AMER. ZOOL., 38:82-96 (1998)

Courtship and Mate Choice in Fishes: Integrating Behavioral and Sensory Ecology1

ROBERT CRAIG SARGENT2, VICTOR N. RUSH, BRIAN D. WISENDEN3, AND HONG Y. YAN T. H. Morgan School of Biological Sciences, Center for Ecology, Evolution and Behavior, University of Kentucky, Lexington, Kentucky 40506-0225

SYNOPSIS. Sexual selection theory predicts a coevolution between male sexual or- namentation and female preference. The implication of this prediction for sensory ecology is that there should be a tight coupling between the physiology of male signal production and the physiology of female signal reception. Indicator models of sexual selection predict that male ornamentation is correlated with male con- dition, and that female preference is correlated with male ornamentation. Indicator models of sexual selection have a conceptual overlap with resource acquisition and investment models of behavioral ecology. Empirical studies with fishes, particularly with guppies (Poecilia reticulata) and threespine sticklebacks (Gasterosteus aculea- tus), suggest a strong connection between acquired resources, male condition, male ornamentation, male courtship, and female preference.

INTRODUCTION selection, which can be defined as the dif- Whereas behavioral ecology focuses on ferential ability of different phenotypes to how major categories of behavior such as obtain mates and reproduce, due to two avoiding predators, feeding, mating, paren- forms of intraspecific interaction: 1. com- tal care, contribute to fitness (Krebs and petition within a sex for access to mates or Davies, 1987; Sargent, 1990), sensory ecol- to resources for mating (intrasexual selec- ogy focuses on the sensory adaptations to tion); and, 2. mate choice between the sexes accomplish these classes of behavior (Du- (intersexual selection). Morphology and be- senbery, 1992). If the behavior of interest havior conducive to fighting ability (e.g., involves intraspecific interaction and com- antlers in deer) are thought to have evolved munication, such as courtship and mate through intrasexual selection; whereas, choice, then integrating these two ap- morphology and behavior involved in proaches can reveal insights into how and courtship (e.g., the peacock's tail) are why signalers and receivers are coadapted. thought to have evolved through intersexual selection (see Andersson, 1994, for review). Since Darwin's (1871) landmark treatise, In most species, females are the limiting evolutionary biologists have been fascinat- sex; that is, female reproduction is limited ed by the phenomena of sexual dimorphism primarily by resources, whereas male repro- and sexual selection. Darwin was particu- duction is limited primarily by the number larly intrigued by his observation that the of females with whom they mate (Bateman, males of most species have elaborate or- 1948; Williams, 1975). Consequently, most naments that are ostentatiously displayed studies of sexual selection have focused on during intrasexual competition and court- males. ship; thus, he proposed his theory of sexual Darwin (1871) himself recognized that these ornaments must have survival costs ' From the Symposium Animal Behavior: Integra- for their bearers; thus, he hypothesized that tion of Ultimate and Proximate Causation presented at the Annual Meeting of the Society for Integrative and the survival costs of male ornamentation Comparative Biology, 26-30 December 1996, at Al- are offset by benefits in obtaining mates. buquerque, New Mexico. An implication of Darwin's theory of sex- 2 To whom correspondence should be addressed; E- ual selection is that male ornaments act as mail: [email protected] signals to rival males, females, or both. ' Current address: Department of Biological Sci- ences, University of Alberta, Edmonton, Alberta, Can- There has been relatively little analytical ada T6G-2E9. modeling of intrasexual selection; however,

82 COURTSHIP AND MATE CHOICE IN FISHES 83 genetic models of intersexual selection il- an estimate of energy reserves by scaling lustrate that through assortative mating, weight to length (see Bolger and Connolly male ornaments and female preferences [1989] for review). This is the definition of may coevolve (e.g., Fisher, 1915, 1930; "condition" that we will adopt here; how- O'Donald, 1980; Lande, 1980, 1981; Kirk- