, at least in part, because males are twice

as big as females. In most cases where attacks were observed and/or relevant data were available

afterwards, the mothers were wounded while trying to defend their infants but were unable to

prevent the infanticides. Female/female cooperation in uncommon and avoidance by fleeing may

be impossible for more than a short time. Watts concluded that, although gregariousness reduces

the foraging efficiency of female mountain gorillas, the permanent association with males offers

females the compensatory advantage of male protection against infanticide. It pays a female mountain gorilla to be with a male who can protect her infants well, and assessment of protective ability may be the most important criterion of female mate choice (Wrangham 1979, 1982;

Stewart & Harcourt 1987; Watts 1989). 155

The northern elephant seal, Mirounga angustirostris, is an extremely polygynous and

highly sexually dimorphic species (Le Boeuf & Peterson 1969; Le Boeuf 1972, 1974). At the

onset of the breeding season, males arrive at island breeding sites and compete among themselves

for positions in a dominance hierarchy that confers access to groups of females. One to several

of the highest ranking males reside with a group of females and these males monopolize access

to the females by physically preventing lower ranking males from approaching L.em. At the Ano

Nuevo rookery in California, the groups may contain 1-40 males, 1-1,000 females and their

pups. Depending on their size, these groups may be surrounded by 0-60 subordinate males excluded from access to females by the male dominance hierarchy. Females arrive on the

rookeries pregnant and with a thick layer of protective blubber. They join a "harem", give birth,

nurse their pups and, in the final days of lactation, mate with dominant bulls for 1-5 days (Le

Boeuf 1972, 1974; Cox &. Le Boeuf 1977).

Males are potentially dangerous to females during mating because of their large size

(males are three to four times heavier than females but, in the extreme, a male may be 11 times heavier, 2,200 kg vs 200 kg; Costa et al. 1986; Deutsch et al. 1990, 1994), large canines, and their habit of biting the neck of the female and dropping the bulk of their weight down upon the female's back to facilitate intromission (Le Boeuf 1972, Le Boeuf & Mesnick 1991). The danger to the female is exacerbated because subordinate males, excluded from access to females by the male dominance hierarchy, pursue potential mates en masse when the females depart the rookery for the sea at the end of the lactation period (Le Boeuf and Peterson 1969, Le Boeuf 1972, Le

Boeuf & Mesnick 1991). During her deparmre, a female typically has to run a gauntlet of subordinate males who compete to intercept and mate with her as she crosses the beach between the harem and the water's edge (mean number of pursuing males/female = 8.2; range = 0-30). 156

The potential for injury to females is greatest during harem deparmres because departing

females receive over 20 times more blows, mounts and copulations in a contracted period of time

(on average, less than 30 minutes) as compared to females residing in the harem. And because

the extradural vertebral vein, located at the back of the neck just where males bite and hold

females, is especially susceptible to rupture at the end of lactation when the protective layer of

blubber is at its thinnest. Bleeding wounds were observed on 5 out of every 1,000 females and

1 out of every 1,000 females was killed by a male during her deparmre (Le Boeuf & Mesnick

1991). Thus, the average female that lives 10 years, stands a one in a hundred chance of being

killed by a male during her departure. These mortality rates are minimum estimates. It is very

likely that some female deaths are not counted because they occur in nearshore waters and the

corpse sinks or the female is injured during her deparmre and dies at sea.

Female elephant seals behave in a number of ways that reduce their vulnerability to male

aggression. First, females gather in groups and compete among themselves for central positions

within those groups, behaviors that reduce disruptions by marginal males (Le Boeuf 1972; Le

Boeuf & Petrinovich 1974; Cox & Le Boeuf 1977; Christenson & Le Boeuf 1978). Second, when

mounted by males, females emit a croaking vocalization that attracts the attention of more dominant individuals, who chase the male away, and increases the female's probability of mating

with a more dominant individual (Cox & Le Boeuf 1977). Third, in a study of the behavior of females during their departures from the rookery (Mesnick & Le Boeuf 1991), we observed that departing females moved directly toward the water. Only when onrushing males reached them did departing females stop their forward motion. Typically, males attempting to mount departing females were rapidly and sequentially displaced by more dominant individuals. When males attempted to mount them, most females (64.2%) were "receptive", facilitating intromission by lying quietly and sometimes spreading their hindflippers. Females that responded receptively to 157

male mating attempts received fewer blows to their necks and backs than did females that resisted

(0.5 vs 2.5 median number of blows). "Resisting" females interfered with male attempts at

intromission by attempting to move away, flipping sand backward at the male, closing and swinging hindflippers from side to side and emitting loud vocalizations. Eighty-eight percent

(93/106) of departing females were mounted or copulated, typically with the highest ranking male

in pursuit.

Halting when males approached, combined with sexual receptivity, appeared to be an especially effective means of reducing the potential for injury because of its dual affect on male behavior. First, males did not need to subdue receptive females with bites and blows in order to facilitate intromission. Second, males that were able to intercept and mate with the departing female clearly dominated other males in the vicinity. When the female resumed her movement to the sea, 78% of these males escorted their mates all or part of the way to the water. Escorts deterred other males from approaching the departing female either by their presence alone

(61/105) or by deterring them physically with blows (44/105).

The copulations of departing females were especially interesting because these females were highly likely to have already been inseminated by dominant bulls before their departure (Le

Boeuf 1972, 1974). Females that were receptive to the mating attempts of peripheral males received significantly fewer blows, copulated more firequently and were more likely to be escorted to the sea than females that resisted male mating attempts. Of the escorts that remained with a female from the time they copulated until the time she entered the water. 50% (10/20) copulated with her again (1.7 additional copulations on average). For females, copulating during departures was an effective means of ensuring safe conduct to the sea.

We addressed two alternative hypotheses to account for the ready copulations of depaning females. We considered the hypothesis that these departure copulations were a continuation of 158

mating behavior, behavior that evolved in the context of facilitating copulation with dominant

bulls in the harem. However, the different responses of females to males during departure

suggested that the context altered female behavior. Females were more likely to terminate

copulations and/or to move away from their mates during departure copulations as compared to

harem copulations (90% 10%). Moreover, females were more likely to respond receptively

to males during departures. Sixty-four percent of departing females were receptive to male mating attempts vs 50% of estrous females residing in groups on the day prior to departure. Before onrushing males reached them, departing females often raised and spread their hindflippers, a behavior that facilitates intromission (Cox & Le Boeuf 1977). These data suggested that female behavior during departures was context specific rather than a continuation of behaviors that facilitated matings with harem males.

We also considered the hypodiesis that females were copulating as a means of ensuring fertilization because we do not know when females ovulate nor how virile harem males may be after copulating repeatedly. Recent molecular analyses indicate that not all females are fertilized by the alpha bull (Hoelzel, Le Boeuf. Reiter, Campagna, pers. comm.). We predicted that if departure copulations were a means of ensuring fertilization, as Cox & Le Boeuf (1977) suggested, females (I) would remain in copula as long as possible to facilitate access of sperm to the female reproductive tract, (2) would move toward males during depanures, and (3) would depart at low tide when they would be more likely to encounter and copulate with males. None of these predictions was supported by our data.

It is difficult to design tests to distinguish among these three alternative hypotheses for departure copulations and, in addition, the hypotheses are not necessarily mutually exclusive.

Moreover, different circumstances may motivate individual females. As Cox & Le Boeuf (1977) 159

emphasized, the important thing is the effect of the female's behavior on nearby males. By

copulating with peripheral males, females effected safe conduct to the sea.

PAIR-BONDING IN HUMANS

Cultural and Biological Influences on Human Behavior — In preface to this section on

humans, it is important to take into account both the similarities and the differences between the

behavior of humans and the behavior of odier animals. First, compared to most other species of animals, behavioral traits in humans are more likely to arise through the processes of cultural evolution. Culmral evolution (the transmission from one generation to the next, via teaching and imitation, of knowledge, values and other factors that influence behavior, Boyd & Richerson

1985:2) is pervasive in the human species and proceeds much faster than biological evolution because of the strong human capacity for learning (Cavalli-Sforza & Feldman 1981; Boyd &

Richerson 1985). Biological evolution is, however, largely responsible for the adaptiveness of the cognitive processes that permit culmral evolution to occur (Papaj 1993). Second, the evolved capacity to respond facultatively depending on context clearly reaches its apex in humans, as evidenced by the great range of variation in social interactions we express within and among populations (Smuts 1995). These two traits, as well as many other kinds of evidence, emphasize that human behavior can be culturally-influenced, variable and multi-flmctional while, at the same time, consistent with the predictions of evolutionary theory (Daly &. Wilson 1983; Smuts 1992,

1995; Wilson et al., this volume).

Third, female humans, as with females of other species, sometimes encounter sexually aggressive males. Here, I focus not on the causes of this aggression (the issues raised by this question have been reviewed extensively elsewhere, e.g., Brownmiller 1975; Dworkin 1981;

Shields & Shields 1983; Thomhill & Thomhill 1983; Bleier 1984; Russell 1984; Pausto-Sterling 160

1985; Ellis 1989, 1993, in review; Hubbard 1990; Smuts 1992, 1995; Tang-Martinez, this volume; Wilson et al., this volume) but rather on the behavior of females within a social environment that can be dangerous. In particular, I consider the role that protection from aggres­ sion by other males (non-mates) may play in the evolution of pair-bondmg in humans.

Pair-bonding — Most human societies typically recognize the existence of the sexual pair-bond (long-term, more-or-less exclusive mating relationships; pair-bonds may be monogamous, serially monogamous or polygamous) and give it formal sanction (van den Berghe

1979; Buss &. Schmitt 1993). Cross-culmral smdies as well as reconstructions of human evolution tend to focus on the importance of resource exchange and intergroup competition in the evolution of pair-bonding {e.g., Alexander & Noonan 1974; Symons 1979; Lovejoy 1981; Tanner 1981;

Zihlman 1981; Pilbeam 1984). However, Brownmiiler (1975), Alexander and Noonan (1979),

Smith (1984b), Smuts (1985, 1992), van Schaik & Dunbar (1990) and Gowaty (1992) have suggested that sexual coercion may play a significant role as well. Smuts (1992) hypothesized that pair-bonds benefited females initially because of the protection mates provided against other males

(including protection from infanticide). Brownmiiler (1975) premises her book on rape and the origins of the lawful possession of women by men, with this descriptive passage:

One possibility and one possibility alone, was available to woman. Those of her own sex whom she might call to her aid were more often than not smaller and weaker than her male attackers. More critical, they lacked the basic physical wherewithal for punitive vengeance; at best they could maintain only a limited defensive action. But among those creatures who were her predators, some might serve as her chosen protectors. Perhaps it was thus that the risky bargain was struck. Female fear of an open season of rape, and not a namral inclination toward monogamy, motherhood or love, was probably the single causative factor in the original subjugation of woman by man, the most important key to her historic dependence, her domestication by protective mating. (p. 16) 161

Pair-bonding is a risky bargain, however, and there are at least five important and

potentially costly consequences for women. First, women become vulnerable to aggression from

their mates (Chagnon 1977; Russell 1982; Koss et al. 1987; Wilson 1989; Wilson et al., 1993,

this volume; see Smuts 1992 for discussion). The risk to women of many forms of sexual

aggression has been found to be as high, or higher, from current or past mates (spouses,

common-law mates or live-in parmers) than firom acquaintances or strangers (Russell 1984; Koss

etal. 1987; Wilson etal., this volume). Second, female mate choice may be restricted, depriving

women of access to resources or potential genetic benefits from other males (Gowaty 1992).

Third, the namral expression of female sexuality may be constrained because of the negative

sanctions that promiscuity brings upon women (Smuts 1992). Fourth, the female must be sexually

available to her mate lest he desert for other females (one of the explanations for the evolution of concealed ovulation/continuous estrus in humans; Alexander & Noonan 1979, Symons 1979,

Strassmann 1981, Fisher 1982). And fifth, the female (and her kin) may have to support the male economically (K. Hill, pers. comm.).

Despite these costs to females, the persistence of pair-bonding suggests that there is a net advantage to female fitness. As indicated earlier, there are many benefits females can derive from extended associations with mates that can significantly enhance female fitness, e.g., paternal care, access to male-controlled resources and protection from other individuals (be they male, female or young) that may threaten a female or her young for any reason; the function of pair-bonding for both females and males is clearly pluralistic. Here, I address the hypothesis that one of the benefits human females derive from pair-bonding is protection from sexual aggression by other males. Identifying the importance of protective mating alliances to the fitness of women (and their young) is one facet toward our understanding of the origins, evolution and variability of pair- bonding among human populations. In this greater endeavor, we need not only to consider the 162

initial and subsequent costs and benefits to females of pair-bonding (including the ones mentioned

here), but also to consider the initial and subsequent costs and benefits to males of pair-bonding

(including the costs and benefits of providing or not providing protection) and to consider the

social conditions (including the possibility of male aggression against females) that may have

constrained the behavior of our human ancestors (see van Schaik & Dunbar 1990; Smuts 1992).

Before proceeding, it is also important to note that today, a variety of behaviors are

effective in reducing female vulnerability to sexual aggression, mcluding enhanced political power

that supports the sexual rights of women, education for both males and females about issues of dominance and control, enforcement of laws against sexual assault, rehabilitation work with

offenders, self-defense and protective alliances with females, kin and men (Koss & Harvey 1991;

Smuts 1992). The use and the effectiveness of particular behaviors varies not only within human

populations but also geographically and temporally, dependmg on culmral beliefs, on individual circumstance and on residence patterns and the relative strengths of the bonds between women, men and kin that determine the availability of support (see Smuts 1992; Smuts & Smuts 1993).

Here, I address two elements of the bodyguard hypothesis. (1) Do women prefer to allocate matings to men that demonstrate their ability to protect them? And, (2) are women (and their young) with mates less vulnerable to aggression from other men? At present, there are no data available to test these questions directly. My goal in presenting the following data is not to attempt a definitive assessment of the bodyguard hypothesis, but rather to review the available data, suggest methodologies and to encourage fumre studies.

Although there is much data to support the contention that women prefer to mate with men that can demonstrate their ability to acquire resources (via indicators such as wealth, status, age and size; Buss 1989, 1994), men that would be better able to protect women, the explanation for this pattern is confounded by the many other resources women can gain from associating with 163

such men. I am aware of only one study that has considered the value of protection from male

aggression, among other criteria, in female mate choice decisions. Buss & Schmitt (1993)

hypothesized that one function of short-term mating (casual sex) is protection from other sexually

aggressive men. They predicted that women would value attributes such as physical size and

strength in short-term mates more so than in long-term mates (a committed relationship) in which

other attributes become more important (Buss 1989, 1994). In their survey of 73 young American

women and 75 men, the characteristic "physically strong" was rated on its desirability among

long-term and short-term mates. Consistent with their hypothesis, women placed greater value

on physical strength than did men and, furthermore, women placed greater value on physical strength in short-term mates than in long-term mates, despite women's generally higher standards overall for a long-term mate. To more directly assess the value that both women and men put on

protection in mate choice decisions. Buss's interview methodology could be expanded to include

individuals of both sexes and could be modified to include behavior-specific questions associated with eliciting protection and with providing protection in social contexts that differ in the degree of risk to women of sexual aggression. For example, building upon the differences found cross- culturally in the occurrence of sexual aggression against women (Sanday 1981), a study ranking the value of protection compared to the value of other criteria in the mate choice decisions of women is one possible approach. Similarly, men could be queried regarding the time and energy they invest in protection of mates in varying social contexts.

Women appear particularly susceptible to aggression from men, including sexual haras­ sment and rape, when a mate is absent (either because the female is unmated or because her mate is unavailable or unable to protect her). Data suggesting that women with mates are less vulnerable to sexual aggression from other men may be found in a variety of contexts. In the

Yanamamo (a Brazilian forest people known for high levels of competition between groups for 164

access to women), if women are alone in the forest, they may be attacked, raped, and abducted

by males from other groups. Consequently, before leaving, females provoke their mates into demonstrations of power so that other males will not attack them (Chagnon 1977). Smuts (1992)

illustrates the special vulnerability of "unattached" women by the existence of words such as

"wliyya" which means "under the protection" among the Awlad'ali Bedouins (Abu-Lughod 1986) and by laws which do not punish acts of sexual aggression against women without mates {e.g., the Azandes, Sanday 1981). Data documenting the elevated frequency of rape during war pro­ vides dramatic evidence that women are highly vulnerable to attack when the social barriers to rape are disrupted, when traditional protective alliances are disturbed, and when men, includmg mates, are absent, dead, or are unable to defend women against invading forces (Brownmiller

1975; Shields & Shields 1983; Dickemann 1984).

Crime victimization studies, conducted in the United States, Canada and Great Britain, frequently include marital status as a socio-economic control variable. Although these smdies were not designed to test the questions posed in this paper, an interesting pattern emerges from these data even when confounding variables, such as the age of the victim, the relationship of the victim to the perpetrator, and the sensitivity of the questioning are controlled. Based on a nationally representative survey entailing about 400,000 individual interviews, the United States

Department of Justice's National Crime Victimization Survey spanning the years 1987-1991

(Bachman 1994), found that women who had never been married or were divorced/separated

(thus single, but older) showed higher rates of rape within the preceding six months than women that were married or widowed (2.9 and 2.8 as compared to 0.3 and 0.3, respectively; rates of victimization are reported as the average annual rate per 1,000 females age 12 and older; see

Belknap (1987) for statistical analyses of National Crime Survey data, in all analyses, marital status appears to be the strongest predictor of risk of non-spousal rape for women 18 and older). 165

From interviews conducted in 1972 with about 250,000 persons in 13 major cities in the United

States, Hindelang & Davis (1977) found that single women and divorced/separated women showed higher rates of rape compared to married and widowed women (650 and 486 compared

141 and 91, respectively; rates of victimization are reported per 100,OCX) females 12 years of age and older). The high percentage of rapes of single women in these studies is partly due to the high incidence of rape of young females. However, after excluding females age 16 or younger from their study of rape victims at Boston City Hospital, Burgess & Hohnstrom (1974) found that

82.6% (76/92) of rape victims were single, divorced, separated or widowed. Russell (1984) reports that when rapes by husbands are identified and then excluded from her 1978 survey of

930 randomly selected adult female residents of San Francisco age 18 and older, 85% of the victims of rape or attempted rape were found to be single at the time of the assault and 15 % were married. Sexual aggression against women often goes unreported. In a recent survey designed specifically to address problems with the design and the scope of traditional crime victimization studies, Johnson & Sacco (1995) conducted phone interviews with 12,300 Canadian women, 18 years of age and older. Johnson (unpub. data) found that a greater number of single, separated and divorced women reported non-spousal sexual assaults (ranging from unwanted touching to rape) during the previous 12 months than did married, common law or widowed women (16.7%

(306/1,833), 13.1% (32/245) and 11.8% (101/859) as compared to 2.5% (184/7,396), 8.0%

(82/1,022) and 1.4% (13/902); a similar pattern was found when the data were analyzed independently by the relationship of the perpetrator to the victim — stranger, date/boyfriend or other known (non-spouse) male. Using the same data set, Rodgers & Roberts (1995) found that a greater number of women reporting multiple victimizations (of which at least one was in the past 12 months) were single, separated, or divorced compared to women that were married or in common law relationships (33% [316/960]) and 23% (129/563) compared to 9% (239/1,654). 166

(Note: no statistical analyses were available for the preceding studies). Using a logistic regression analysis, Rodgers & Roberts controlled for demographic variables (age and income) and non- demographic variables Gifestyle, exposure, proximity, guardianship) and found that in all cases of non-spousal multiple victimization, whether perpetrated by strangers or other known males, single, separated and divorced women showed statistically significantly higher rates compared to women who were married, widowed or in common law relationships.

Married women appear to be sexually harassed in the workplace less often than single, widowed, separated or divorced women. Terpestra & Cook (1985) found that of 76 American women who filed sexual harassment complaints, single women were significandy over-represented

(43% of complaints vs 25% in the labor force) and married women were significantly under- represented (31% of complaints vs 55% in the labor force). The U.S. Merit Systems Protection

Board (1981; cited in Terpestra and Cook 1985) reported that 53% of single women had experienced sexual harassment on the job within a two year period, compared to 37% of married women. Schneider (1982; cited in Smdd and Gattiker 1991) found that 45% of single, separated and divorced respondents reported incidents of sexual harassment within a 12 month period, compared to only 31% of married women. Lafontaine & Tredeau (1986; cited in Studd &

Gattiker 1991) found that single and divorced professional women experienced higher frequencies of all forms of sexual harassment for which they had adequate data.

The studies described above are confounded by a number of factors, however, including:

(1) biases In reporting and recording incidences of sexual aggression in humans are numerous and, in panicular, incidences involving married women are under-reported (Hindelang & Davis

1977; Russell 1984; Koss 1992, 1993; but see Gartner & Macmillan 1995; Johnson & Sacco

1995); 2) victims of rape and sexual harassment tend to be young and are therefore less likely to have mates (Hindelang & Davis 1977; Shields «& Shields 1983; Thomhill & Thomhill 1983; 167

Russell 1984; Studd & Gattiker 1991; Wilson etal. 1993); (3) men tend to attack women when

they are alone (meaning that it may not be the presence of a mate, per se, but simply the presence

of another individual — male or female, mate or non-mate — that reduces female susceptibility);

and (4) single women show higher victimization rates for all types of violent crimes (Katz &

Mazur 1979; Bachman 1994; Rodgers & Roberts 1995; reviewed in Belknap 1987). The

following studies do, however, suggest methodologies for designing fumre tests. For example,

to control for age affects, a victimization survey designed sensitive to reporting biases and that

specifically excludes incidences perpetuated by mates, can be analyzed by age to better isolate

the relationship between marital status and rates of sexual aggression perpemated by non-mates

(see Rodgers & Roberts 1995; Wilson & Mesnick, this volume). If a correlation is found between

marital status and rates of sexual aggression, further empirical research will be necessary to

determine the causation for the observed patterns. A correlation could be due to the physical

protection of women by their mates, or indirectly, due to differences in lifestyle, in the amount

of time spent in public places and/or in the amount of time spent alone. These, and other

alternative explanations, will need to be identified and their affects on the observed patterns tested

{e.g., Rodgers & Roberts 1995).

Alexander & Noonan (1979), Van Schaik & Dunbar (1990), and Smuts (1992) suggested

that protection of young from aggression by conspecific males may be an important factor in the evolution of pair-bonding in humans. In humans, and in contrast to other non-human primates,

infanticide appears to be most commonly committed as a parental manipulation tactic (Alexander and Noonan 1979; Dickemann 1984; Hrdy & Hausfater 1984; Hill & Kaplan 1988). Dickemann

(1984) attributes this pattern to the effectiveness of the pair-bond as a protective system against other conspecific males. However, there are examples in several cultures of men (as well as women) killing children sired by other individuals (reviewed in Daly & Wilson 1984; 168

Schienfenhovel 1989; Daly & Wilson 1994; Wilson & Daly 1994; during times of war,

Dickemarm 1984). Because human males invest heavily in their young and because human

females have relatively long interbirth intervals, it is important for a male to ensure that he is

investing in his own young, and to terminate investment when ever he is led to believe he is not

the father (van Schaik & Dunbar 1990). One way to terminate investment is to kill the offspring.

The death of the child may hasten ovulation in the female and may increase the maternal

resources invested in his own young (Alexander & Noonan 1979; van Schaik & Dunbar 1990;

behaviors consistent with the theory of sexually selected infanticide, Hrdy 1974, 1979; Sherman

1981).

The following studies provide circumstantial evidence that children reared with their

biological fathers are less vulnerable to infanticide by other males. Van Schaik &. Dunbar (1990)

point out, however, that such data do not enable us to distinguish between the hypotheses that

pair-bonding evolved because male help is essential for the female to rear her offspring

successfully (with infanticidal protection as an incidental benefit) and the alternative, that pair-

bonding initially evolved to prevent infanticide (with male care appearing subsequently as an

additional benefit).

In reviews of the ethnographic materials in the Human Relations Area Files adulterous conception/or siring by a previous husband or non-tribal male was given as one of the reasons for infanticide in 16 of the 39 societies in which infanticide had been recorded (n = 60 societies;

Daly & Wilson 1984, see also Schiefenhovel 1989). Daly &. Wilson (1988a) reviewed homicide rates for children raised within genetic and stepparent homes. In Canada, from 1974-1983, step­ children are approximately 65 times more likely to die within the first two years of life than children living with both their biological parents. And in the United States in 1976, a child living with one or more step-parents is approximately 100 times more likely to be fatally abused than 169

a same-age child living with both genetic parents (see Wilson & Daly 1994 for additional smdies

showing similar results). Homicides by step-fathers far outweigh those by step-mothers in these

studies (note, however, that men are more likely to kill than women in most contexts; Daly &

Wilson 1988b). Differences in vigilance and supervision, socioeconomic status, maternal age,

family size or personality characteristics of the abusers do not appear to account for the observed

patterns (see Daly & Wilson 1988 for review). Evidence also indicates that abusive stepparents are discriminating, sparing their own children within the same households (Daly & Wilson 1985).

Data were not available to test the differences between the fates of children raised in stepmother and stepfather homes.

These studies suggest that the pair-bond (with the biological parents) can be an effective protective system against sexual aggression and infanticide and may be an important factor enhancing the fitness of women, their mates and their young. However, the role of protection in the mate choice decisions of human females, and in the evolution of pair-bonding, remains to be critically tested.

CONCLUSIONS

Sexual aggression affects the lives of females in numerous ways. But this does not imply that females are helpless victims. On the contrary, females display a remarkable array of mechanisms of resistance. In particular, females may choose to allocate matings to certain males that have demonstrated their ability to dominate other males and can therefore offer females and/or their young protection. Protective males defend their own reproductive interests and also augment a female's ability to survive and reproduce. For a certain fraction of each sex, protective mating alliances may represent the best way to maximize fitness given the prevailing constraints.

These alliances can take many forms. They may differ in duration and the number of females 170 guarded by a single male, but they share a fundamental similarity; the female benefits ft^om reduced male aggression and the male guards females during times critical to the female. Mate guarding, traditionally interpreted in terms of male interests, may be favored by female interests in protection as well. The importance to females of protection from sexual aggression is a factor that should be considered in smdies of mate choice and in studies of the evolution of mate guarding, female gregariousness and breeding synchrony, leks, "harems", monogamy, polygyny and pair-bonding in humans.

• • •

I thank Patty Gowaty for the opportunity to share my ideas on this subject and for her assistance in revising earlier versions of this manuscript. I thank Bumey Le Boeuf for providing the opportunity to study northern elephant seals and for proposing the project of documenting female counterstrategies. Bumey originally suggested the idea of "trading sex for safety". I thank him also for insightful comments on earlier drafts of this manuscript. Three papers, two by

Barbara Smuts and the other by Barbara and Robert Smuts, were tremendously important to the formulation of my ideas on this subject. I thank Barb for sharing her knowledge of primate behaviour and ideas on sexual coercion with me as well as for valuable comments on the manuscript. I am especially indebted to D.A. Thomson, advisor and friend, for his continued support, critical discussions, and thoughtful editing of the manuscript. I am grateful to the many investigators who took their time to share with me their areas of expertise; J. Ames, G. Amqvist,

M. Bateson, D. Boness, S. Brownmiller, R. Caldwell, Y. Cruz, L. Frank, J. Graves, K. Hill,

R. Howard, H. Johnson, H. Kaplan, J. Koprowski, F. McKiimey, M. Riedman, K. Rodgers, K.

Schultz, S. Shuster, R. Smith, M. Staedler, B. Subramanian, B. Sullivan, M. Tharan, R.

Thomhill, J. Waage, P. Wrege. For their interest and thoughtful comments on the manuscript,

I diank G. Amqvist, R. Baird, J. Bronstein, J. Byers, A. Cohen, M. Daly, P. Hastings, W. 171

Maddison, K. Mangin, S. McLaughlin, A. E. Michel, N. Moran, R. Smith, Z. Tang-Martinez and M. Wilson.

SUMMARY

Sextial aggression affects the lives of females in numerous ways. This paper reviews the costs to females of sexual aggression and reviews the forms of female resistance. In particular,

I focus on females who may choose to allocate matings to those males that have demonstrated their ability to dominate others males and can therefore offer females and/or their young protection. I term this the bodyguard hypothesis of female mate choice. The resulting protective mating alliance is a more-or-less long-term period of interaction between the male and the female during which time the female copulates and the male protects his mate (and their young) from other males during times critical to the female.This paper details assumptions of the bodyguard hypothesis, presents a series of predictions, and suggests critical tests of the hypothesis. I review examples consistent with elements of the bodyguard hypothesis, present data illustrating the effectiveness of protective males in reducing the probability of aggression fi-om other males, and suggest the importance of protective mating alliances in the evolution of a diversity of animal mating systems including mate guarding, female gregariousness and breeding synchrony, leks,

"harems", monogamy, polygyny, and pair-bonding in humans. 172

TABLE 1. Potential costs of sexual coercion for females.

Costs of Sexual Coercion for Females Example

Time and energy expended avoiding males waterfowl, McKinney et al. 1983, Sorenson 1994; squirrels, Koprowski 1993; sirenians, Anderson & Birtles 1978, Hartman 1979; ungulates, Geist 1971. Berger 1986, 1994; insects, Drummond 1984, Robertson 1985

Circumvention of female's ability to choose scorpionflies, Thomhill 1980 her sexual partner (depriving her of potential genetic or material benefits)

Thwaning a female's freedom of movement New Zealand sea lion, Marlow 1975; hamadiyas baboon, Abegglen 1984

Disruption of female feeding common eider, Ashcroft 1976; horses. Berger 1986, Rubenstein 1986; insects, Odendaal et al. 1989, Rowe et al. 1994, Stone 1995

Disruption of maternal care abandoning breeding; birds, Koenig 1982, McKinney & Stolen 1982, Afton 1985, Davies 1985; young becoming separated from their mothers: pinnipeds, Marlow 1975, Campagna et al. 1988. 1992; disruption of oviposition: walnut flies, D. Papaj, pers. comm.; interruption of lactation: pinnipeds, Hiruki et al. 1993b, Boness et al. 1995

Mate abandonment waterfowl, Sorenson 1994, Afton 1985

Disruption of female reproductive cycles and horses, Berger 1986; primates. Smuts & Smuts 1993 abortion

Infanticide primates. Hrdy 1977. Hausfater & Hrdy 1984, Smuts & Smuts 1993, Hiraiwa-Hasegawa 1994; lions. Packer & Pusey 1983; pinnipeds, Campagna et al. 1992; tree swallows, Robertson 1989

Death pinnipeds, Campagna et al. 1988, Le Boeuf & Mesnick 1991, Hiruki et al. 1993b; waterfowl (wild, urban & captive), McKinney et al. 1983; sea otters. Staedler & Reidman 1994; squirrels, Koprowski 1993; fallow deer, Clutton-Brock et 1992; cheetah (captive), Wielebnowski pers. comm; primates. Carpenter 1942, Vanderbergh & Vesey 1968. Smuts & Smuts 1993 TABLE 2. Hypotheses, predictions, and tests of the benefits of mate-guarding. See text for discussion.

Mate Guarding

Other Hypothesis Advantage Key prediction Experimental Manipulations Falsified by predictions increase male remove guard sex that density after maintains insemination proximity Bodyguard female guarding reduces mcrease female seeks encounters with female male aggression guarding another mate non-mates are not costly

Paternity male guarding mcrease female does not lack of sperm male assurance increases guarding seek another competition number of mate offspring sired TABLE 3. Hypotheses, predictions, and tests of the benefits to females of mating with dominant males. See text for discussion.

Female Preference for Mating with Dominant Males

Fitness Experimental Hypothesis advantage Key prediction manipulation Falsified by Other predictions increase density extended cheaters * association of mates

Bodyguard direct guarding reduces mating frequency encounters with non- yes yes male aggression increases and/or mates not costly duration of association of mates increases

"Good indirect heritable differences mating frequency female preferences no no genes" among males and duration of do not increase increases fitness of association of mates fitness of progeny progeny stays the same?

• "cheaters" are females that associate with protective males but mate with other males. 175

APPENDIX A

SEXUAL DIMORPfflSM, SPECIES DIVERSITY, HABITAT, AND EGG TYPE OF FAMILIES OF TELEOST FISHES

This Appendix summarizes the most relevant data compiled for this study, but is not a data set itself; it was a tool used to find the sister-taxa comparisons tallied here. It is incomplete in many ways because (1) the original data set records information on several additional behavioral and ecological characteristics (see Methods); (2) I skipped recording data for families in which I thought there would be no variation in sexual dimorphism; e.g., families within the

Pleuronectiformes likely to be similar in their sexual dimorphism scores (monomorphic) and my time was better spent elsewhere (like the zoo!); and (3) in the original data set, I often broke down the familial categories into sub-families and tribes. Here, however, I combined these into a single familial sexual dimorphism score; lost in the process are the many references recorded for these lower taxonomic levels. These are available upon request.

SPECIES/GENERA DIVERSITY estimates were taken from Nelson 1994 unless more recent taxonomic reviews were available. SEXUAL DIMORPHISM (record): Records the presence or absence of all sexually dimorphic charac­ ters observed for each family. For most species, it is unclear to what extent, if at all, these characters are displayed during courtship or are evaluated by females during mate choice decisions. They are included in the data set in the following categories pending specific information on their function. Absent 1 = Monomorphic Present — Non-display 2 = Structures associated with gamete transport. 3 = Female fecundity. 4 = Internal structures.

Noted in text = Dimorphic characters associated with ecological differences. 176

Present — Display 5 = nuptial coloration 12c = eye position and size 6 = mdes larger than females 12d = opercular modifications 7 = visual — color 12e = scalation 7a = egg spots 12f = dentition 8 = acoustical 12g = odontodes, spines 9 = electrical 12h = fleshy head extensions 10 = tactile 12i = body shape 11 = chemical 12j = gonopodium 12 = visual — morphological 12k = cirri 12a = fin extensions 121 = flesh swells 12b = head shape 13 = visual — structural

SEXUAL DIMORPHISM (qualitative score): Based upon that subset of characters considered most likely to function in courtship, and their relative degree of elaboration. I = monomorphic n = slight in = moderate, 1-2 dimorphic characters rv = extreme, > 2 dimorphic characters V = sexes considered different species HABITAT: Information was taken from Nelson 1994. M = marine B = brackish FW = fireshwater EGG TYPE: D = dispersive (pelagic) ND = non-dispersive (demersal or brooded) FL = floating nest REFERENCES: The primary references for these data are listed in the Methods section and full references for each of the comparisons tallied are found in Appendix B. Many of the references cited in this Appendix are not found in the References section of this disserta­ tion. They are available upon request. 177

Number of Sexual dimorpbism Common quali­ Egg Order Family Habitat name genera species record tative type score References

Osteo- glossifonnes

Nebon 1994. Lttider & Liem 1983. ^xton & Osteoglossidae arapaima 4 7 1.2 I FW nd &chmeyer 1994« Breder & Rosen 1966, Btrlow 1986

Nelson 1994. Uuder &. butterfly Uetn 1983. Pudon & Pancodontidae 1 1 2,3.5? I FW d fish Esctimeyer 1994. Breder & Rosen 1966

Nelson 1994, Breder & Hiodonddae mooneyes 1 2 7 7 FW d Rosen 1966

Nelson 1994. Pixion & FW some Notopteridae knifefishes 4 8 8? m? nd Eschmeyer 1994. Breder B & Rosen 1966

Nelson 1994. Greenwood in Paxton & Eschmeyer 1994. Breder & Rosen 1966. elephant Aves-Gomes & Hopkins Morrayridae 18 198 8,9,12i IV FW nd flshes ms. Hopkins ms. Hopkins & Bass 1981. AlveS'Comes et al. 199S. Hopkins pen. comm.

Nelson 1994. Paxion & Gymnarchidae gymnarchids 1 1 9 in FW nd Eschmeyer 1994. Breder & Rosen 1966

Elopiformes

Nelson 1994. Paxion & tenpounders, Elopidae I 6 I I M d Eschmeyer 1994. Breder ladyfish Sl Rosen 1966

Nelson 1994. Paxion & Megalopidae tarpon 1 2 I I M d Eschmeyer 1994, Breder A Rosen 1966

Albuiliformes 178

Nebon 1994. Piudon & Atbulidae bonefish 2 4(25) I I M d Esciinieyer 1994. Brcdcr & Rosen 1966

Nebon 1994. Hulan & Halosauridae halosauis 3 15 1 I M d EKfemeyer 1994, Bieder t Rosen 1966

Nebon 1994. hidon A Notacanthidae notacanthids 3 10 1 I M d Esduneyer 1994. Bieder & Rosen 1966

Anguillifonnes catadrom Nebon 1994. Breder A. Anguillidae FWeeU 1 15 2? ,3,7,12c n d ous Rosen 1966

Nebon 1994. Breder &. Heterenchelyidae 2 4 7 7 M d Rosen 1966

Nebon 1994. Breder & Moringuidae spagetti eels 2 6 2.3 V M d Roien 1966. Thtesher 19M

Nebon 1994, Breder & Xenocongridae &lse moray 8 16 I.3,4,l2a.l2i i(n?) M d Rosen 1966, Thresher 1984

Myrocongridae 1 2 ?? 77 M Nebon 1994

Nebon 1994, Breder & i.n(iv M some Muraenidae moray 15 200 1.5,6 d Rosen 1966, Thresher - Isp.) FW 1984

Nebon 1994. Breder & Synaphobranchidae cutthroat 10 26 1 I M d Rosen 1966

Nelson 1994. Breder & worm, M some Ophichthidae 52 250 1 I d Rosen 1966, Thresher snake FW 1984

Colocongridae 1 5 M Nebon 1994

Derichchyidae 2 3 M Nelson 1994 Muraenesoc-ldae pike congers 4 8 M Nebon 1994

Nemichthyidae snipe 3 4 M Nebon 1994

Nebon 1994, Ptxun & Eschmcyer 1994, Congridae conger 32 150 M d Thresher 1984. Breder &. Rosen 1966

Nebon 1994, Breder & Nettastomatidae duckbill 6 30 1 I M d Rosen 1966

Nebon 1994, Breder & Serrivomeridae sawtooth 2 9 1 I M d Rosen 1966

Saccopharyng- iformes 179

Cyematidae bobtail snipe 2 2 M Keison I9M Saccophaiyngidae swallowers 1 9 M Seison 1994

gulpers/ Nebon 1994 Eurypharyngidae 1 1 M pelican Monognathidae 1 14 M Nelson 1994

Clupeiformes dendcle Nelson 1994, hjuon & Denocipiddae 1 1 FW herring Esdinieyer 1994

Nelson 1994, Puun & M some Engraulidae anchovies 16 139 I I d Esclinieyer 1994. Breder FW & Rosen 1966

M, some Nebon 1994 Prist!gasteridae 9 34 FW

Chironcentridae wolf herring 1 2 M Nebon 1994

Nebon 1994. Puum &. herring, M: some d& Clupeidae 56 181 I I Eschmcyer 1994. Breder sartline FW nd & Rosen 1966

Gonorhynch- iformes

M some Nelson 1994. Breder & Chanidae milkfish 1 1 I I d FW RoKn 1966

Nelson 1994. Breder & beaked Gonorhynchidae 1 1 1 I M d Rosen 1966, Pixion & sandfishes Eschmeyer 1994

Nelson 1994. Breder & Kneriidae 4 27 4?,12d? i?n? FW Rosen 1966. Paxuxi Sl Eschmeyer 1994

snake Nelson 1994. Breder & Phractolaemidae 1 1 1 I FW 7 mudfish Rosen 1966

Cypriniformes

Nelson 1994. Pajtion tc. Eschmeyer 199*. Breder & Rosen 1966, minnows/ 1,2,3,5,7,10,1 i.n,ra, Cyprinidae 210 2010 FW nd Civender & Cobum carp 2a IV 1992. Winrield& Nebon 1991. Howes 1991. Smith 1991

nucum & Eschmeyer Gyrinocheilidae algae eaters 1 4 FW 1994. Nebon 1994

Nebon 1994. Breder & Catostomidae suckers 13 68 3.7,10 m FW nd Rosen 1966

Nebon 1994. Breder &. Cobitidae loaches 18 110 3,5,7,12a ra FW nd Rosen 1966 180

Balitoridae river loaches 59 470 FW Nebon 1994

Cbaraciformes

nd. Neboa 1994, Breder & Citharinidae 20 98 3,5,7,12a m FW d Rosen 1966

Nelson 1994, Breder & Hemiodontidae 9 50 7.12a 7.12a FW nd Roien 1966

Nelson 1994, Fuian & (ootbiess Curimaddae 11 125 7,87,I2a m FW Esdimeyer 1994, Viri characins 1983, etc.

Neboa 1994, Breder & Anostomidae 12 110 3,5or7.8 m FW nd Rosen 1966, Pison & Esctuneyer 1994

Nebon 1994. Puum & Erythrinidae trahiras 3 10 3,7,12a,12b m FW nd Eschmeyer 1994. Breder & Rosen 1966

Nebon 1994, hnon & Lebiasinidae 6 51 FW Esdimeyer 1994

pike- Nelson 1994. Puion & Ctenoluciidae 2 4 FW characids Esdimeyer 1994

Nelson 1994, Breder &. Hepsetidae I 1 12 n FW nd Rosen 1966

freshwater Nebon 1994. Ruion t Gasteropelecidae 3 9 FW hatchetfishes Esdimeyer 1994

Nelson 1994. Puian & Esdiemeyer 1994. i.n.ra. nd. 4,5,7.87,11, Breder & Rosen 1966. Characidae characins 170 885 (IV- FW som 12a,I2d.l2e Weioxntn <196Z). Buit some) e d a al. I9gg. Bulow 1986

Siluriformes

Diplomystidae 2 3 FW Nebon 1994

N. Nebon 1994. Bvkw American 1986 Ictaluridae 7 9 FW freshwater catfish

bagrid Nebon 1994 Bagridae 30 210 FW catfish

Olyridae 1 4 FW Nebon 1994

amorhead Nebon 1994 Cranoglanididae 1 1 FW catfish

Siluridae sheatfish 12 100 FW Nebon 1994 181

scliilbeid Nebon I99« catfish, Schilbeidae 18 45 FW African glass catfish

Pangasiidae giant catfish 2 21? 8 m FW Nelson 1994

Amphiliidae loach catfish 7 47 FW Nebon 1994

sisorid Nebon 1994 Sisoridae 20 85 FW catfish

torrent Nebon 1994 Amblycipiddae 2 10 FW catfish

stream Nebon 1994 AJcysidae 3 13 FW catfish

Patalcysidae I 2 FW Nebon 1994

squarehead, Nebon 1994 angler or Chaddae I 3 FW fitjgmouth catfishes

airforeathing Nebon 1994 Clariidae 13 100 FW catfishes

airsac Nebon 1994. Bvlow Heteropneustidae I 2 FW catfish 1986

electric Nebon 1994 Malapteniridae 1 2 8? ra? FW catfish

Ariidae sea catfish 14 120 8 in M Nebon 1994

Nelson 1994, Thmlier eeltail Plotosidae 9 32 8? m? M. FW 19g4. 1. Kutz pers. catfish comm.

squeakers or Nebon 1994 Mocholcidae upside down 10 167 8 in FW catfish

"doridoids'

Nebon 1994. Freil Aspredinldae banjo catfish 12 34 8 m FW dbsertuion

thorny or Nebon 1994 Doradidae talking 35 90 8,12a ra FW catfish

bottlenose Nebon 1994, Wabh 8,10.12a,12b, Ageneiosidae or barbelless 2 12 IV FW dssemdons, Femni 12h catfish dbsertuion

driftwood Nelson 1994, Femris Aucbenipteridae 15 30 2,8 ra FW catfish dissertenaiion

long-whiske Nebon 1994, Lundierg Pimelodidae 56 300 FW red catfish I991t.b 182

lookdown or Nelson 1994 Hypophthalmidae loweye I 3 FW catfish

whaieliice Nelson 1994 Cetopsidae 4 12 FW catfish

Helogeneidae 1 4 FW Nelson 1994

"loricarioids" Nelson 1994 Nematogenyidae 1 I FW Nelson 1994

pencil or Nelson 1994 Trichomycteridae parasitic 36 155 FW catfish

callicfathyid Nelson 1994. Reis Callichthyidae armored 7 130 8 m FW (Cssenitian catfish

spiny dwarf Nelson 1994 Scoloplacidae 1 4 FW catfish

Nelson 1994, SduefTer dissenenuion. L. Ripp suclcermouth Py-Duiiel pen. conun.. 550- Loricariidae armored 80 1.2.3.12g i.n.iv FW Schaefler 1990. 1000 catfishes Sclucffer i Uuder 1996, de Pinna dissenuion

climbing Nelson 1994 Astroblepidae 2 40 I I catfish

Gymno- nformes

glass Nelson 1994 Stemopygidae 5 15 FW knifefishes

sand Nelson 1994 Rhamphichthyidae 2 3 FW knifefish

Hypopomidae 4 12 9 ra FW C. Hopldiis

ghost Nelson 1994 Apteronotidae 10 27 FW knifefish

naked-back Nelson 1994. Breder & Gymnotidae 1 3 1 I FW knifefish Rosen 1966

electric Nelson 1994 Elechoidae I 1 FW knifefish

Esocifonnes

Nelson 1994. Breder & Esocidae pikes 1 5 3(slight),5/7 n FW nd Rosen 1966. Fwaon & Eschemeyer 1994 183

mud- Nebon 1994. BrakrA Umbridae 3 5 3.5^ n FW nd minnows Risen 1966 Osmeriformes

argentines Nebon 1994. Breder& Argentmidae or herring 2 19 I2h n M d Roien 1966 smelts

Nebon 1994. Breder & Microstomatidae 3 17 M d ROKn 1966

deep sea Netson 1994 Bathylagidae I 15 M smelts

barreleys or Nelson 1994. Bretier & Opishoproctidae 6 10 M d spoolcfish Rosen 1966

Lepcochilichthyidae 1 3 M Nebon 1994

Alepocephalidae slickheads 24 63 M Nebon 1994

Platyroctidae 13 37 M Nebon 1994

northern Nebon 1994. Breder Sl l?,3,5/7,12a. i,in- M, ana- Osmeridae smelts, 7 13 nd Rosen 1966. Paxiofl & 12e capelin dromous capelin Esehmeyer 1994

ana- Nebon 1994. Breder & icefisb or Salangidae 4 11 I m dromous nd Rosen 1966 noodlefish FW

Sundaland Nebon 1994 Sundasalangidae 1 2 FW noodlefish

NZ or Nebon 1994. Breder t Reinnidae southern 3 5 I m FW, B Rosen 1966. Pixmn & smelts Esehmeyer 1994

salmander- Nebon 1994 Lepidogalaxiidae 1 1 FW fish

FWdia- Nebon 1994, Breder & Galaxiidae gaiaxiids 8 40 1,2,7 1. n nd dromous Rcsen 1966

Salmoniformes

Nebon 1994. Siolz & FW 3.5,6,7,9,12a. n.ni,i Schnell 1991. Hutchings Salmonidae II 66-67 ana- nd I2b V & Morris. Siearley & dromous Smith 1993

Stomiiformes

bristle- Nebon 1994 Gonostomaddae 17 75 7 7 M mouths

Slemoptychidae hatchetfish 3 35 T 7 M Breder & Rosen 1966 Photichthyidae lightfishes 7 18 M

barbeled Breder & Rosen 1966 Stomiidae 27 228 7 7 M dragonfishes 184

Atcleopod- iformes jellynose Ateleopodidae 4 12 M fishes

Aulopifortnes

Breder & Rosen 1966. telescope- Giganturidae I 2 7 7 hxton & Eiduneyer fishes 1994

Nebon 1994, Tbresher Aulopodidae aulopus 2 9 I2a Q M 1984

Chlorophthalmidae greeneyes 2 20 M

Ipnopidae 6 29 M

Scope larchidae pearleyes 4 17 M

Notosudidae waryfishes 3 19 M

Breder & Rcun 1966. M, rarely d. Puioa & Esduneyer Synodonddae lizardfishes 5 55 1.3,12a n B nd I994,nireiher 1984. OUyania 1984

Pseudotiichonotidae 1 2 M Paralepididae barracudinas 12 56 M

Anotopteridae daggertooth 1 I M sabertooth Evermannellidae 3 7 fishes

Omosudidae I 1 M

Breder i. Rosen 1966: Aleopisauridae lancetfishes 1 2 12a n? M hnon& Esduneyer 1994. Nebon 1994

Myctoph- ifonncs

Pinon &. Eschmeyer Neoscopelidae 3 6 1 I M 1994. Nelson 1994. Ptxioneiil. 1984

HuUey in Puum & Eschmeyer 1994. Nelson 1994, Breder & Rosen Myctophidae lantern fishes 32 235 1.13 i.m M d 1966. Mooer el it. & Puion et il. 1984 , Puaon et al. 1984

Lampridi- formes spinyfin and Veliferidae sailfin 2 2 M velifers 185

Lamprididae opah 1 2 I I M Brcder £ Rosen I9£6 tube-eye or Scylephoridae I 1 M thread tail

Lophoddae ciestfishes 2 2 M Radiicephalidae I 1 M Trachipteridae ribbonfishes 3 10 M Regalecidae oarfishes 2 2 M

Polymixi- iformes Nebon 1994, Pixion in Polymixiidae beardfishes 1 5 M Pixion& Eschmeycr 1994

Percops- 6 9 iformes Bndei &. Rcttn 1966, trout- Percopsidae I 2 1 I FW Pmoa& Escluneyer perches 1994

Bftder & Rosen 1966. Aphredoderidae pirate perch 1 I 1 I FW Pixioa & Eschnicycr 1994, Barlow 1986

Amblyopsidae cavefish 4 6 10 U FW Bnder & Rosen 1966

Ophidiiforraes carapids and Thresher 1984 Carapidae 7 32 I I M d pearlfishes

Ophidtidae cusk-eeis 46 209 1 1 M Thresher 1984 viviparous Thomson ef al. 1983, Bythitidae 31 90 2.12j? I on?) M brotulas Thfeslierl984

Aphyonidae 6 21 2 1 M false Parabroculidae 2 3 2 I M brotulas

Gadiformes Ranicipiddae tadpole cod 1 I M

Euclichthyidae eucia cod 1 1 M grenadiers, Fihty & MatUe 1984 Macrouridae 38 285 M rattails

luminous Fahay & MarUe 1984 Steindachneriidae 1 I M bake

morid cods Fihay & MarUe 1984 Moridae 18 98 M or moras

Melanonidae pelagic cods 1 2 M Fahay & MarUe 1984 southern Macnironidae 2 7 1 I M hakes 186

F^y £ Mirkle & Bregmaceroddae codlets 1 12 M HaiideI9S4

Filoy A MarUe. Bcedcr Muraenolepididae eel cods 1 4 1 I M ft Roieii 1966

merluccid Falny & MarUel9g4. Merlucciidae I 13 M hakes Breder & Rosen 1966

Gadidae cods 15 30 1 I M

Batracoid- iformes

Neboa 1994, Puma & Batrachoididae toadfish 19 69 8,13? m M nd Eichmeycr 1994

Lophiifonnes Lophiidae goosefishes 4 25 1 I M d Bieder & Rosen 1966

Breder A Rosen 1966, Antennariidae frogfishes 14 43 7 n M d Thresher 1984. Pieisch ft Grobeciter 1987

Brachionichthyidae handfishes I 7 1 I M Breder ft Rosen 1966 Ogcocephalidae batfishes 9 62 1 I M Pieisch 1984. 1987

Nelson 1994, Benelsen 35 149 3.11 in M 1984

Caulophrynidae 2 4 3.11 m M Breder ft Rosen 1966 Neoceratiidae 1 1 3.11 m M

Melanoce-ddae I 5 3.11 in M football- Himantopophidae 1 18 3.11 m M fishes

Oneriodidae 16 34 3,11 ni M Thaumadchthyidae 2 9 3.11 m M deep-sea Cenhyrynidae 1 1 3.II ra M anglerfish

Ceradidae seadevils 2 4 3,11 m M Breder ft Rosen 1966 Gigantacdnidae 2 21 3.11 in M

Linophrynidae 5 49 3.11 in M

Mugiliforraes

Nelson 1994, PiteiUi 1993. Stiassny Mugilidae mullets 17 66-80 1.3.5 i.n M 1990.1993. Johnson ft Pilteison 1993. de Sylvi 1984

Atheriniformes Madagascar Bedodidae rainbow- 2 4 ? a FW fishes 187

Australian PvoaoA Eiduneyer Melanotaeniidae rainbow- 6 53 3,7,12a IV FW, B nd 1994. AOen & Cnxs fishes 1982, Fdner 1967

Putaa& EKhmeyer 1994, Bceder t Rosen Pseudomugilidae blue-eyes 3 15 37577,12a IV B, FW nd 1966. AUen & Cress 1982

silversides, M, some lee hrend 1993, Breder Atheminidae 25 165 1,3 1,3 nd gninion FW ftRoien 1966

Pixuxi & Eschmeyer Notocheiridae 2 6 M 1994

sailfin Pixuxi & Eschmeycr silversides 1994 FW. B, Telmatherinidae or Celebes 4 17 7,I2a IV nd M rainbow- fishes

Pumnjb Eschmeycr Dentatherinidae 1 I M 1994, Piremi pen. comm.

see Puemi 1989, Breder B, FW. Phallostethidae 4 19 2,3 I & Rosen 1966. Pmni rarely M pen. comm.

Beloniformes

Neboo 1994, Pmon & Eschmeyer 1994, Breder adrian- Adrianichthyidae 4 18 2,5/7,l0,l2a i,n FW, B & Rolen 1966. CoUeoe ichthyids ei >1. 1984. Puemi pen. comm.

Nelson 1994. Breder St. Belonidae needlefishes 10 32 1 I M, FW (nd) Rosen 1966

Nelson 1994. Breder St Scomberesocidae sauries 4 4 1,6,7,12b n M d Rosen 1966

(d. Nelson 1994. Bieder & Exocoetidae flyingfishes 7 or 8 52 1,3,5/7? i.n M nd) Rosen 1966

Nelson 1994, Breder t d, Hemiramphidae halfbeaks 12 85 2,3.5/7,8 i.m M Rosen 1966, Piremi nd pen. comm.

Cyprinidont- iformes

FW, Nelson 1994. Scheel Aplocheilidae rivulines 20 310 6,7 n,iv nd rarely B 1990. Puemi 1981 188

hnmi I98I, BrcderA Middle Rosen 1966, Puoon t Profbnulidae America 1 5 3 I FW nd Esctuneyer 1994, Ncbon killifishes 1994. Meyer Lydesrd 1993

ParEnti 1981, Brcder & copminnows Rosen 1966. hxton & FW, B, Funulidae and 5 46 3,5,10 IV nd Eschnieyer 1994, Nelson rarely M killi&hes 1994. Foster 1967. Meyer & Lydeard 1993

Valenciidae 1 2 I 3 FW nd

hrenii 1981. Breder& four-eyed Rosen 1966. ftxloa & FW, B, Anableptdae fishes, 3 9 2,3,7 n nd Esduneyer 1994. Ncbon rarely M cuatro oyos 1994. Meyer A Lydevd 1993

Btcder Sc. Rosen 1966. Parend 1981. Rosen & poecilids. BtUey 1966. Plxton &. mollies, Esduneyer 1994, Nelson guppies, 2,3,5,6,7,12a. Poeciliidae 30 293 FW, B nd 1994, Meyer & Lydevd mosquitofish I2j 1993 . Ftrr and 1989.Tnivis. Endler. swcrdtails KodiK-Btovm. Constamiz. etc.

Bteder & Rosen 1966. Nebon 1994. Pventi goodeids 1981, Meyer &. Lydeard Goodeidae 19 40 2,3?,6?,7,12a ni FW nd (splitfins) 1993. Saborn ct tl. 1996. Pirenti pen. comm.

Brcdcr S. Rosen 1966. Nebon 1966. Meyer & 3,4,5,7,12a, a,in,i Cyprinodontidae pupfishes 9 100 FW nd Lydeard 1993. I2e V Kodric-Brown. Foster 1967

Stephano- beryciformes bigscale Nebon 1994 Melamphaidae fishes or 5 33 M ridgeheads

Gibberichthyidae gibberfishes I 2 M Nebon 1994

Stephanoberycidae pricklefishes 3 3 M Hispidoberycidae I I M 189

redmoutb Nebon 1994, Rudoa Rondeledidae 1 2 M whalefisfaes 1994

red Nebon 1994, huon Barbourisiidae 1 I M -halefish 1994

flabby Nebon 1994. Fuion Cetomimidae 9 35 M whalefishes 1994

Mirapinnidae mirapinnids M laigenose hxion 1994, Nebon Megalomycteridae 4 4 U? 7 M fishes 1994

Beryciformes Anoplogastridae fangtooths I 2 M Nebon 1994

Nebon 1994. Puton Diretinidae spinyfins 3 4 M 1994

flashlight Nebon 1994 fishes or Anomalopidae 5 6 M lantern fishes

pinecone Nebon 1994, Puaon Monocentridae 2 3 M fihses 1994

roughies Nebon 1994 (includes the Tachichthyidae orange 7 35 M roughy)or slimeheads

Nebon 1994, Puttm Berycidae alfonsinos 2 9 M 1994, Keene & Tithe 1984

Nebon 1994. squirrel- Holocentridae 8 65 1.5,6.7.8 M d B>xIonl994, Breder & fishes Rosen 1966

Zeiformes Parazenidae parazen I 1 M Macrurocyttidae 3 4 M Zeidae dories 7 13 M

Oreosomaddae oreos 4 9 M gram- Gramtnicolepididae 3 4 M micolepidids

Caprcidae boarfishes 2 8 M

Gastero- steiformes

Nebon 1994, On & Hypoptychidae sand eel 1 1 M nd Pietschl994 190

Nebon I99«. Orr& M, Piasdil99«. Aulorhynchidae tubesnouts I 2 3? n coastal nd FritzKlKl984. Breder & marine Rosen 1966

Nebon 1994. Otr & PieiichI994. Fri(ziclieI9g4. Breder & M. B, Gasterosteidae sticidebacks 5 7 3,5.12b m nd Rosen 1966. Rol£ FW 1989i.b. BeU & Foster 1994, A. Vincent pen. comin.

Nelson 1994, FrilzxlieI984, A. 2,3 or Pegasidae seamoths 2 5 in M, B d Vincent perJ. comm.. 6(some),7 Herald St. Oufc 1994. Kuiier 1985

Syngnathoidea nd

Nelson 1994, Orr & ghost Pielsclil994, Solenostomidae 1 3 2 I M nd pipefishes Frilzicliel984. Btrlow 1986

Nelson 1994. Orr ft Pietscbl994 . pipefishes M, B, Fntzsdiel984, Breder ft Syngnathidae and 52 215 2,3,7,12 i,in Some nd Rosen 1966. Berglund ft seahorses FW, Rosenqvist I990.Gronell 1984

Neboa 1994. Breder ft Indoscomidae paradox fish I 1 1 I FW 7 Rosen 1966

trumpet- Neboa 1994. Thresher Aulostomidae I 3 5 n M d? fishes 1984

Nebon 1994.nireiher Fistulariidae cometfishes I 4 1 I M d 1984

Macroramphosidae snipe fishes 3 12 1 I M nd Nebon 1994

shrimpfishes Nebon 1994 Centriscidae or 2 4 I I M 7 razorfishes

Synbranch- iformes

Nebon 1994. Ueml994. Synbranchidae swamp-eels 4 15 1 I FW, B nd Breder ft Rosen 1966

Chaudhutiidae 4 5 FW Nelson 1994

Mastacembelidae spiny eek 4 67 FW Nebon 1994 191

Scotpaen- iformes

flying or Nelsoa 1994. helmet EsdKnieycrl994, Breder Dactylopteridae (newer 2 7 1 I M d ftRoun 1966 name) gurnards

Nebon 1994. Escbemeyer 1994. scorpion- M, rarely d. Washingion et il. 1984 . Scorpaenidae fishes 56 388 2,3,6,7,8?, 12 i.n/ra? FW nd Breder & Rosen 1966. (rockfishes) Birsukov 1981. KendaU 1991

coral Nelson 1994. crouchers, Eschine>crl994 Caracanthidae 1 4 M orbicular velvetfishes

Nelson 1994. Aploactinidae velvetfishes 17 37 M Eschineyerl994

Australian Nelsoa 1994, Pataecidae 3 5 M ptt)wfishes Eichmeyerl994

red Nelsoa 1994. Gnathanacanthidae 1 1 M velvetfish EschineyerI994

racehorses Nelson 1994. Congiopodidae (pigfishes or 4 9 M Eschmeyerl994. horsefishes) Wtshintion et *1.1984

searobins Nelson 1994, Triglidae 14 too 237812 in M d (gunards) Wuhingun ei il. 1984

deepwater Nelsan 1994. Bembridae 4 S M flatheads Esdinieyerl994

M, some Nelson 1994. Platycephalidae flatheads 18 60 2-some,3.7,12 n d B Eschnieyerl994

spingy or Nelson 1994. Hopiichthidae ghost 1 10 M Esdinieyerl994 flatheads

(2-some),3,7,l Nelson 1994. Breder & Anoplopomaddae sablefishes 2 2 n M d 2 Risen 1966

greenlings Nelson 1994, DcMutini Hexagrammidae 5 11 2(some),3,7,12 n M nd and lingcod 1987

Noimanichthyidae 1 1 M

grunt Nelsan 1994 Rhamphocot-tidae 1 1 M sculpin

Ereuniidae 2 3 M Nelson 1994 192

Netaon 1994. Yabe I98S. Wuhintion et tL 2-some,3,5,6, t9M, Bicder St. Rosen Cottidae sculpins 70 300 7,8 (one sp.), m M, FW nd 1966. Mueunto & 12a, 12b, 12k Biaaza 198S, Downhower Brown

Baikal Nelsoa 1994. Comephoridae 1 2 2-some,3,7,12 n FW nd oilfishes Wuhingtoo et il. 1984

AbyssQConidae 6 20 FW Nebon 1994

Heniitriptcridae 3 8 M Neboo 1994

Nelsoa 1994. Eiduneyer 1994 . clisnflcadoa Agonidae poachers 20 44 2-some,3,7,l2 a M nd ToUows Kunyanu 1991, Wishington et il. I9S4

fathead Nelson 1994. Esdnneyer Psychroluddae 7 29 M sculpins 1994. Ytbe I9gS

BathyludchUiyidae I I M Nelson 1994

lurapfishes Nelson 1994, Breder & Cyclopteridae (lump- 6 28 M Rosen 1966. suckers) Eschineyerl994

Perciformes

Percoidei

Liparidae snailfish 19 195+ M nd Nelson 1994

M, B, Nelson 1994. Cenomidae snooks 3 22 FW Greenwood 1976

Asiatic M, B, Nelson 1994 Chanidae 8 41 glassfishes FW

temperate B, M, Moronidae 2 6 basses FW

temperate Nelson 1994. ice perches, loiuison 1984 FW, Percichthyidae stripped 11 22 rarely B bass (G. Morone)

temperate Nelson 1994 Acropomatidae U 40 M ocean-basses

Nelson 1994, Baldwin Sl d, i.n,ra, M, rarely Johnson 1993. Kendall Serranidae sea basses 62 449 1.3,4,5,6 som V FW 1984. Johnson 1984. e nd Bieder A Rosen 1966

Ostracobeiycidae I 3 M Nelson 1994

Callanthiidae 2 9 M Nelson 1994 193

Nebon 1994. lohmon & Pseudochromidae dottybacks 16 98 1,2,6.7.12a i.ni.iv M nd 0011994. Mok a iL 1990

Nelson 1994. Gffl & Grammaddae basslets 2 10 6.7 n M nd Mooi 1993. Johnson & 0011994, Thresher 1984

roundheads, Nelson 1994. Mooi longfins, 1993. Johnson & spiny 0011994. Moketil. Plesiopidae II 38 5 n,ra? M nd basslets, 1990 devilfishes, prettyfins

Nelson 1994. D. Hosey Notograpddae I 5 1 I M ft 0. Allen

Nelson 1994. Mooi i(n,ra 1993, Smhh-Viniz. Opistognatbidae jawfisbes 3 60-90 1.5.7 M nd Breder & Rosen 1966. some) Mok et il. 1990. Thresher 1984

Dinopeicidae 2 2 M Nelson 1994

Nelson 1994. Breder &. Baitjosidae I 1 M Rosen 1966

sunfish, Nelson 1994, Johnson & bluegiil, 0011994. Mabce 1988, Centrarchidae largemouth 7 31 5,6.7.8 m FW nd 1993. 199S. Gross 1982. bass, Dominey crappies

Nelson 1994. CblleOe perch, 2.3,7.10. 1963.CoUeoe & Percidae walleye, 10 162 n.iv FW I2a,I2e.I2I Bamrescu I9T7. Wiley daiters 1992. Ct*ig 1987

bigeyes, Nelson 1994. Thresher Priachanthidae 4 18 M d? catalufas 1984

Nelson 1994. Johnson M, some cardinal- 1984. 1993. Thresher Apogonidae 22 207 1,3,5 i.n B, few nd fishes 1984. Kuwunun 1983. FW 198S

deepwater Nelson 1994 Epigonidae cardinal- 5 15 M fishes

sillagos, Nelson 1994. Breder & M, B, whitings, Rosen Sillaginidae 3 31 1 I rarely d smelt- FW whtiings 194

sand diefisb, Nelson 1994. Clarke Malacanthidae S 39 6.l2i n M d diefuh 1988. Tbnaher 1984

false Lactariidae 1 2 M tievaUies long-finned Dinolesddae I I M pike

Pomatomtdae bluefishes 2 3 M Nemadstiidae roosterfish I 1 M Nebon 1994

Echeneidae remoras 4 8 M Nelson 1994

Rachycentridae cobia 1 I M Nelson 1994

dolphin- Nebon 1994 Coryphaenidae 1 2 7.12b m M fishes

Nelson 1994. UraclK ei I.(n- jacks and M rarely •1. 1984, Smidi-Vtniz Carangidae 32 140 1,7 one d pompanos B 1984. Gtishiken 1988. spp) Thresher 1984

Menidae moonfish 1 1 M Nebon 1994

ponyfishes, Nelson 1994, Breder &. Leiognathidae slimys or 3 24 1 I M, B d Rosen 1966 slipmouths

Bramidae pomfrets 6 18 M Nebon 1994

Carisdidae manefishes 1 4 M Nebon 1994

Nelson 1994, Johnson It Etnmelichthyidae rovers 3 14 M Cini994

Nebon 1994. Thteslier 1984. Johnson & GUI I.OI snappers 1.3(lspp).6,7. M, rarely 1994. Bieder Sc. Rosen Lutjanidae 21 125 few d and fusiliers 12a B&FW 1966, Johnson 1980. spp) Carpener 1990 & Johnson 1993

M, a. Nebon 1994 Lobotidae tripletails 2 4 1 I FW

M, rarely Nebon 1994 Geireidae mojarras 8 40 B&FW

M. B, Nebon 1994. Johnson Haemulidae grunts 17 150 rarely in d 1980. Breder & Rosen FW. 1966. Thresher 1984

bonnet- Nelson 1994. Johnson Inermiidae 2 2 M mouths 1980

Nebon 1994, Johnson M. very d, 1980. Thresher 1984, Spandae porgies 29 100 1,3,5/7 n,ra? rarely nd Johnson & GiUI994, B.FW Bteder & Rosen 1966 195

Nebon 1994, Jotasoa Centracanthidae 2 8 1.6 m M 1980. Thnalier 1984

emperors or Ncboa 1994, Johnson Lethiinidae emperor 5 39 1.6 n? M d 1980. Thresher 1984 breams

threadfin Neboo 1994, lahfuoo Nemipteridae 5 62 1 I M breams 1980. Thresher 1984

Polynemidae thread fins 7 35 I? I? M. B d Nebon 1994 drums, Neboa 1994, Stuki croakers, M, B, 1989. Thresher 1984. Sciaenidae 70 270 8 ra d jackknife FW Breder & Rosen 1966 fish

M, rarely Ncboa 1994. Thresher MuUidae goatfishes 6 55 3,5.6 n B 1984

Pempheridae sweepers 2 25 M, B Nebon 1994

pearl Neboa 1994 Glaucosomatidae I 4 M perches

M, B, Nebon 1994 Lepcobramidae beachsaimon 1 1 occasiona Ily FW

Bathyclupeidae I 4 M

moonfish, M.B. Nebon 1994 Monodactylidae 2 5 fingerfishes some FW

M. B. Nebon 1994 Toxotidae archerfishes 1 6 FW

galjeon Nebon 1994 Coracinidae 1 3 M, B fishes

Nebon 1994. Doris & Drepantdae 1 2 \ I M Rucabado 1987

Nebon 1994, Thresher 1984. Allen 1978. Breder & Rosen 1966. butterfly- Chaetodonddae 10 114 1.4.5,6,7 I.IV.V M d G>Un 1989. Blum fishes I98S/9. Reese 1975. DriscoB & Drocoll 1988. Houripui 1989

Nebon 1994. Thuher 1984. Mka 1978. Moyer et >1. 1983. Pomacanthidae angelfishes 9 74 1.5,6,7.8,12a i.n,ra M d Mayer & Nilazono 1978. Tresher 1982. Moyer 1990

Nebon 1994. Sieene Enoplosidae oldwtfe I I M 1977 196

armorheads, Nebon 1994 Pentaceroddae 7 11 1,6 I,IV M boarfisbes

FW, Ntbun 1994. Breder t Nandidae leaffishes 7 10 1.5 i.n nd some B Rosen 1966

Kyphosidae sea chubs 15 42 1 I M Nelson 1994 Australian Arripidae 1 4 M salmon

grunters, M, B, Nebon 1994 Teraponidae 16 45 dgeipeiches FW

flagtails M, B. Nelson 1994 Kuhliidae I 8 1 I (aboleholes) FW

Nelson 1994. Bieder & Opiegnathidae Icnifejaws 1 6 M d Rosen 1994

Nebon 1994. Thresher I9S4. Damdson & Cirrhiddae hawidish 9 32 1.6,7 I, n M d G)lin 1989. Donaldson 1990. DooVboa 1986

Chironemidae Icelpfish 2 4 M Nebon 1994

Aplodaccylidae marblefishes 3 5 3 I M Nebon 1994

Nebon 1994. Thresher Cheilodactylidae tnorwongs 5 18 M d 1984

Latridae tnirapeters 3 9 M

Cepolidae bandftshes 4 19 M Nebon 1994

Elassomatoidei pygmy Nelson 1994 Elassomaddae 1 6 FW sunfish

Labroidei

Nebon 1994. Allen 1.3,5,5,6.7 M, I97S. Allenl994. Pomacentridae damseifishes 28 315 (rare),8(few), i.n.ni nd rarelyB Thresher I9S4. Allen 12a(few) 1991

Nelson 1994, Lauder & 1,11,111. Cichlidae cichlids 105 1300 l,3?5.6?7 FW. B nd Liem 1983. Keenleyside rv.v 1991

Nebon I99t. Breder & Rosen 1966, Nakazono M, rarely ct al. I98I. Uem 1986. Embiotocidae surf^iches 13 24 2,3.5.6.12a n,in nd FW Warner &. Harlan 1982. DeManini 198S. Darling ei al. 1980, Baa 1974 197

Nelson 1994. L&LI983. Webb 1990. Pkaoo & Eiduiwyer 1994. Thresher 1984, 14.6.7.12a. Labridae wrasse 60 SCO M Robeftson & Hofliiun I2b IV ,V I977>Ioyer £ Yogo 1982. Westneu 1993. Tibonky ei il. 1987. Roede 1990

Nelson 1994. Lauder & butterfishes Liem 1983. Oiotl &. Odacidae or rocic 4 12 M d Belh«oodl994. Thresher whitings 1984

Nelson 1994. Uuder t Liem 1983. Chad & Scaridae parrotfishes 9 83 l.6,7,12a,12b I.IV,V M d Bellwaodl994, Thresher 1984. BeUwood 1994. Nalnzono

Zoarcoidei Bathymasteridae ronquils 3 7 M Nelson 1994

d. Nehon 1994 Zoarcidae eelpouts 46 220 M nd

Sdchaeidae pricklebaclcs 39 65+ M Nebon 1994 Ciyptacanthodidae wrymouths 4 4 M Nelson 1994

Pholidae gunnels 4 14 M Nelson 1994 Anarhichadidae wolfftshes 2 4 M Nelson 1994 Ptilichthyidae quillfish 1 1 M Nelson 1994 Zaproridae prowfish I I M Nelson 1994

Scytaltnidae graveldiver 1 I M Nebon 1994

Nouthenioidei

Bovichthyidae 3 11 M Nelson 1994 Noiotheniidae cod ice fishes 17 50 M Nelson 1994

plunder- Nelson 1994 Haipagifehdae 5 29 M fishes

Antarctic Nelson 1994 Bathydraconidae 10 15 M dragonfishes

crocodile Nelson 1994 Channichthyidae II 17 M icefishes

Trachinoidei

Chiasmodontidae 4 15 M Nelson 1994

Champsodonddae I 5 M Nelson 1994 convict Nebon 1994 Pholidichthyidae 1 1 M blenny 198

Trichodonddaea sandfisbes 2 2 M Nebon 1994 Pinguipedidae sandperches 4 50 M Nebon 1994 Cheimairhichthy- Nelson 1994 1 1 FW idae

Nelson 1994. Kinen et Trichonaddae sanddivers I 6 6,7,12a m M iL 1991

sand- Nebon 1994 Creediidae 7 16 M butTOwers

Percophidae duckbills 13 40 M

southern Nelson 1994 Leptoscopidae 2 4 M sandfisbes

Nelson 1994, Stevens et Ammodyddae sand lances 5 18 M >1. 1984

Traciiinidae weeverfishes 2 4 M

M, some Nelson 1994 Uranoscopidae stargazers 8 50 B

Blennioidei

Nelson 1994, Thresher 1984. Springert994. Huongs & Springer, triplefin M, rarely Honeman & Bimon Tripterygiidae 20 115 15 i,n nd blennies B 1993. Springer 1993, Petersen 1989, Thompson 1986. Friclce 1994

Nelson 1994. Thresher 1984, Sptingerl994. sand 1,4,7(1 sp.), M, rarely Dactyloscopidae 9 46 i.n Doyle 1996. Diwson stargazers 12a B 1974. 1976. 1977. 198a>. Springer 1993

Nelson 1994. Thresher 1984. Springerl994. 2,5&7,6, Hulings & Springer Labrisomidae labrisomids 16 102 n,m M nd I2be,b tree. Springer 1993. Stepiin 1993, Brooks 1990 199

Nelson 1994, Throlier 1984. Sprii]gerl994, rebdaoihipi: Hubbs kelp 1952 (brief jurwy found 2.3,4,5&7.6. Clinidae blennies, 20 80 n,m M nd only 1 mention of sex di I2b.e,h Mipfishes chrom), Hastngs & Sprinter tree. Sprinter 1993. Siepiiii 1993. see Sleptu I99Z

Nelson I9M. Thresher 1984, Sprinterl994, pike, tube 2,5.6,7.12a. i,n,m. Stephens 1963. Hasiints Chaenopsidae! or tl 65 M 12b.l2h,I2k IV & Springer tree. flagblennies Springer 1993, Slepivi 1993

2,3.4.5,6,7, i.n,in, Springer & Spreioer Blenniidae combtooth 53 345 M nd I2a.b,f,k IV 1978. Springer 1988

Icosteoidei Nebon 1994

Icosteidae ragfish 1 1 M

Gobiesocoidei M, few Gobiesocidae clingfishes 36 120 2,6,7,12i nan?) nd FW

Nelson 1994. Houde 1984. Fricke 1983. Callionymoidei Nalcibo. WUson 1978. T>lda &. Okamoco 1979

dragonets, Nelson 1994. Friclce Callionymidae mandarin 18 130 2,I2a ra M d 1992) fish

Nelson 1994. WimeriMOam 1993. Draconecddae 2 7 6,7.I2a,12c in M 7 Hoese 1994. Thresher 1984

Gobioidei Rhyacicihthyidae loach gobies 1 2 FW Nelson 1994 Odontobutidae 3 5 FW Nelson 1994 Eleotridae M, B. sleepers 35 150 (Eleotrididae) FW

M, B, Nelson 1994. Barlow Gobiidae gobies 212 1875 rarely nd 1986 FW

sandfishes Nelson 1994 M, rarely Kraemeriidae or sand 2 8 BorFW gobies 200

Xenisthoiidae M Nebon 1994 wormfishes Neboa 1994 M, rarely Microdesmidae and 9 60 BorFW dartfishes

Schindleriidae 1 2 M Nebon 1994

Kunoidei Nebon 1994

Nebon 1994. Uis A nursery- Kurtidae 1 2 B Rjchtrds fishes [984.Wintert)oiioin 1993

Acanthuroidei

Nelson 1994. Breder A M, rarely Ephippidae spadefishes 7 20 d Rosen 1966. B Winteiboaom 1993

Nelson 1994, Thresher icn 1984, Leis & Richards M, B. Scatophagidae scats 2 4 l,3,l2t(one sp) one 1984. Lacson & Nelson some FW spp) 1993. Wtmerbodom 1993. Tyler et tl. 1989

nd, Donaldson 1986. Lacson Siganidae rabbitfishes I 27 M, B d A Nelson 1993

Nelson 1994, Thresher 1984. Johnson & Luvaridae louvar 1 I I I M d 0011994. Tyler e( tl. 1989. Wimcrboaom 1993

Nelson 1994. Thresher 1994. Johnson A GUI 1994. WintetbooDm 3,5(sonie 0, A McLennan 1993. Zanch'dae moorish idol I I 6.12a,t2b, i.in M d Witteitooaom 1993. I2i Gutisu A WiraerboQom 1993. Robertson et al. 1979

surgeon- 5.6,I2a.I2b, Nelson 1994. Robertson Acanthuridae 6 72 in M d fishes I2i 1979. Barlow 1986

Scombrolabrac oidei

Nelson 1994. Johnson Scombrolabracidae 1 I 1,57,6? i,n? M 1986, CoUelie. Poohoff etal 1984

Scombroidei

Nelson 1994. Breder A Sphyraenidae barracudas 1 20 I I M Rosen 1966 201

snake Nebon 1994. Bicder £ Gempylidae 16 23 I I M d mackerels Rosen 1966 Trichiuridae cudassfishes 9 32 M d mackerels M, rarely Scombridae 15 49 d and tuna FW Xiphiidae billiishes 4 12 M

Stromateoidei Amarsipidae 1 I M Nelson 1994

medusa- Nelson 1994 Centrolophidae 7 27 M fishes

driftfishes, Nebon 19M Nomeidae man-of-war 3 15 M fish

Ariomattidae ariommatids 1 6 M Nebon 1994

Nebon 1994, Breder St Tetragonuidae squaretails I 3 M Rosen 1966

Nebon 1994, Uuder & Liem 1983. Fonelius Stromateidae butterfishes 3 13 M d 19S7, Johnson & Gill 1994

Ansbantoidei Luciocephalidae pikehead 1 I 5 n FW Nebon 1994 climbing FW, Nebon 1994 Anabantidae 3 30 5 n nd gouramies rarely B

kissing 1,5.7,8?. 12a, Nebon 1994. Liem 1963 Helostomatidae I 1 i,n,m FW fl gouramies 12b

Belontiidae gouramies 12 46 FW giant Osphronemidae I 3 FW nd gouramies

Channoidei

Nebon 1994. Chipletu 1993. Uuder & Liem Channidae snakeheads 2 21 1 I FW 1983. Hensley & Ahbirom 1984

Pleuronect- 1-alI? I-all? iformes Psenodidae psetroidids 1 3 M

Nebon 1994, Moser et Citharidae citharids 4 5 M U. 1984

lefieye Nebon 1994 Bothidae 20 115 M d founders 202

southern Nebon 1994. Maser a Achiropsetddae 3 4 M fIoui\ders il. 1984

Nelson 1994. Moeret Scophthalmidae 5 18 M d ll. 1984

M, rarely Nebon 1994. Uuder & Paialichthyidae 16 85 d FW Uem 1983

righteye M. rarely Nebon 1994 Pleuronectidae 39 93 (1) 0) flounders B orFW

Samaridae 3 20 M Nebon 1994

American Nebon 1994. LwiderdL Achiridae 9 28 M, FW soles Uem 1983

Nebon 1994. Under & Soleidae soles 20 89 M Liem 1983

M, rarely Cynoglossidae tonguefishes 3 110 (I) (D FW

Tetradont- tformes Triacanthodidae spikefishes 11 20 M d

Triacanthidae triplespines 4 7 M d

Nebon 1994. Ltuder & Uem 1983. Masoun & Tyler 1994, Abotmamn g

• & Lea 1984 . Thresher

Balistidae triggerfishes 11 40 1,5,6,7.12b i.m M ' 1984. Birlow 1987. Kiwue & Nikizono 1994, Niicizono & Kawase 1994. Clark ci •1. 1988

6,7.I2a,l2i, Barlow 1986 Monocanthidae filefishes 31 95 ffl M nd I2g

Nebon 1994, Maouun boxfishes, & Tyler in Paxion & cowfishes Eschmeyer 1994, Ostiaciidae 14 33 5.6,7,12i n.iv M d and Aboussouan & Leis tiunkfijhes 1984. Wineitiaaom £ Tyler 1983

three- Nebon 1994. Uuder Sc toothed Uem 1983, Maouura &. Triodontidae 1 I M d puffer, Tyler 1994. Uis 1984. purse fish Thiesber 1984

M, rarely nd, Threjber 1984 Tetradontidae puffers 19 121 1,6.7,I2i i.n FW& B d 203

poTcupine- Nelson 1994. LtuderA d. Diodontidae fishes, 6 19 1,5,6 i,n M Liem 1983. Maotnira SL nd burrfishes Tyler 1994. Uis 1984 molas, Molidae ocean 3 3 I? I? M d sunfish 204

APPENDIX B

SUMMARY OF MULTIPLE SISTER-TAXA COMPARISONS

OSTEOGLOSSEFORMES MORMYRIDAE

Mormyrids are found primarily in riverine habitats in central and southern Africa

(Hopkins 1986). The Mormyriformes comprises two families, the Gymnarchidae, which is

monotypic, and the Mormyridae. The Mormyridae, m turn, is composed of two subfamilies, the

Petrocephalinae {Petrocephalus with 26 species) and the Mormyrinae (16 genera and 165 species;

AIves-Gomes & Hopkins 1996).

Many mormyrids are sexually dimorphic in size and produce weak electric discharges by

a highly specialized electric organ in the tail (Hopkins 1986; Alves-Gomes & Hopkins 1996).

Electric communication is well developed and shows a sex difference; males show long duration

pulses (C. Hopkins pers. comm.). Within the family, there is a phylogenetic trend toward

increasing elaboration of the electrical signal. The plesiomorphic condition (Gymnarchus and

Petrocephalus) lacks sex differences. The more derived condition {Brienomyrus and several other

genera in the subfamily Mormyrinae) have advanced features and a variety of sex differences

(Hopkins 1986; Alves-Gomes & Hopkins 1996). In the later, electrical discharges play a vital role

in species and sex recognition (Hopkins 1983; Bass & Hopkins 1985; Crawford 1991,1992;

Friedman & Hopkins 1996). Females discriminate among males on the basis of the duration of

the discharge (Hopkins & Bass 1981; Hopkins 1988).

Mormyrids are also quite sensitive to sound which may allow communication over greater

distances (Crawford et al. 1981). A large repertoire of sounds is produced at various phases during nesting, courtship, and territory defense in Pollimyrus isidori (Mormyrinae). In this 205

species, although electrical discharges are sexually dimorphic, they appear to play a less

important role in courtship (Crawford et al. 1986; Alves-Gomes & Hopkins 1996). Crawford et

al. 's observations suggest that females are the target of male acoustic signals and that they may

also be important in individual recognition. No data are available on sound production in any

other mormyrid (C. Hopkins, pers. comm.).

Little is known about mormyrid breeding behavior except for Gymnarchus, which

produces a large floating nest and has an elaborate system of parental care, and Pollimyrus

isidori, which has been observed to build nests and show male parental care in aquaria (Hopkins

1986). In many species of mormyrids, reproduction by males is delayed until the males are quite

large and it is likely that young males do not breed at all (C. Hopkins pers. comm., Hopkins

1986). In other species, however, males do not delay any more than females, and in some,

females may be larger and older than the males with whom they are breeding and males of all sizes may breed in these species (C. Hopkins, pers. comm., Hopkins 1986).

CYPRINIFORMES CYPRINIDAE

At a very general scale, the Cyprinidae is divisible into two types of mating systems, scramble competition/broadcast spawning and nesting (Breder & Rosen 1966; Howes 1991;

Johnson & Page 1992). The Cyprininae tend to be broadcast spawners with scramble competition, and sexual dimorphism tends not to be well developed. Within the "Leuciscini", nesting is more developed, there is male parental care, and sexual dimorphism tends to be more developed. The monophyly and composition of the these groups is uncertain (Nelson 1994; Cavender & Cobum

1992; Cobum & Cavender 1992) and no further comparisons are possible at this time. However, within the Leuciscinae, the North American Notropis group (the "shiners") stands out for the marked sexual dimorphism of some species (Johnson & Page 1992, R. Mayden pers. comm.). 206

The "shiners" are sister to a clade comprised of the "chubs" and the "western clade". The former appears to show greater overall dimorphism, although this is variable (the shiners are also more diverse, 147 species in the shiners compared to 123 species in the chubs + western clade;

Cobum & Cavender 1992; Mayden et al. 1992).

In particular, in the genus Cyprinella (28 species), recently recognized as a distinct genus firom Notropis, sexual dimorphism is kick ass! (R. Mayden pers. comm.; Mayden 1989; Cobum

& Cavender 1992). Males are larger than females in size, dichromatic, and have larger breeding tubercles. Within Cyprinella, basal lineages are widespread in distribution, more aggressive, and have fine breeding tubercles. The more derived species have smaller geographic distributions, are less aggressive, and the courtship displays are more developed; males are more colorfiil and have bigger tubercles (R. Mayden pers. comm.; Mayden 1989). Spawning activity and species recognition are enhanced by sound in some species (Winn & Scout I960; Mayden 1989).

Cyprinella are described as crevice spawners, males are territorial and guard the spawning site, but there is no parental care after spawning (Mayden 1989; Page & Johnson 1990; Johnson &

Page 1992).

The sister to Cyprinella is probably the clade consisting of Pimephales (4 species) +

Opsopoeodus (1 species) + Codoma (1 species; the position of Opsopoeodus and Codoma are uncertain; R. Mayden pers. comm.; Mayden 1989; Cobum & Cavender 1992). Males are larger than females, show some tuberculation, are darker, and boldly patterned (D. Thomson pers. comm.; L. Page pers. comm.) but show relatively little elaboration of color, if any. Compared to Cyprinella, Pimephales is significantly less sexually dimorphic (R. Mayden pers. comm.).

Pimephales, Opsopoeodus and Codoma are described as territorial, egg-clusterers, with male parental care of the eggs (Page & Ceas 1989; Page & Johnson 1990; Johnson & Page 1992). 207

The two outgroups, Luxilus (11 species) and Lythrurus (10 species) are both sexually

dimorphic (R. Mayden pers. comm.; Mayden 1989; Cobum & Cavender 1992). It is probable

that all species of Luxilus are capable of building pit nests and/or broadcast spawning as nest

associates (spawning in the nests of other fishes). Lythrurus are nest associates (Johnson & Page

1992).

SILURIFORMES LORICARHDAE

The Loricariidae of Central and South America comprise a monophyletic group of

approximately 550-1,000 species (Schaefer 1986; de Pinna 1993; Nelson 1994; Schaefer &

Lauder 1996). Among the five subfamilies, sexual dimorphism is well developed in the

Loricariinae and the Ancistrinae, less so in the Hypostominae (not necessarily monophyletic) and

has not been reported in the Neoplecostominae and the H)rpoptopomatinae (L. Rapp Py-Daniel

pers. comm.). Reproductive behavior is poorly known among loricariids because of their habit

of living in turbid waters. Some parental care can be found in almost all species, while some

attach eggs to aquatic vegetation (Breder & Rosen 1966). Unlike most other catfishes, loricariids

are active in the day (Ferraris 1991).

The only well-known case of permanent sexual dimorphism occurs in the genus Ancistrus

(L. Rapp Py-Daniel pers. comm.). Males develop an amazing array of fleshy tentacles on the anterior body which become more numerous and bifurcate with age. Females have up to six small

tentacles throughout life. Ancistrus is sister to the tentacleless Chaetostoma which comprises 13 genera (L. Rapp Py-Daniel pers. comm.). One of the species in this clade, Chaetostoma jegui, has the only other known case of permanent sexual dimorphism. Males have a cylindric and conspicuously divided genital papilla (with separate genital and intestinal openings) whereas females do not (Rapp Py-Daniel 1991). Based on Ferraris (1991) males probably guard the eggs 208

in both groups. Diversity estimates were obtained from S. Muller (pers. comm. to L. Rapp Py-

Daniel) who is currently revising the genus Ancistrus. In contrast, Armbruster & Page (in prep)

tentatively have Lithoxus, with about 6 species, as sister to Ancistrus, which would change the

direction ofthis comparison. Thiscomparison awaits further phylogenetic resolution. The

Loricariinae (35 genera) contains many temporarily sexually dimorphic species. During the

breeding season, odontodes (long bristles present in many species of Loricariidae) become

enlarged, harder and much more numerous. In some species, lips become enlarged to

accommodate an egg mass. And, in some genera, males have round, crowded teeth while females

have more slender shaped teeth (L. Rapp Py-Daniel pers. comm.). The Loricariinae is sister to

the non-dimorphic subfamily Hypoptopomatinae (one genus with 6 species; Schaefer 1986; de

Pinna 1993; Nelson 1994). Within the Loricariinae, the gems Rhineloricaria has especially well

developed odontodes. They cover the snout, predorsal and interopercular area and pectoral fins.

Odontodes may function as a visual, or perhaps tactile, signal in intrasexual or intersexual

interactions, or they may be displayed toward potential predators if a male is guarding a nest.

These alternatives have yet to be examined (L. Rapp Py-Daniel pers. comm.). The Rhineloricaria

are sister to the genus Harttia which are not sexually dimorphic. These genera do not lip brood;

perhaps they nest in the open as some other Loricariinae are known to do (Ferraris 1991).

CALUCHTHYEDAE

The Callichthyidae of South America and Panama are comprised of two subfamilies,

Corydoradinae and Callichthyinae (Reis 1993). In the genera, Brochis (with 3 species) and its sister Corydorus (with at least 120 species) males and females have an elaboration of the ridges on the dorsal phlange of die pectoral fin which enables them to stridulate using high frequency sounds (I. Kaatz pers. comm.; Kaatz & Stewart 1996). Juveniles and females lack ridges. Sister 209

to these two genera is the genus Aspidoras. No ridges have been observed in the genus, but the

individuals studied might have been juveniles (I. Kaatz pers. comm.). In the three species of

Corydorus in which sounds have been recorded, males produced uncoordinated sounds in non-

reproductive aggressive interactions and produced highly coordinated series of sounds during the

breeding season. The "castanets" of each species was found to be very different. Females

probably stridulate in response to disturbances, given their pectoral morphology (I. Kaatz pers. comm.). Corydorus species are shades of black and white or with a bit of blue or yellow (L. Page pers. comm.). While they are active both day and night, courtship activity has only been recorded at night. During courtship, females apparently sit inactively and males hover nearby, stridulating.

After a courtship embrace, eggs are released, caught in the female's pelvic fins, and attached to aquatic vegetation (Ferraris 1991). Sometimes the female fertilizes the eggs after finding a suitable site with sperm she previously gathered in her mouth. There is no further parental care.

In the Callichthyinae, only low frequency grunts have been recorded (possibly produced by the swim bladder; I. Kaatz pers. comm.). The pectoral phlange in the genus Haplostemum is simple, lacking the system of ridges. Haplostemum and Callichthys are not externally sexually dimorphic (I. Kaatz pers. comm.). Males of these genera, and of the genus Dianema, build floating nests of bubbles and aquatic vegetation (Ferraris 1991). A complex courtship culminates in the females depositing eggs on the lower side of the nest and leaving. All guarding is done by the male.

DORADOEDS

The doradoids would be a fascinating group with which to study the relationship between acoustic signals and species diversification, pending more information on the breeding system (I.

Kaatz). Because they reside in murky waters little is known about which sex (or both) is 210

producing the sounds. Many species within these catfish families are known to produce sound

during the reproductive season by stridulating with their pectoral fins and by producing sounds

with their swim bladders. The presence of an elastic spring apparatus (ESA) is associated with

the capacity to generate swim bladder sounds. This structure is easily defined, its occurrence can

be mapped onto a tree, and changes in diversification rate can be analyzed with respect to changes in the trait. The ESA mechanism is known to be present but weakly developed or degenerate in the Malapteruridae, the electric catfish, a hypothesized basal lineage to the doradoids. The Ariidae, another hypothesized basal group, provides the first evidence of a fully developed ESA. Males are known to make sounds in defensive situations. Swim bladder sounds are unknown in the Plotosidae. All other hypothesized doradoid families, the presumably basal

Mochokidae, and the Asperinidae, Doradidae, Ageneiosidae and Auchenipteridae are known to produce swimbladder sounds during the reproductive season (I. Kaatz pers. comm.).

GYMNOTIFORMES

The Central and South American knifefishes are nocturnal and hide in dense vegetation or lie buried in sand during the day (Hagedom 1986; Ferraris 1991; Moller 1995). They are remarkable for their ability to generate and detect weak electric signals which are used to find food, navigate and for intraspecific communication (Lauder & Liem 1983; Nelson 1994).

Reproduction is known from laboratory studies of some species, e.g., Eigenmannia, Pateronotus, and Hypopomus (Hopkins 1974; Hagedom 1986; Hagedom & Heiligenberg 1985). From laboratory observations, some species have been observed to spawn repeatedly, over a period of several months, and there is an indication in some species of a post-spawning mortality.

Although Hypopomus is best known, other genera in the Stemopygoidei (57 species) are also thought to be sexually dimorphic in size, the length of the caudal filament which contains 211

the caudal portion of the fish's electric organ, and the waveform of the electric organ discharge

(Hopkins pers. comm.; Hopkins et al. 1990; Franchina & Hopkins 1996). Female choice is

thought to have played a role in the evolution of long duration discharges among males, and

males may have secondarily grown longer tails. Based on observations of field caught specimens,

however, selection for increasing tail size appears to be countered by predation pressure because many males have tails bitten by predators (or by other males) and may be a case of the "handicap principle" in operation (Hopkins et al. 1990). Interestingly, long duration pulses tend to be weaker than shorter duration pulses, and that by preferring males with long duration pulses, females are selecting for males that have extra capacity for generating signals, even when so disadvantaged (Hopkins et al. 1990).

In the Gymnotoidei (4 species), the Gynmotidae (3 species) are the best known and not known to have a sexually dimorphic electric organ discharge; the remaining species are considered to be similar (C. Hopkins pers. comm.).

SALMONIFORMES

The Salmonidae is comprised of three subfamilies whose relationships and species diversity are uncertain (Nelson 1994). Many biological species exist that are not named.

Phylogenetic trees based on morphological and larval characteristics (Stearley & Smith 1993 and

Kendall & Behnke 1994, respectively) suggest that the Coregoninae is sister to a ciade comprised of the Thymallinae + Salmoninae but trees based on life history and molecular characters

(Hutchings & Morris 1985 and Skurikhina et al. 1986, respectively) suggest that Thymallinae are divergent from Coregoninae and Salmoninae. Because of these uncertainties, I have omitted the

Salmonidae from the present analyses. 212

Information on sexual dimorphism and mating behavior was obtained from Breder &

Rosen (1966) and Stolz & Schnell (1991). The Coregoninae (32 species) are circumpolar. Sexual

dimorphism is not striking m the Coregoninae; males are smaller and trimmer than females and have pearl organs. Individuals are not territorial. Breeding pairs or small groups rise to the surface or spawn along the bottom. The Thymallinae (4-5 species) are European and Eurasian.

Sexual dimorphism is moderate; males are larger, have more brilliantly patterned dorsal fins, longer snouts and some have ^ extensions. The spawning pair disturbs the sand where small eggs are buried. The Salmoninae (30 species) are Eurasian and North American. Sexual dimorphism is extreme. Males are larger than females, more brilliantly colored (although females take on a lesser nuptial coloration as well), have modified head, jaw, fin, and body shapes. Males defend territories which contain the redds of a number of females. Male competition for access to females is intense.

MYCTOPHIFORMES

The Myctophiformes is comprised of two monophyletic families, the Myctophidae (235 species) and the Neoscopelidae (6 species; Moser era/. 1984; Okiyama 1984; Paxton etal. 1984;

Nelson 1994). The Mycophidae are the most widely distributed, the most species-rich, and the most abundant of all fishes in the deep open seas (Hulley 1994). Species in the Myctophidae are oviparous and spawn pelagic eggs. The Neoscopelidae are less abundant. They occur over the continental and island shelf regions in tropical and subtropical waters.

All but a few species of myctophid have lateral photophores arranged in a species specific pattern (the exception is Taaingichthyspaurolychnus mdNotolychnus; Paxton etal. 1984; Hulley

1994). These photophores are thought to play a role as an identifying signal in shoaling behavior and/or as camouflage. Typically, males and females have different light organs near the tail. 213 suggesting that these may be used for sex recognition. The structure of these glands varies in complexity, ranging from a single (sometimes black-bordered) organ to a series of overlapping luminous scales (Hulley 1994). These caudal luminescent organs are brighter than all other light organs combined. Caudal luminous organs are absent in the Neoscopelidae and only one species in the genus Neoscopelus has photophores (Paxton etal. 1984). In the Myctophidae, the ancestral caudal organs were not thought to be sexually dimorphic (Paxton et al. 1984). Luminous caudal organs are present in all but three myctophid genera (Diaphus, with 65-75 species;

Gymnoscopelus] Hintonia, with 1 species; Paxton et al. 1984) where their loss is considered derived. (However, Hulley 1994, says that luminous caudal organs are only not present in the

Lampanyctus, with 40 species, and Lampadena, with 8-9 species; Hulley 1994).

The two families are found in different habitats, violating the methodology outlined above in which comparisons were excluded when the sister taxa reside in different habitats. However,

I would predict that the mid water habitat of the Myctophidae is less heterogeneous than the continental shelf habitat of the Neoscopelidae, and therefore has less geographic barriers to promote speciation. Thus, the difference in habitat biases the comparison against the sexual selection-diversity hypothesis and I have proceeded with the inclusion of this comparison. How­ ever, this comparison is tentatively included. It could be argued as well that the continental shelf habitat is unusual (and maybe new) habitat for myctophiform fishes and, in addition, is smaller in size and less productive than the mid water habitat. If this is true, it biases the comparison in favor of the sexual selection-diversity hypothesis, and the comparison should be excluded. This dilemma remains to be resolved.

I conservatively considered half of the myctophid species to have sexually dimorphic caudal organs, and used this figure in the comparison. Pending resolution of the species diversity estimates and confirmation of which genera have and do not have luminescent organs, I will be 214

able to compare genera within the Myctophidae. At present, at the generic level, the comparisons

are ambiguous (two are strongly contrary to the sexual selection-diversity and two support the

hypothesis). Regardless of the sexually dimorphic luminous organs, the lateral photophores of the

Myctophidae could be used as a comparison with the Neoscopelidae to test the social selection-

diversity hypothesis.

LOPHIIFORMES

The superfamily Ogocephalioidea is comprised of two monophyletic groups, the Cera­

tioidea (11 families and 134-149 species) and the Ogocephalioidea (1 family with 62 species).

Bertelsen 1984, Pietsch 1984, Nelson 1994). The Ceratioidea are found from the subantarctic to

the subarctic and most adults dwell at meso or bathypelagic depths (Nelson 1994). The Ogo­

cephalioidea are found in tropical and subtropical waters. Most prefer mesopelagic depths but

some occur in shallow water. The two superfamilies are found in different habitats, violating the

methodology outlined above in which comparisons were excluded when the sister taxa reside in

different habitats. However, I would predict that the meso or bathypelagic habitat of the ceratioids

would be less heterogeneous than the shallow water habitat of the ogocephalioids, and therefore

has less geographic barriers to promote speciation. Thus, the difference in habitat biases the

comparison against the sexual selection-diversity hypothesis, and I have proceeded to include the

comparison.

Striking "reverse" sexual dimorphism is characteristic of the ceratioids (Nelson 1976,

1994; Bertelsen 1994). In the past, males and females have been described as different species.

Males, who do not feed as adults, are dwarfed, reaching less than five to ten percent of the size of the largest females. Pietsch (1976) describes three reproductive strategies utilized by ceratioid anglerfishes: obligatory sexual parasitism occurs in at least four families (the Ceratiidae, 215

Linophrynidae, Neoceratiidae, about 20% of the ceratioid species); facultative sexual parasitism

probably occurs in the Caulophrynidae and the oneirodid genus Leptacanthichthys; and the

Melanocetidae, Himantolophidae, Gigantactinidae, and at least some oneirodid genera, are non­

parasitic (at least 50% of the ceratioid species are non-parasitic). After metamorphosis, males

actively seek out females. Nearly all males are equipped with huge olfactory organs and these are

the only deepsea fish group with ftmctional eyes (T. Pietsch pers. comm.). Females probably

produce species-specific pheromonal displays that attract males from long distances and species-

specific luminescent signals from the ilicium that attract males from shorter distances (T. Pietsch

pers. comm.; Pietsch 1976).

There is no obvious sexual dimorphism in the Ogocephalidae (T. Pietsch pers. comm.;

Pietsch 1984, 1987). Mating habits of both groups are unknown (Breder & Rosen 1966; Pietsch

& Grobecker 1987).

ATHERINIFORMES

The Atheriniformes cannot be defined cladistically (Rosen &. Parenti 1981). Relationships

among the families, and the monophyly of many of the families are uncertain (White et al. 1984,

Parenti 1993). Allen (1980) combines the pseudomugilids with the melanotaeniids and Rosen &

Parenti (1981) provisionally accept that alignment. More, recently. Dyer & Chemoff (1996) place

the Belotinidae as sister to the Melanotaeniidae -t- Pseudomugilidae + Telmatherinidae. L.

Parenti (pers. comm.) does not agree with all of their characters but tentatively accepts this alignment. There are interesting parallels between the rainbowfishes of Australia and Madagascar

(Allen 1994). True "primary" freshwater species are largely absent in both areas and inland fishes have evolved relatively recently from marine ancestors. Several undescribed species may exist in both groups. 216

The colorful Melanotaeniidae, Pseudomugilidae, and Telmatherinidae (with a combined

species diversity of 85) are found in the freshwaters of New Guinea, northern and eastern

Australia, and parts of eastern Indonesia. They are laterally compressed and very colorful. They

are extremely sexually dimorphic in coloration and fin extensions (Allen & Cross 1982). The

genus Melanotaenia (the largest genus with 32 species) is closely related to the genus Glossolepis,

and is the most dimorphic. In addition, along with Chilatherina, they are considered to be the

most derived. Spawning occurs year round with local peaks of activity at the onset of the rainy

season. A relatively small number of eggs are deposited each day among aquatic vegetation.

Telmatherinerina ladigesi has a "peculiar and energetic" courtship (Allen & Cross 1982).

The Bedotiidae (9 species) are confined to the fireshwaters of Madagascar (Nelson 1994).

They are fusiform in shape, colorful, but not terribly sexually dimorphic (L. Parenti pers.

comm.). I found no references to their mating behavior.

CYPRINIDONTIFORMES APLOCHEHJDAE APLOCHEILINAE

The family Aplocheilidae is comprised of two lineages, the Aplocheilinae and the

Rivulinae (Nelson 1994). Both subfamilies include some extremely dimorphic species, and both

include some members that are termed "aimuals". In these, adults spawn during the rainy season

and the eggs survive dry periods buried in the substrate. The Aplocheilinae, in turn, consists of

two lineages, the Aphyosemion-Nothobranchus clade (225 species) of western and central Africa

and the Aplocheilus-Pachypanchax-Epiplatys clade (92 species) of India, Laurasia, and the Indo-

Pacific archipelago (Parenti 1981). Many species are poorly defined (Scheel 1990). Both groups appear to share the typical cyprinodontid mating behavior: males chase females, pair, an egg is 217

extruded, fertilized, and then attached to aquatic vegetation or buried in the sand, but there is little information available on either group (Scheel 1990). Both groups are colorful (Scheel 1990).

The species in the Aphyosemion-Nothobranchus clade have more rounded heads, are not surface-dwelling, are not particularly good swimmers, and do not form schools (Scheel 1990).

Members are both annual and nonannual (Parenti 1981). Many species are strikingly sexually dimorphic and dichromatic and many subspecies of Aphyosemion are reproductively isolated

(Scheel 1975, dbl ck; Haas 1976; Scheel 1990). Many species are also extremely variable morphologically and karyotj^jically (Scheel 1990). Males of the genus Notobranchius are especially dichromatic. In Nothobranchius guentheri, courtship is virtually absent, and pairings last only long enough to lay the egg (Haas 1976). Females will make the initial approach if a male does not see the female first. Dominant males aggressively interfere with reproductive efforts by other males and are differentially preyed upon by birds. In laboratory choice experiments, females approach males for spawning in response to the degree of intensity of red color of the tail fin which is best transmitted in the turbid pools in which they reside (Haas 1976).

Members of the Aplocheilus-Pachypanchax-Epiplatys are pike-like and surface dwelling

(Scheel 1990). All members are nonannual (Parenti 1990). Members are colorfiil but sexual dimorphism is not well-developed. Little other information is available.

POECILIIDAE

The Poeciliidae are comprised of three subfamilies, the Poeciliinae (live bearers; 194 species), the Fluviphylacinae (oviparous; 1 species), and the Aplocheilichthyinae (oviparous; 100 species; Nelson 1994; Parenti & Rauchenberger 1989). Poeciliids live in groups and females can store sperm for several months. Some poeciliid species exhibit no courtship, while in others, stereotyped male courtship displays and female acceptance postures precede copulation (Farr 218

1989). All courtship displays are visual and involve a combination of stereotyped swimming

motions and fin postures. Courtship is clearly not necessary for mating to occur but is suggested

to have evolved to facilitate female mate choice (Farr 1989). Male courtship is significantly

correlated with the degree of sexual dimorphism (Farr 1989) and females have been found to

discriminate among males on the basis of color, size, and motor pattern (reveiwed in Kodric-

Brown 1990).

In those species with no courtship, the male simply orients behind a female, swings the

gonopodium forward, and attempts to inset the gonopodial tip into the female's gonopore. This

behavior has no signal function and cannot be considered a display (Farr 1989). Elaborate male

coloration does not occur in the internally fertilized but egg-laying poeciliid, Tomeurus gracilis,

which is hypothesized to be basal to the remaining poeciliid species (Parenti 1981). The

hypothesized sister, the Anablepidae (9 species; Meyer & Lydeard 1993), do not have well-

developed sexual dimorphism either (Breder & Rosen 1966, Parenti 1981).

POECnJA

Within the Poeciliinae, the subgenus Poecilia of the genus Poecilia, can be divided into

two species complexes, the "high-fin" group (40 species: e.g., P. latipinna, P. petenensis, P.

velifera) and the "low-fin" group (9 species, e.g., P. chica, P. catemaconis, P. sphenops) with

P. formosa to be phenotypically intermediate (Rosen & Bailey 1963; Miller 1975, 1983).

The high-fm group is characterized by sexual dimorphism in which males possess a greatly

enlarged dorsal fm and are more brightly pigmented than the females. Within a species, there is

a large variation in male size and large males are aggressively dominant over small males. Small

males, however, are sexually mature and actively pursue females. All high-fin species exhibit a courtship display in which the dorsal fin is erected and presented to the female; the female 219

responds by remaining stationary and sometimes twisting the abdomen to accept a copulation.

Courtship behavior is correlated with size. Large males display more, and small males exhibit

a higher rate of gonopodial thrusting.

In the low-fin group, there is at most only slight sexual coloration differences (males may

have some yellow in the fins, A. Basalo pers. comm.) and most, if not all species, lack a

courtship display (Farr 1989 and references within). P. chica males use only gonopodial

thrusting, P. vivipara and P. sphenops lack a courtship display. It is unclear whether P. mexicana have a courtship display. There are no published data on sexual behavior of the remaining species.

XlPHOPHORUS

The genus Xiphophorus (17-26 species) is sister to the genus Priapella (3 species) based on both morphological and molecular phylogenies (A. Basolo pers. comm; Rosen 1979;

Rauchenberger 1989; Rauchenberger et al. 1990; Meyer et al. 1994; Borosky et al. 1995).

Species of the genus Xiphophorus are found in Atlantic drainages fi-om the Rio Grande to

Honduras. Males of many species of Xiphophorus possess a ventrally elongated caudal fin, the sword. Mate choice experiments have shown that females (of species with or without swords) prefer to mate with males with longer swords over males with shorter swords (Basolo 1990a,b;

1991, 1995).

Fishes of the genus Xiphophorus are commonly divided into the swordtails and platyfishes. This genus is the most complex group of poeciliids with regard to pigmentation, morphology and courtship behavior (Farr 1989). The platies are commonly divided into two lineages, the northern (3 species) and southeastern (5 species) platies (A. Basolo pers. comm.;

Rosen 1979; Rauchenberger et al. 1990; Basolo 1991; but see Meyer et al. 1994). The northern 220

platies exhibit very little sexual dimorphism (some color differences), males do not possess

swords, and two species have a courtship display (Farr 1989). The southern platies show a

variety of sex limited traits, including variable sexual dichromatism and differences in body

shape, and are variable for the presence of the sword among species (X. xiphidium and X. andersi

do not have a sword, they have a slight extension of the rays at the base of the caudal fin but lack

the color components of the sword) A. Basolo pers. comm.; Farr 1989; Basolo 1991, 1995. Some

species have a courtship display, while others exhibit primarily gonopodial thrusting (Farr 1989).

Similarly, the swordtails are conunonly divided into two lineages, the northern (9 species)

and southern (4-8 species) swordtails. Smaller males are often found in tributaries while larger

males are found under ledges in fast moving waters. Males of all species have swords, but of

varying lengths and many species are sexually dichromatic. Some species have a courtship display and some exhibit primarily gonopodial thrusting. Depending on the phylogeny followed, there either is (Rosen 1979; Rauchenberger et al. 1990), or is not (Meyer et al. 1994), a phylogenetic progression toward the complete sword in Xiphophorus, composed of all four sword components

(A. Basolo 1995).

The genus Priapella lives in small schools and inhabits rapidly flowing streams in southeastern Mexico. Priapella lacks the sword and there are no recorded color differences (A.

Basolo pers. comm.; Farr 1989).

GOODEIDAE

The family Goodeidae is mostly endemic to the Mesa Central of the Mexican plateau, where they have undergone an adaptive radiation of at least Miocene antiquity (reviewed in

Turner et al. 1983). The family is comprised of two lineages, the Goodeinae (36 species) and the

Empetrichthyinae (4 species); Farenti 1981; Miller «fe Smith 1986; Grudzien et al. 1992; Meyer 221

&. Lydeard 1993. The Goodeinae are euviviparous with an intromittent organ that is simpler than

in other cyprinodontoids (Breder & Rosen 1966; Lydeard 1993). They are diverse in body form

and foraging habits, and are strikingly sexually dimorphic. Most males are bigger, have fin

extensions, and have more brightly colored flns than females. Some of them show elaborate

courtship behaviors (Sabono et al. 1996). Species in the Empetrichthyinae have a very restricted

and relictual distribution among pools and springs in Nevada (Hubbs etal. 1974); there once may

have been more species (L. Parenti pers. comm.). They are oviparous, females are larger than

males, and they are not otherwise sexually dimorphic (Parenti 1981; Lydeard 1993; Nelson

1994). Parenti (pers. comm.) wonders whether, regardless of the differences in their geographic

distribution, the Empetrichthyinae would have ever been as species rich as the Goodeinae because

of the differences in their biology.

GASTEROSTEIFORMES SYNGNATHIDAE

The infraorder Syngnatha comprises the Pegasoidea and the Syngnathoidea (Nelson 1994).

Fritzsche (1984) suggests that the Pegasoidea is the primitive sister group to the Solenostomidae

and the Syngnathidae. Both the Pegasoidea and the Solenostomidae are monogamous and show slight sexual dimorphism (females are larger than males and have differentially shaped rostrums,

there is no sexual dichromatism; Barlow 1986; Herold & Clark 1994; A. Vincent pers. comm.).

The Syngnathidae are widely distributed in shallow water around the world, primarily in warm temperate to tropical areas (Nelson 1994). The family is comprised of the Syngnathinae

(215 species) and the Hippocampinae (35 species; A. Vincent pers. comm.; Nelson 1994). Mating in the Syngnathidae is characterized by an elaborate entwining courtship dance in which the female passes eggs repeatedly to the male who fertilizes and broods them in a pouch or beneath 222

the tail (Oir & Pietsch 1994). Herald (1959) describes increasing elaboration in the pouch within

the Syngnathinae and the Hippocampinae. There is an apparent association between the mating system and the sex roles: polygamous species show reversed sex roles whereas monogamous species exhibit "conventional" sex roles (Vincent etal. 1992). In the Syngnathinae, many, if not most, of the species are sex role reversed, polygynous, and sexually dimorphic. The female is often ornamented, brighter in color, and larger than the male. Pending further resolution of the relationships within the Syngnathinae (A. Vincent and A. Meyer in prep.), genera known to contain monogamous and sexually monomorphic species (Corythoichthys, Filicampus, Dunckero- campus, and Doryrhamphus and Hippocampus-, Vincent et al. 1992, Dawson 1985) were subtracted from the diversity estimate in the sister-taxa comparison.

The Hippocampinae all have conventional sex roles (Vincent 1994a, b). All but two of the species are monogamous and sexually monomorphic. H. obdominus is the only sexually di­ morphic sea horse, males are larger than females, more spotted and very brightly colored. H. breviceps is not obviously monogamous, individuals range widely and occur in groups (A.

Vincent pers. comm.).

PERCIFORMES PERCOIDEI SERRANIDAE ANTHHNAE

Baldwin & Johnson (1993) present preliminary evidence that the Serraninae are sister to a clade comprised of the Anthiinae (175 species) + the Epinephelinae (203 species; C. Baldwin pers. comm.; Baldwin 1990; Heemster & Randall 1993; Nelson 1994). Within the Serranidae, the primitive reproductive pattern is simultaneous hermaphroditism, as seen in the Serranus, while protogynous hermaphroditism has apparently evolved independently several times (Hastings 223

1981). Anthiines, and most of the ephinephelines, appear to be sequential protogynous

hermaphrodites (some of the later, e.g., Liopropoma, are presumably secondary gonochorists but

this remains to be determined; P. Hastings pers. comm.; Anderson et al. 1990; Randall 1994).

Basal lineages within the Anthiinae (e.g., Acanthistius, Tracypoma, Hypoplectrodes) tend

to be grouper-like; they are solitary, found in shallow water, carnivorous, and not very colorful

(C. Baldwin pers. comm.; Baldwin 1990). Cladistically derived groups, (e.g., Pseudanthias,

Rabaulichthys, Luzonicthys. Nemanthias, andAnatolanthias) are, in general, small, planktivorous,

schooling, and more closely associated with the bottom than are many other planktivores (C.

Baldwin pers. comm., Anderson et al. 1990; Randall 1994). They are Indo-Pacific and among

the most beautifully colored fish in the world (Randall 1994). Intermediate lineages contain

additional genera with solitary species and some deeper water schooling forms that may be quite

colorful {e.g., Anthias; Baldwin 1990). Basal and intermediate lineages are found in both the

Atlantic and Pacific. Comparisons within the Anthiinae await fiirther phylogenetic resolution (C.

Baldwin in prep).

Many of the cladistically derived lineages are sexually dimorphic. Males are larger than females (a consequence of sequential hermaphroditism) and differ in finnage and coloration {e.g.,

Pseudanthias with 45+ species; Randall 1994; Nelson 1994). Typically, males defend harems

(Randall 1994). Courtship, however, has only been described for three species (Thresher 1984 and references therein). Male defend territories either temporarily or permanently, and court females that arrive on the breeding grounds. To me, these descriptions appear to describe polygynandrous (or sequentially polygynous), rather than haremic, mating systems.

The Epinephelinae are shallow water, solitary, ambush predators (Randall 1994). Most are cryptically colored but some are brightly colored as well (e.g., Liopropoma, Grammistes; C.

Baldwin pers. comm.). They tend to group or pair spawn following a ritualized courtship 224

(Thresher 1984). Mating has been observed in only a few species. Males tend to be larger than

females (a consequence of sequential hermaphroditism), sexual dichromatism is slight, if present

at all, and additional morphological sex difference appear to be absent (Thresher 1984).

PSEUDOCHROMIDAE

Pseudochromids are small, reef-associated Indo-Pacific fishes (Johnson & Gill 1994).

They are small in size, and have relatively narrow distributions when compared with other marine

fishes (Gill & Woodland 1992). They are brightly colored, and many show pronounced sexual

dimorphism in finnage and coloration (Thresher 1984, Johnson & Gill 1994). They are probably

simultaneous hermaphrodites and probably have a similar mating system with egg guarding (of

a spherical egg mass) and long term pair bonds (T. Gill pers. comm.; described for four species

of Pseudochromis, Thresher 1984 and references therein). Males can only care for one egg mass

and must be able to manipulate it, the result being that males probably do not have multiple mates

(T. Gill pers. comm.). Whereas Mok et al. considers the Pseudochromidae sister to a clade

comprised of the Grammidae + Opistognathidae, Gill & Mooi (1993) find no characters that

corroborate these relationships.

The Pseudochromidae comprises four subfamilies (Nelson 1994). The Pseudochrominae,

which may be polyphyletic (76 species), is the primitive sister to the remaining subfamilies (T.

Gill pers. comm.). The Pseudoplesiopinae (25 species) is sister to the Anisochrominae (2 or 3 species) + Congrogadinae (22 species; T. Gill pers. comm.). Although the Pseudochrominae is

probably not monophyletic, there are recognizable clades within the clade (R. Mooi and T. Gill

pers. comm.). The subfamily is variable for sexual dimorphism (T. Gill pers. comm.). The genus

Pseudochromis is probably not monophyletic and is comprised of several lineages, some with

pronounced sexual dimorphism and others without (T. Gill pers. comm.). Basal lineages in the 225

subfamily do not appear to be sexually dimorphic (R, Mooi pers. comm.)- Comparisons within

the subfamily await further phylogenetic resolution (T. Gill in prep.).

The remaining subfamilies are each monophyletic (T. Gill in prep.). Members of the

Pseudochrominae are thought to be sexually dimorphic. Comparisons involving this family await

further biological information, however. The remaining subfamilies are sister taxa, the

Anisochrominae, which are sexually dimorphic, and the Congrogadinae, which show no sexual

dimorphism. This later subfamily, the eel blennies, differ from the other members of the family

in being very elongate.

CENTRARCHIDAE

The centrarchids are comprised of two groups of genera based on the number of anal

spines, Enneacanthus, Lepomis, and Micropterus fwith 20 species), and Acantharchus,

Ambloplites, Archoplites, Centrarchus, and Pomoxis (with 9 species; Nelson 1994). Members

of the family are endemic North American temperate freshwater fishes that are similar in form

and mating system (Johnson & Gill 1994). Males of most species hollow out a small depression

in the gravel or vegetation in which they care for the eggs and the young (Johnson & Gill 1994;

Nelson 1994). Mating is typically polygynandrous (or loosely sequentially polygynous, although sometimes monogamous), both males and females spawn with multiple partners, and sneak spawning is commonly observed (Weigmann et al. 1992; Gross 1982). Adult centrarchid fishes exhibit a wide range of lateral body pigmentation as adults which evolve primarily by addition or deletion of homologous elements (Mabee 1995; who did not consider sexually dimorphic pigment patterns).

The basses {Micropterus with 6-7 species), primitive sister to the remaining genera, are larger in size and are not sexually dimorphic (P. Mabee pers. comm.; Breder & Rosen 1966; 226

Lauder & Humphries 1992; Mabee 1993). They are sister to two clades, the lineage comprised

of Lepomis (11 species) + Enneacanthus (3 species), and a lineage comprised of the remaining

genera (9 species). Lepomis, the sunfishes, is smaller in size than the basses, sexually

dichromatic, and at least one species (L. cyanellus) is known to court with sound. Enneacanthus

is smaller in size than Lepomis and shows little, if any, sexual dimorphism.

PERCIDAE

Percid fishes are freshwater derivatives of a marine perciform that have undergone a

tremendous radiation in North America of relatively recent age (Pliocene or later; Page 1985).

There are two differing hypotheses regarding relationships within the Percidae. Collette and

BSnSrescu (1977) recognize two subfamilies, the Percinae (153 species) and the Luciopercinae

(9 species). The Percinae are thought to contain the Percinia (8 species) with Perca +

Gymnocephalus and Percarim, and the Etheostomatini (145 species) with Ammocrypta/Crystal-

laria + Percina and Etheostoma. The Luciopercinae is comprised of Stizostedion and Zingel +

Romanichthys. Wiley (1992) presents an alternative classification, based on osteology, which

places Perca as the sole member of Percinae and all remaining genera in the Etheostomatinae.

Other classifications of the family, based on scales, are presented in Cobum & Caglione (1992,

cited in Nelson 1994).

Based on either classification there is lineage (or lineages) of small, brightly colored, sexually selected and sexually dimorphic fish that has been independently derived from larger,

dull-colored, group spawning, and non sexually dimorphic fish (Page 1985; Nelson 1994).

Species in these basal lineages, e.g., Perca, Percarina, Gymnocephalus, and Stizostedion are

broadcast spawners or "stranders" (eggs encased in gelatinous strands), and mating is best described as scramble competition; a single female is accompanied by a number of males, eggs 221 are released, fertilized, and attached to aquatic vegetation or the substrate (Page 1985, Craig

1987). Spawning in walleye is nocturnal. Some males are territorial {e.g., S. lucioperca).

Within the Etheostomatini of Collette & B5n5rescu (1977) or the Etheostomatinae of

Wiley (1992), the genus Etheostoma (103 species) is sister to the Percina (39 species; Page

1985). The position of the genera Ammocrypta (6 species) and Crystallaria (1 species) is unresolved regarding its inclusion (Page 1985, Simons 1992) or exclusion (Bruner 1996) from

Etheostoma. Neither resolution affects the conclusions of the comparison tallied here. Etheostoma shows a variety of reproductive strategies that range in complexity (Page 1983, 1985). The most primitive of which is egg burying in which there is no parental care beyond some territorial behavior. The most derived parental care pattern is egg clumping, or clustering, in which males guard territories and eggs. Sexual dimorphism ranges from low to extreme (Page 1983, 1985).

Percina are egg buriers (Page 1983, 1985). Etheostoma as a whole, is more dimorphic than

Percina, which has some dimorphic species, but none as dimorphic as those in Etheostoma (Page pers. comm.. Page 1983). More detailed comparisons await further phylogenetic resolution.

Page (1985) analyzes the evolution of percid reproductive strategies in a phylogenetic context and shows a trend toward increasing reproductive complexity. These trends include a suite of correlated traits; the development of territoriality, invasion of small streams, decrease in time to reproductive maturity, decrease in promiscuity, increase in parental care, and an increase in sexual dimorphism (corroborating the findings of Winn 1958). Page found that sexual dichromatism is most extreme in egg buriers, a reproductive strategy intermediate in complexity.

Interestingly, some of the more derived groups show a secondary loss of complex reproductive strategies and a reversal of sexual dimorphism, e.g., Ozarka and Boleichthys, are nonterritorial and females are larger than males. Percid relationships are a current area of active research {e.g.,

Bruner 1996; Shaw 1996; Turner 1996; and others). This group presents one of the best 228

opportunities available for multiple tests at the subgeneric level of the sexual dimorphism- diversity hypodiesis, correlated with detailed information produced on reproductive strategies.

POMACANTHIDAE AND CHAETODONTIDAE

The Pomacanthidae (74 species) and Chaetodontidae (114 species) were, until recently, combined in the same family (Nelson 1994). They are primarily Indo-Pacific, reef-dwelling fishes, known for their brilliant coloration. Both families spawn pelagic eggs and have relatively large geographic distributions. Interestingly, duration of larval stage and adult size show a strikingly poor correlation with species range in pomacanthids (Thresher & Brothers 1985).

The chaetodontids display a wide range of social groups, from home-ranging and mono­ gamous pairs to large aggregations and group spawning in planktivorous species (Reese 1975;

Burgess 1978; Thresher 1984; Hourigan 1989). However, I found no reports of sexual di­ morphism, except in C. (Prognathodes) aculeatus in which males are 7% larger in the Caribbean

(Neudecker & Lobel 1982; Thresher 1984). Neudecker (1989) discusses the use of chaetodontid color patterns in social signalling.

Most of the pomacanthids studied to date appear to be protogynous hermaphrodites

(Moyer 1990). They have highly variable mating systems, both between and within species

(Neudecker & Lobel 1982; Thresher 1982, 1985; Moyer etal. 1983; Moyer 1990). This appears to be due, in part, to variation in population density across a species' range. Many species show mating patterns that range geographically from territorial monogamous pairs, to polygynandry, to harems or leks (Thresher 1982; Moyer 1990). Moyer (1990) suggests that most pomacanthids display the potential for polygynous, single male, multi-female social groups arranged in size- dominant hierarchies; most display similar motor patterns involved in courtship, permanent and/or temporary dichromatism, and sexual size dimorphism with males larger than females. 229

Divergence from the "general" type includes the multi-male system of some Genicanthus, lekking

in Holocanthus passer, and promiscuity in Pomacanthus arcuatus.

Sexual size dimorphism in the pomacanthids is widespread, males are larger than females,

and may be universal in the family Ginked to sequential protogynous hermaphroditism; Thresher

1982). In contrast to size dimorphism, sexual dichromatism occurs sporadically and is not clearly

related to social organization (Thresher 1982; Moyer et al. 1983; Moyer 1990). Despite

numerous studies, this conclusion is understandable given the behavioral flexibility manifest

within the family. Whereas many traits suggest that the pomacanthids should be more diverse

than the chaetodontids, e.g., the presence of polygynous mating systems, protogynous herm­ aphroditism (suggesting more intense competition for mates), and sexual dimorphism, the comparison does not support the sexual dimorphism-diversity hypothesis. I was, however, not happy with the comparison at the familial level because of the variation in sexual dimorphism expressed within the Pomacanthidae. Following the methodology outlined above, and Maddison

(1996), I searched at shallower nodes of the tree for better reconstructions.

Blum (1989) considers the Pomacanthidae to consist of two subfamilies, the

Holocanthinae and the Pomacanthinae. The subfamily Holocanthinae consists of two lineages,

Genicanthus (9 species) -1- Centropyge (29 species) and a clade which comprises Apolemichthys

(6 species), Pygoplites (1 species) and Holocanthus (8 species; Allen 1978, Nelson 1994). The following was obtained from Allen (1978), Thresher (1982, 1984), Moyer et al. (1983), and

Moyer (1990). Species within Genicanthus are herbivorous and those within Centropyge, plank- tivorous; both tend to occur in large aggregations at slightly deeper depths than the remaining genera. Within the family, sexual dichromatism is most well-developed in these two genera and is especially so in Genicanthus while variable in Centropyge. The remaining genera are benthic foragers on invertebrates. Species in the Apolemichthys clade, as well as in all other genera in 230

the Pomacanthinae, show slight (e.g., Pygoplites, Holocanthuspasser. Chaetodontoplus, Poma- canthus) or no (remaining Holocanthus species) sexual dichromatism.

Clearly, the sexual dimorphism-diversity hypothesis requires further testing within these lineages. Studies of Centropyge would be especially rewarding.

LABROIDEI POMACENTRIDAE

Relationships among and within the three subfamilies of pomacentrids are generally unresolved (G. Hoelzer pers. comm.). Classification is complicated by numerous species com­ plexes and color patterns that vary with individuals and between localities (Nelson 1994). As far as is known, pomacentrids are permanently or temporarily (males) territorial with male or bi- parental care of eggs (Thresher 1984). Courtship typically consists of a suite of motor, sonic, and color patterns (Thresher 1984; Thresher & Moyer 1983).

The Amphiprionae (28 species) are comprised of protogynous and protandrous herm­ aphrodites (Sadovy ms; Nelson 1994). Typically, the mating systems is monogamous although, in some denser populations, polygynous, and multi-male multi-female systems have been observed

(Barlow 1986). Because of the permanence of the association of individuals at an anemone, there is little opportunity for female mate choice and little opportunity among males to mate with other females (Thresher 1984). They are the most colorful of all damselfishes. Sexual size dimorphism is correlated with hermaphroditism. There are scattered records of slight and inconsistent sexual dichromatism {e.g.., A. perideraion, Allen 1972). In A. clarkii, sexual dichromatism is a sign of sex and dominance and is more pronounced in denser populations that show a tendency to poly­ gyny- 231

The Chrominae (87 species) are midwater planktivores that generally occur in

aggregations (Allen 1975; Nelson 1994). Some species are protogynous hermaphrodites (Coates

1982; Sadovy ms). During spawning, males are temporarily, or rarely permanently, territorial

(reviewed in Thresher 1984). They are generally polygynandrous, but because of the large size

of the aggregations, there is a greater opportunity for polygyny among males than in either of the

other subfamilies. The Chrominae tend to be more brighdy colored than the Pomacentrinae and

courtship displays are more pronounced. Permanent sexual dimorphism is slight or non-existent

but temporary nuptial coloration may be well developed (sometimes in both sexes; Thresher

1984). The use of sound during courtship has been observed (e.g., Dascyllus, Mann & Lobel

1995). In Dascyllus (9 species) protogynous hermaphroditism is associated with relatively

permanent social groups at isolated coral heads with haremic mating, and gonochorism is

secondarily derived (Godwin 1995). Haremic species appear to be sexually monomorphic,

perhaps correlated with a reduction in the intensity of sexual selection among these relatively

permanent social groups (Coates 1982). The Lepidozyginae (1 species) occurs in large schools

and are considered most closely aligned with the Chrominae.

The Pomacentrinae (199 species) is comprised of species that are benthic foragers that

are permanently territorial, with less polygyny opportunity among males, and mid-water

planktivores that are temporarily territorial (Allen 1975; Thresher 1984). Comparisons between

these groups await further phylogenetic resolution. Benthic species tend to be drab in color

{Glypidodontops is an exception) whereas midwater species are brighter (Allen 1975). Permanent sexual dimorphism is slight (e.g., Chrysiptera, Glyphidodontops), or non-existent, but temporary

nuptial coloration is common and the use of sound during courtship has been observed (e.g.,

Atlantic Stegastes, Myrberg 1972, 1986). In Glyphidodontops, Thresher & Moyer (1983) found

no correlation between the type of sexual dichromatism and the intensity of sexual selection but 232 found an inverse correlation between the development of sexual dichromatism and courtship complexity.

The sexual dimorphism-diversity hypothesis requires further testing within these lineages.

Studies of Pomacentrus, Dascyllus, or Glyphidodontops may prove especially rewarding. Pending further resolution, I can compare the monogamous Amphiprionae to either, or both together, of its temporarily sexually dichromatic relatives. For the most conservative estimate, relative to the sexual selection-diversity hypothesis, I compare the Amphiprionae to the Chrominae + Lepio- zyginae in the statistical calculations.

CICHLIDAE

The cichlid fishes of the Great Lakes of East Africa is the most spectacular example of an explosive speciation and adaptive radiation within a single vertebrate family, perhaps totalling over 1500 species (McKaye et al. 1984; Nelson 1994). Dominey (1984) and Mayr (1984) were the first to suggest that this unusual diversity may be due, in part, to sexual selection, which drives the rapid evolution of male color pattern and results in prezygotic reproductive isolation

(see Turner 1994 for a recent review). However, this hypothesis has not been explicitly tested.

Conventionally, cichlids are divisible into two mating types (reveiwed in Barlow 1991;

P. Reinthal pers. comm.). Substrate spawners are predominantly monogamous (although some are haremic, e.g., several lamprologines), relatively isomorphic (males may be slightly bigger but sometimes dimorphism is extreme, e.g., the dwarf species in the neotropical genera

Nannocara and Apistogramma), and both parents guard the eggs and larvae in a nest (although the parents invest differently). Mouthbrooders are predominantly polygynous (although several species are monogamous), usually dimorphic (males are usually, but not always, larger and more 233

colorful) and in the vast majority of species the female carries the eggs and larvae in her mouth.

Mating is typically brief and thus no long-term pair bonds are formed.

Substrate spawning is the primitive condition and is common in most of the Madagascar

and neotropical fauna (Barlow 1991; Stiassny 1992; P. Reinthal pers. comm.). Mouthbrooding

has apparently evolved several times independently from substrate spawning and sexual

dimorphism has arisen and been numerous times. Both situations provide many possible ways to

test the sexual selection-diversity hypothesis (see Table 8). The most general of these is outlined

below.

The haplochromine cichlid fauna of Lakes Malawi, Victoria and Tanganyika are sexually

dimorphic in color (especially the Lake Victoria flock, 300+ species, and the mbuna in Lake

Malawi, 200+ species) and in "bower" construction (the sand dwelling flock in Lake Malawi,

200+ species). All but one studied species are maternal mouthbrooders (Fryer & lies 1972,

reviewed by Barlow 1991) and most are strongly sexually selected (not often supported by hard

evidence but is probably a correct supposition, E. Verheyan pers. comm); monogamy is

uncommon (Barlow 1991). Most common is the defense of a display site by the male {e.g., the

mbuna) and lekking (e.g., the sand-dwelling Malawi species). Females tend to aggregate in the

water column and visit and spawn with one or more males. Monophyly has been established by

Meyer et al. (1990), Bowers et al. (1994), Moran et al. (1994) and is reviewed by Meyer et al.

(1994). Behavioral studies have shown that females discriminate among males on the basis of color in the mbuna {e.g., Pseudotropheus zebra, Holzberg 1978) and bower characteristics in the sand dwelling cichlids {e.g., Lethrinops lituris group, McKaye et al. 1990); reviewed in McKaye

(1991).

The sister to the Haplochromini is the Tropheini (Sturmbauer & Meyer 1992). This

Tanganyikan tribe itself consists of two lineages, Tropheus and Simochromis (Sturmbauer & 234

Meyer 1992, Kocher et al. 1995). Tropheus is colorful, but not sexually dimorphic (Sturmbauer

et al. ms). They are maternal mouthbrooders and strictly confined to rock habitats. They seem

to reside in densely packed populations in which both sexes are territorial (Sturmbauer et al. ms).

Tropheus form temporary pairs in the territory of the male and the female leaves the male's

territory after spawning (Sturmbauer et al. ms). Species diversity ranges from five (Axelrod

1993) to six (Poll 1986), and more than 70 distinctly colored races (Schupke, pers. comm in

Sturmbauer et al. ms).

Simochromis live in schools and are much more mobile than either Tropheus, or the

outgroup, the eretmodines (Brichard 1989; Sturmbauer et al. ms). Only dominant males hold

territories. They are less gaudy than Tropheus but are sexually dichromatic (Sturmbauer et al.

ms). There are six species with more expected to be described (Brichard 1989; Axelrod 1993).

Tropheus and Simochromis themselves represent a sister comparison which, depending on the species diversity estimate used, is resolved either ambiguously or in support of the sexual selection-diversity hypothesis. I use the more conservative estimate, relative to the sexual selection-diversity hypothesis {Tropheus with six species), in the statistical calculations. Using the outgroup, the eretmodines, to polarize the character states of die ingroup, 1 consider the sexual dimorphism of Simochromis to be derived. Thus, for the sister-taxa comparison tally, I use die sexual dimorphism character state of Tropheus to categorize the Trophieini (see Methods). (No,

I'm not satisfied with this either. I need to get comparisons within the Haplochromini and leave the Tropheini alone as dieir own comparison.)

The outgroup to the Haplochromini and the Tropheini is the Eretmodini (Sturmbauer &

Meyer 1992). They are small in size and the only group of cichlids which are adapted to living in the surf zone (Brichard 1989). Most eretomodines (it has not been reported for Simochromis malieri) are paternal mouthbrooders (Sturmbauer et al. ms). They live in permanent pairs and 235 are sexually monomorphic. There are three genera and four species (Sturmbauer et al. ms).

Numerous geographically isolated population have been described for all four species, but color differences among populations are less pronounced than in Tropheus (Sturmbauer et al. ms).

The sexual selection-diversity hypothesis requires further testing in cichlids. Comparisons extracted firom lineages showing variation in the intensity of sexual selection or sexual dimorphism, such as the haplochromines (C. Sturmbauer in prep.) or lamprologines, or between the sexually dimorphic dwarf neotropical genera Nannocara and Apistogramma and their relatives, should be especially rewarding.

BLENNIOIDEI

The suborder Blennioidei comprises six families of small, shallow-water and bottom- dwelling fishes (Nelson 1994, Springer 1994). The vast majority spawn demersal eggs (save for some viviparous labridsomids and clinids). The eggs are deposited in protected areas where they are fertilized and cared for by the male (Springer 1994). Larvae of some families have an extended pelagic existence {e.g., Blenniidae) while the larvae of others stay close to reefs {e.g.,

Chaenopsidae, Tripterygiidae, Labridsomidae, Dactyloscopidae; Matarese et al. 1983; Brogan

1994).

Because of their similar reproductive behavior, mating systems are expected to be fairly consistent among the families (P. Hastings pers. comm.). In general: females are mobile and able to choose among males. Males court females from their territories with motor and visual displays

(color, fin extensions, and various head ornamentation). Both males and females may mate multiply. The resulting mating system may best be described as resource defense polygyny

(Hastings 1988). In a number of species it has been shown that females prefer to mate with large males with good shelters and long tenure (reviewed in Kodric-Brown 1990). Interestingly, In 236

Acanthemblemaria crockeri, the nuptial coloration of males shows no correlation with reproductive success and courtship intensity is negatively correlated (Hastings 1988). Hastings emphasizes that this is perplexing in the light of their seemingly high cost; it may indicate that males which do not meet the criteria of females may attempt to compensate by increasing the vigor of their display. It may also be a trait that varies over time depending on whether or not the male is tending eggs.

Preliminary evidence on relationships among the families (Hastings & Springer unpub. data) suggest that the Tripterygiidae (115 species) is the primitive sister to the remaining families

(Holleman & Buxton 1993 suggest that the Tripterygiidae may be sister to the Clinidae). The remaining families form a trichotomy: the Dactyloscopidae (46 species; Dawson 1982);

Blenniidae (345 species) + Chaenopsidae (65 species; Springer 1993); and the Clinidae (80 species) + Labridsomidae (102 species). Sexual dimorphism is roughly consistent with these lineage designations: slight in the tripterygiids and dactyloscopids, moderate in the clinids and labrisomids, and well-developed in many species of blenniids and chaenopsids. Moreover, increasing dimorphism is associated with increasing lineage diversity. Pending further informa­ tion, there was no discemable phylogenetic pattern regarding sexual dimorphism within any of the following families, except for the Chaenopsidae. Further studies of the blenniids would be especially interesting.

Tripterygiids show their greatest diversity in New Zealand (Fricke 1994). The only reported sexual dimorphism is temporary nuptial coloration and this is not often well developed

{e.g., Axoclims carminalis shows intense nuptial coloration; Thresher 1984; De Jonge & Videler

1989; Fricke 1994).

Dactyloscopids are found primarily in warm seas of the western hemisphere (Nelson

1994; Doyle 1996). They are drab in color. There are some reports of some permanent sexual 237

dichromatism and sexual dimorphism in finnage (some associated mth male incubation of the

eggs within the pectoral fins; Thresher 1984; Dawson 1974, 1982).

Labridsomids are found in the New World with species diversity greatest in Central and

South America (Nelson 1994). Monophyly of the group is uncertain (George & Springer 1980;

Stepian et al. 1993; Springer 1993). In general, males may be larger than females, show

temporary nuptial coloration, and have minor morphological differences (tentacles, jaws, scales) and anal fin morphology (Hubbs 1952; Springer 1959; Stephens & Springer 1974; Thresher

1984). In some species, females may be more brightly pigmented (Stephens & Springer 1973).

Clinids are primarily found in temperate waters of both Northern and Southern hemispheres, and especially South Afnca and Australia (Stepian 1992; Stepian et al. 1993;

Springer 1993; Nelson 1994). In general, males may be larger than females, show temporary nuptial coloration, and have minor morphological differences (head filaments, jaws, scales) and anal fin morphology (Hubbs 1952; Penrith 1969, 1970; George & Springer 1980; Thresher

1984). In some species, females may be more brightly pigmented (Stephens & Springer 1973).

Blermiids are primarily tropical and subtropical (Smith-Vaniz 1990; Nelson 1994). Most blenniids are cryptically colored but many are extremely brightly colored (Springer 1994). Some species exhibit two or three color patterns so strikingly different that each pattern has been described as a different species. Many species change their basic pattern to achieve an intraspecific signal function when appropriately motivated, as in the case of competition or spawning (Abel 1993). Sexual dimorphism is well-developed in many species. Males are often longer than females and some show permanent sexual dichromatism and/or temporary nuptial coloration. There are numerous morphological differences {e.g., cirri, meristics, teeth, jaws, head crests, tentacles, fin glands) and differences in anal-fin morphology (Springer 1971; Springer & 238

Gomon 1975; Springer 1972; Smith-Vaniz 1976; Thresher 1984; Springer 1988; Williams 1990;

Abel 1993).

The chaenopsids are an inquiline (tube-dwelling), amphi-American family (Stephens 1963;

Hastings & Springer 1994; Nelson 1994). Sexual dimorphism in the basal lineages, Neodinus (9

species), Mccoskerichthys (1 species) and Stathmonotus (6 species) is least known but appears to

be slight. Neodinus males have longer jaws and Stathmonotus shows slight sexual size dimorphism, differences in the shape of the head and jaw, and sexual dichromatism (Hastings &

Springer 1994). The unpublished work of Hastings summarizes sexually dimorphic traits for all other species in the family. This is the first instance where differences in sexual dimorphism between sister lineages can actually be quantified.

Sexual dimorphism in the Acanthemblemaria clade (20 species) is generally slight, reduced or lacking (0-9 sexually dimorphic characters). Sexual dimorphism in the Chaenopsis clade (25 species) varies from none to moderate (0-20 or more characters). Sexual dimorphism in the Coralliozetus clade (18 species) varies from none to well developed (1-20 or more sexually dimorphic characters). Due to the variation in sexual dimorphism within each lineage, no comparisons were attempted. However, each lineage provides numerous possible sister taxa comparisons. The following follows Hastings (pers. comm. and unpub. data) with the added caution that additional data on live and nuptial coloration are needed as well a way to discriminate between sexually dimorphic characters involved in social displays with those associated with differential shelter use of males and females.

The members of the genus Ekemblemaria (3 species) are secretive. They show 4-6 sexually dimorphic traits including permanent sexual dichromatism (Hastings 1992). Most members of the genus Acanthemblemaria (17 species) show none, or 1-3, sexually dimorphic characters. However, A. crockeri is permanently sexually dimorphic over most of its range and 239

shows 7-9 sexually dimorphic characters, A. macrospilus is slightly permanently sexually

dichromatic and shows 7-9 sexually dimorphic characters, and A. balanorum shows 4-6. Both

males and females in both lineages reside in shelters.

The genus Cirriembletmria (1 species) is dramatically sexually dimorphic (7-9 sexually dimorphic characters). There is no data on shelter occupancy for Cirriemblemaria (A. Kerstitch pers. observation to P. Hastings indicates that females may not reside in shelters, although this remains to be confirmed). Members of the genus Emblemariopsis are moderately dimorphic, most showing 4-6 or 7-9 sexually dimorphic characters. There is little information on shelter occupancy in this genus as well, although A. Acero (pers. observation to P. Hastings) has found females of one species residing out of shelters, on brain corals.

The genus Coralliozetus (6 species) shows some of the most extreme sexual dimorphism and dichromatism in the family, all species show 20 or more sexually dimorphic characters. Only males reside in shelters during the spawning season. The genus Protemblemaria shows moderate sexual dimorphism, 7-9 sexually dimorphic characters. Both males and females reside in shelters.

ACANTHUROIDEI ACANTHURIDAE

Relationships among the acanthuroid families, a primarily Indo-Pacific clade that is also conspicuous in the Western Atlantic, are well resolved (Tyler et al. 1989; Lacson & Nelson

1993; Winterbottom 1993). Most have a specialized and long larval stage and subsequently species have relatively large geographic ranges (Lacson & Nelson 1993; Nelson 1994). Some spawn pelagic eggs, others spawn demersal eggs (e.g., Ephippidae and some Siganidae; Leis &

Richards 1983; Lacson & Nelson 1993). Spawning itself has rarely been observed in any species

(Thresher 1984). All basal lineages appear to be sexually monomorphic (Thresher 1984). 240

The Acanthuridae (72 species) are primarily Indo-Pacific. The family shows a variety of

mating systems between and within species (group spawning, monogamy, polygynandry, and

harems) which probably vary with population density (Robertson et al. 1979, Robertson 1983,

Thresher 1984 and references therein). Acanthurids vary widely in the type and degree of sexual

dimorphism that they exhibit (in size, color, and morphology; Robertson 1983; Thresher 1984).

There is no discemable phylogenetic signal, nor correlation, among mating systems and the

intensity of sexual selection, which is understandable given the aforementioned behavioral

flexibility (Robertson ms). Beside sexual size dimorphism, the Nascinae are the only permanently

dimorphic group (Thresher 1984). Haremic species tend to have larger males and show size

assortative mating; isomorphic species tend to have group spawning (Robertson et al. 1979;

Robertson 1983; Robertson ms). Temporary sexual dichromatism (in males and sometimes

females) is widespread (Thresher 1984). Pair spawning males often, though not invariably,

undergo a specific color change whereas group-spawning males develop a distinctive color pattern

that is different to, and often more conspicuous than, that developed by pair-spawning males

(Robertson 1983). Comparisons within the family await further phylogenetic and biological

information.

Little is known about the biology of the Zanclidae (1 species; Thresher 1984). They are

commonly seen in pairs or small groups and it is likely that spawning is in pairs. I have no

mention of any sexual dimorphism. Pending further resolution within the Acanthuridae, I compare the Zanclidae to the Acanthuridae (while this is not particularly satisfactory, the conclusion is robust, even if all basal lineages are combined as a giant polytomy and then compared to the Acanthuridae). 241

ANABANTOIDEI BELONTDDAE

Liem (1963) established three subfamilies, which represent the three major evolutionary lines: the Macropodinae (siamese fighting fishes and paradisfishes, with 32 species), the

Trichogastinae (gouramies, with 12 species), and the Belontiinae (combtail gouramies, with 2 species). Relationships among these lineages are under study by S. Norris (P. Hastings pers. comm.).

In most anabantoids, the male builds a nest of floating bubbles (females in some species may help briefly and at least two species of Macropodinae and one of Trichogastinae oral incu­ bate; Nelson 1994). Eggs are deposited (after which the female sometimes collapses!) and the male exhibits parental care. The belontiids and ospronemids are sister groups (Lauder & Liem

1983). Males in the later tend to be brighter, have fin extensions, and thickened lips during the spawning season. Information on mating and sexual dimorphism is taken ft-om Breder & Rosen

(1966); Forselieus on order.

In the Macropodinae, sexual dimorphism is well-marked in Macropodus, in male fins and nuptial coloration. Ctenops is reported to make courtship sounds (this species shows little marked sexual dichromatism). Male Betta splendens have brilliant colors and finnage. In the Triogastinae,

Trichogaster trichopterus is monochromatic, Colisa spp. is sexually dichromatic and has fin extensions (but Breder & Rosen 1966 describe these as less marked). I have no information on sexual dimorphism in the Belontiinae. Clearly, more information on sexual dimorphism is needed before finalizing this comparison. Here, I combine the Belontiinae and the Trichogastinae to give the most conservative estimate, relative to the sexual selection-diversity hypothesis, in the statistical calculations. 242

APPENDIX C

CHARACTERS, AND CHARACTER STATES

1. d-signal tn-pattern 6. d-pattem f-anterior dorsal f 0: absent 1: present 0: slant 1: curved 2. d-signal f-pattem 2: de-curved 0; absent 1: present 3: solid

3. sig-area m-dorsal fin 7. d-melan m-anterior dorsal 0: no signal area 0: absent 1: n 1: present 2: m 3: IV 8. d-melan f-anterior dorsal 4: V 0: absent 5: VI 1: present 6: Vn 7: Vm 9. dm-Ioc m-anterior dorsal fin 8: IX 0: distal 9: X 1; mid 2: proximal 4. sig-area f-dorsal fin 3: not applicable 0: no signal area 1: II 10. dm-loc f-anterior dorsal fin 2: III 0: distal 3: IV 1: mid 4: V 2: proximal 5: VI 3: not applicable 6: VII 7; VIII 11. d-carot m-anterior dorsal 8: IX 0: absent 9: X 1: present

5. d-pattem m-anterior dorsal fin 12. d-carot f-anterior dorsal 0: slant 0; absent 1: curved 1: present 2: de-curved 3: solid 13. dc-loc m-anterior dorsal fin 22. d-irid f-anterior dorsal fin 0; distal 0; absent 1: mid 1: present 2; proximal 3; not applicable 23. di-num m-anterior dorsal fin 0: none 14. dc-loc f-anterior dosal fin 1: few 0: distal 2: some 1; mid 3: lots 2; proximal 3: not applicable 24. di-num f-anterior dorsal fin 0: none 15. d-clear m-anterior dorsal 1: few 0; absent 2: some 1: present 3: lots

16. d-clear f-anterior dorsal 25. di-area m-anterior dorsal 0: absent 0: not applicable I: present 1: 111 2: IV 17. dc-loc m-anterior dorsal 3; V 0: distal 4: VI 1; mid 5: Vn 2: proximal 6: vn 3; not applicable 26. di-area f-anterior dorsal 18. dc-loc f-anterior dorsal fin 0; not applicable 0; distal 1: m 1: mid 2: IV 2: proximal 3: V 3: not applicable 4: VI 5: vn 19. d-spot m-anterior dorsal 6: vn 0: absent 1: present 27. br-pattem m-branchiostegals 0; uniform 20. d-spot f-anterior dorsal 1: bars 0; absent 2: spots 1: present 28. br-pattem f-branchiostegals 21. d-irid m-anterior dorsal fin 0: uniform 0; absent 1: bars 1: present 2; spots 29. br-color m-membranes 37. md-color m-anterior body 0: uniform 0: reddish-orange 1; dark distal margin 1: brown 2; dark wide distal margin area 2: orange-brown 3: faint outline 30. br-color f-membranes 4: heavy outline 0: uniform 5: spot 1: dark distal margin 6: brown-orange 2; dark wide distal margin area 38. md-color f-anterior body 31. jaw m-lower 0: reddish-orange 0: uniform 1: brown 1: spot 2: orange-brown 3: faint outline 32. jaw f-lower 4: heavy outline 0; uniform 5: spot 1: spot 6: brown-orange

33. body m-general pattern 39. I-pattem m-anterior body 0: dense 0: dense 1: open 1: moderate 2: open 34. body f-general pattern 0; dense 40. I-pattem f-anterior body 1: open 0: dense I: moderate 35. md-pattem m-anterior body 2: open 0; speckled 1: dashes 41. I-color m-anterior body 2: blobs 0: reddish-orange 3: blotches 1: brown 4; bands 2; orange-brown 5: broken blotches 6: varigated 42. I-color f-anterior body 0: reddish-orange 36. md-pattem f-anterior body I: brown 0: speckled 2: orange-brown 1: dashes 2: blobs 43. I-irid m-anterior body 3: blotches 0: absent 4: bands 1: present 5: broken blotches 6: varigated 44. I-irid f-anterior body 53. cheek m-pattem 0: absent 0: uniform 1: present 1: medium-sized blotch 2: large spot 45. face m-pattem 0; iiniform 54. cheek f-pattem 1: chin lighter 0: uniform I: medium-sized blotch 46. face f-pattem 2: large spot 0: uniform 1: chin lighter 55. ch-loc m-cheek spot 0: anterior 47. f-mel m-face coloration 1: mid 0: none 2: posterior I: few 3; not applicable 2: many 56. ch-loc f-cheek spot 48. f-mel f-face coloration 0: anterior 0: none 1: mid 1: few 2: posterior 2: many 3: not applicable

49. f-carot m-face coloration 57. op-pattem m-operculum 0: none 0: uniform 1: faint 1; spot 2 dark 2: mottled

50. f-carot f-face coloration 58. op-pattera f-operculum 0: none 0: uniform 1; faint 1: spot 2: dark 2; mottled

51. f-irid m-face coloration 59. op-color m-operculum 0: none 0: not applicable 1: few I: faint 2: many 2: dense 3: orange-brown 52. f-irid f-face coloration 0: none 60. op-color f-operculum 1: few 0; not applicable 2; many 1: faint 2: dense 3: orange-brown 61. c-supraorbital m-cirri 71. sp-color m-post. sp-dorsal 0: uniform 0: reddish-orange 1: striated I: orange-brown 2: olive 62. c-supraorbital f-cirri 0: uniform 72. sp-color f-post. sp-dorsal 1: striated 0: reddish-orange 1: orange-brown 63. c-nasal m-cirri 2: olive 0: uniform 1: striated 73. so-pattem m-soft dorsal 0: uniform 64. c-nasal f-cirri 1: Igt. internal, dk distal stripe 0: uniform 2; dark distal stripe only 1 striated 74. so-patten f-soft dorsal 65. p-pattem m-posterior body 0: uniform 0: dense I: Igt. internal, dk distal stripe 1: open 2: dark distal stripe only

66. p-pattem f-posterior body 75. so-color m-soft dorsal rays 0: dense 0: reddish-orange 1: open 1; orange-brown 2: mixed 67. p-color m-posterior body 3: red 0: reddish-orange 1: brown 76. so-color f-soft dorsal rays 2: orange-brown 0: reddish-orange 3: mixed 1: orange-brown 2: mixed 68. p-color f-posterior body 3: red 0; reddish-orange 1: brown 77. d-base m-dorsal pattern 2: orange-brown 0: uniform 3: mixed 1: spots

69. sp-pattem m-post. sp-dorsa 78. d-base f-dorsal pattern 0: uniform 0: uniform I; banded 1: spots 2: stripe 79. aa-pattem m-anter. anal fin 70. sp-pattem f-post. sp-dorsal 0: uniform 0: uniform 1: internal and distal stripes 1; banded 2: distal stripe only 2: stripe 80. aa-pattem f-anter. anal fin 89. ca-pattem m-caudal fin 0: uniform 0: uniform 1: internal bands and distal strip 1; bands 2: distal stripe only 2: dark basal area

81. aa-color m-anterior anal raysra 90. ca-pattem f-caudal fin 0: reddish-orange 0: uniform 1: orange-brown 1: bands 2: olive-brown 2: dark basal area

82. aa-color f-anterior anal rays 91. ca-color m-caudal fin 0: reddish-orange 0: reddish-orange I: orange-brown 1: orange-brown 2: olive-brown 2; mixed 3: brown-orange 83. pa-pattem m-posterior anal 0: uniform 92. ca-color f-caudal fin 1: internal light stripes 0: reddish-orange 2: dark distal stripe 1: orange-brown 2: mixed 84. pa-pattem f-posterior anal 3: brown-orange 0: uniform 1: intemal light stripes 93. pf-pattem m-pectoral fin 2; dark distal stripe 0: uniform 1: scattered or basal 85. pa-color m-posterior anal 2; dense or shading 0: reddish-orange 1: orange-brown 94. pf-pattem f-pectoral fin 2: mixed 0: uniform 1: scattered or basal 86. pa-color f-posterior anal rays 2; dense or shading 0: reddish-orange 1: orange-brown 95. pb-pattem m-pectoral base 2; mixed 0: uniform 1; spot 87. a-base m-anal fin pattem 2: mottled 0: uniform 3; basal band 1: spots 96. pb-pattem f-pectoral base 88. a-base f-anal fin pattern 0: uniform 0: uniform 1: spot 1: spots 2; mottled 3: basal band 97. pb-color m-pectoral fin base 0: uniform 1: reddish-orange 2: orange-brown 3; outline

98. pb-color f-pectoral fin base 0: uniform 1: reddish-orange 2: orange-brown 3: outline

99. pl-pattem m-pelvic fin 0: uniform 1; scattered or basal 2; dense or shading

100. pl-pattem f-pelvic fin 0: uniform 1: scattered or basal 2: dense or shading

101. g-pattem m-genital area 0: uniform 1: white 2: dark tipped

102. g-pattem f-genital area 0: uniform 1: white 2: dark tipped APPENDIX D

COLOR AND PATTERN STATES

Acanlhembleiiuiria crocktri A. A. A. ipinosa inaria bal- macn Puerto Pucrio UU lsi> Isia Cabo anomm Rcrugio t^bos Coronado San San San Pedro Ignacio loicas Nolasco de Farralon d-signal m-pattern 1 1 1 1 1 1 1 1 1 1 d-signal f-paUern 1 1 1 1 1 1 1 1 1 1 sig-area m-dorsal Tin 8 9 4 8 7 7 2 7 8 5 sig-area f-dorsal fin 7 6 8 7 6 6 1 ? 7 5 d-paitern m-anlerior dorsal fin 1 1 1 1 0 0 2 2 3 2 Q-paitem f-anterior dorsal f 1 1 1 1 0 0 2 2 3 2 d-melan m-anterior dorsal 1 1 1 1 1 1 1 1 1 1 d-melan f-anterior dorsal I 1 1 I 1 1 1 1 I 1 dm-loc m-anlerior dorsal fin 1 1 1 1 1 1 2 2 0 1 dm-loc f-anierior dorsal fin 1 1 1 1 1 1 2 2 0 I d-carot m-an(erior dorsal 1 1 1 1 1 1 1 i 0 I d-carot f-anterior dorsal 1 1 1 1 1 ! 1 \ 0 1 dc-loc m-anterior dorsal fin 0 0 0 0 0 0 0 0 3 0 dc-loc f-anierior dosal fin 0 0 0 0 0 0 0 0 3 0 d-clear m-anierior dorsal 1 1 I 1 1 1 7 7 0 1 d-clear f-anterior dorsal 1 1 1 1 1 1 ? 7 0 I dc-loc m-anterior dorsal 2 2 2 2 2 2 7 7 3 \ dc-loc f-anterior dorsal fin 2 2 2 2 2 2 7 7 3 I d-spot m-anlerior dorsal 0 0 0 0 0 0 0 0 0 O&l d-spot f-anierior dorsal 0 0 0 0 0 0 0 0 0 O&l d-irid m-anterior dorsal fin 1 1 1 1 0 0 ? ? 1 I d-irid f-anterior dorsal fin 1 1 1 1 0 0 7 7 1 1 di-num m-anlerior dorsal fin 3 2 2 2 0 0 7 7 7 7 di-num f-anterior dorsal fin 3 1 2 2 0 0 7 7 7 7 di-area m-anterior dorsal 6 4 5 4 0 0 7 7 7 7 di-area f-anterior dorsal 5 2 3 1 0 0 7 7 7 7 br-patiern m-branchiosiegals 0 0 0 0 0 0 1 2 0 0 br-patlern f-branchiostegals 0 0 0 0 0 0 1 2 0 0 br-color m-niembranes 2 2 2 2 2 2 2 0 0 I) APPENDIX D - Continued

Aconlhemblemaria crockeri <4. A. A. spinosa maria bol- macro Pueno Pucclo Isia Isia Isia Cabo anorum Rctugio Lobos Coronado San San San Pedro Ignacio Ljjcas Nolasco dc Farralon br-color f-membranes 1 1 I 1 1 1 1 0 0 0 jaw mOower 1 1 1 1 1 1 1 1 0 I jaw Mower 1 1 1 1 i 1 1 1 0 1 body m-general pattern 0 0 0 0 0 1 0 1 1 1 body f-general pattern 1 1 I 1 1 1 1 1 1 1 md-pattern m-anterior body I 1 I 1 1 3 0 4 2 2 md-pauern f-anteridr body 3 3 3 3 4 3 5 4 2 2 md-coloT m-anterior body 2 1 2 2 2 3 1 1 6 0&6 md-color f-anterior body 4&6 1&2&4&6 2&4 2&4 2&3 3 1 1 6 0&6 l-pattern m-anterior body 0 0 0 0 0 1 0 4 2 2 1-pattern f-anterior body 2 2 2 2 1 2 5 4 2 2 l-color m-anterior body 2 1 2 2 2 2 1 1 2 0&2 l-color f-anterior body 2 I&2 2 2 2 2 1 1 2 0&2 l-irid m-anterior body 1 I 1 1 1 1 7 7 1 1 l-irid f-anterior body 1 0 O&l 0 0 O&l ? 7 1 1 face m-pattern 1 1 1 1 1 1 1 1 1 1 face f-pattern 1 1 1 1 1 1 1 1 1 1 f-mel m-face coloration 2 2 2 2 2 2 3 3 3 3 f-mel f-face coloration 2 2 2 2 2 2 3 3 3 3 f-carot m-face coloration 2 2 2 2 2 2 0 0 2 9 f-carot f-face coloration 2 2 2 2 2 2 0 0 2 7 f-irid m-face coloration 2 2 2 2 2 2 7 7 1 2 f-irid f-face coloration 2 2 2 2 2 2 7 7 1 2 cheek m-pattern 2 2 2 2 2 2 1 1 2 1 cheek f-pattern 2 2 2 2 2 2 1 1 2 1 ch-loc m-cheek spot 1 1 1 1 1 1 0 0 0 0 ch-loc f-cheek spot 1 1 1 1 1 1 0 0 0 0 op-pattern m-operculum 1 1 1 1 1 1 2 1 0 1 op-pattern f-operculum 1 1 1 1 1 1 2 1 0 1 APPENDIX D - Continued

Araiiihembleimrin crockeri A. A. spinosa mnria bat- macrospUus Pucito Putito IsU ls\a hta Cabo anarum Refugio Lobos Coronado San San San Pedro Ignacio Lucas Nohsco dc Farralon op-color m-operculum 2 2 I&2 1&2 1 1 0 1 0 1 op-color f-operculum 2 2 2 I&2 1 I&3 0 1 0 1 c-supTaoTbital m-cirri 1 1 1 1 1 1 0 0 0 0 c-supraorbital f-cirri 1 1 1 1 1 1 0 0 0 0 c-nasal m-cirri 1 1 1 1 1 1 0 0 0 0 c-nasal f-cirri 1 1 1 I 1 1 0 0 0 0 p-paitern m-pos(erior body 0 0 0 0 0 1 0 1 1 1 p-pallern f-posterior body 1 1 1 1 0 1 1 1 I I p-color m-poslerior body 2 1 2 2 2 3 1 1 2 2 p-color f-posterior body 2 1&2 2 2 2 3 1 I 2 2 sp-patiern m-post. sp-dorsa 2 1 1 1 1 1 2 2 0 1&2 sp-pa((ern f-post. sp-dorsal 2 1 1 I 1 1 2 2 0 I&2 sp-color m-posi. sp-dorsal 2 1 1 1 I I 0 0 I 1 sp-color f-post. sp-dorsal 2 1 1 I I I 0 0 1 1 so-pattern m-soft dorsal 1 1 1 1 1 1 0 0 0 ? so-paiien f-soft dorsal I 1 1 1 1 I 0 0 0 7 so-color m-soft dorsal rays 1 2 2 1 3 2 0 0 I 7 so-color f-soft dorsal rays 2 2 2 I 3 2 0 0 I ? d-base m-dorsal pattern 1 1 1 1 1 1 1 1 1 1 d-base f-dorsal pallern 1 1 1 1 1 1 1 I I I aa-pattern m-anter. anal fin 1 I 1 1 1 1 0 1 0 1 aa-pattern f-anier. anal Tin 1 1 1 1 1 1 0 1 0 I aa-color m-anterior anal raysra 2 1 1 1 I i 1 ? 1 7 aa-color f-anierior anal rays 2 1 1 1 1 1 1 ? 1 ? pa-pattern m-posterior anal 1 O&l 0 0&1&2&3 O&I 1 7 7 0 1 pa-pattern f-posterior anal 1 0 0 O&l O&l 2 ? ? 0 1 pa-color m-posterior anal 2&3 1 1 1 1 1 ? 7 1 7 pa-color f-posterior anal rays 2&3 2 2 2 2 2 1 ? 1 7 a-base m-anal fin pattern 1 1 1 1 1 1 1 1 7 1 APPENDIX D - Continued

Acaniheinblrmaria crockeii it. A. A. .1 spinosa iiutna bal- mi Puerto Pucno Isia Isia ls)a Cabu anorum Rcfujio Lobos Coronado San San San Pedro ignacio Lucas Nolasco de Faiiaton a-base f-anal fin pattern 1 1 I I I 1 1 1 7 1 ca-pattern m-caudal fm 1 1 1 1 1 1 7 0 0 2 ca-patletn f-caudal Tm 1 i 1 J 1 1 7 0 0 2 ca-color m-caudal fln 3 2 2 1 0 2 7 7 1/3 3 ca'color f-caudal fln 1 2 0 2 0 2 7 7 1/3 3 pf-pattern m-pectoral Tin 2 2 2 2 2 2 2 0 2 1 pr-pactern f-pec(oral fin I 1 1 1 1 1 1 0 2 1 pb-pattem m-pectoral base 0 0 0 0 0 O&l 2 3 0 0 pb-pattern f-pecioral base 0 O&l O&l O&l 0 1 2 3 0 0 pb-color m-pectoral Tin base 0 0 0 0 0 1 7 7 7 7 pb-color f-pectoral Tin base 0 0&3 0&2&3 0&2&3 0 1&3 7 7 7 7 pl-pai(ern m-pelvic fin 2 2 2 2 2 2 2 2 2 I pl-paiiem f-pelvic fin 1 1 1 1 1 1 1 2 2 I g-pattern m-geniial area 1 1 1 1 1 1 1 1 I&2 1 g-pal(ern f-genital area 1 1 1 1 1 1 1 1 1&2 I

Note: Data from the other Acanthemblemaria species were collected from museum specimens. 253

APPENDIX E

FEMALE AGGRESSION TOWARD MALES DURING MATING

In a conflict over mating, the male is not always the initiator, nor the lone aggressor. Female

behaviors that bias or coerce male mating decisions have been given little attention in the

literature (but see Hunter et al. 1993). This is probably due, in part, to the fact that female

coercion of male mating decisions is not generally manifested as physical aggression and thus is

more subtle to observe.

Compared to the number of accounts of male aggression against females, accounts of

female aggression against males are rare. Mutual aggression during mating is observed in some

species of carnivores in which well-armed predators must synchronize their activity for breeding

(Ewer 1973; lions, Schaller 1972; crabeater seals, Siniff et al. 1979). Cannibalism of males by

females during or after copulation is observed in some spiders, scorpions, copepods, mantids,

and other species (reviewed in Elgar &. Crespi 1992). In birds, aggression by resident females

toward their mates has been observed in both experimental and in natural situations and may

ftmction to prevent their mates from engaging in polygyny or extra-pair copulations (reviewed

in Slagsvold & LiQeld 1994). In the mantis shrimp, Pseudosquilla ciliata, females frequently

initiate courtship and engage in vigorous chases in which they grasp, sometimes strike at, and occasionally injure males as they attempt to mate with them (Hatziolos & Caldwell 1983). Males appear to exercise choice by preferentially courting and mating with nonaggressive females.

Males attempt to avoid aggressive females by withdrawing from courtship attempts and by moving rapidly away. The authors suggested a number of alternatives to explain aggressive female behavior: misdirected aggression, a demonstration of the female's ability to defend the brood, a need to replenish sperm supplies, or a form of "female harassment". Caldwell (pers. 254

comm.) suggests that the later appears most consistent with their observations although why

females would harass males remains a puzzle.

Sexual selection theory (Trivers 1972) predicts that in those species in which males invest

more in reproduction than do females, males are expected to be discriminating in mating and

females are expected to actively pursue copulations and, at least potentially, to coerce reluctant

males to mate by the use of force directed against them or their young (Emlen et al, 1989; Smuts

& Smuts 1993; Gowaty, this volume). Indeed, females are active in soliciting copulations from

males in some polyandrous species (reviewed in Hatziolos & Caldwell 1983). However, I found

no references to male injuries or deaths caused by females during mating in these species.

The hypothesis of sexually selected infanticide (Hrdy 1974, 1979; Sherman 1981) was tested

by Emlen et al. (1989) in the wattled jacana, a polyandrous shorebird. In this species, males

perform virtually all parental care duties and individual females defend areas that encompass 1

to 3 male territories (Emlen et al. 1989). Intense fights between resident and intruder females

occurred and frequendy led to territory (and male) takeovers by the challenger. When such a

takeover occurs, the males usually are caring for eggs or chicks from the former female. The

hypothesis of sexually selected infanticide predicts that the new female would behave in a way

that decreases the costs of rearing the offspring of other females. When the authors

experimentally removed two resident females, two replacement females quickly reoccupied the

territories. These replacement females killed or evicted three of four existing broods of chicks and sexually solicited four of five usurped males, results consistent with the hypothesis of sexually selected infanticide.

The dynamics and evolutionary consequences of female behaviors that bias or coerce male mating decisions deserve further attention. 255

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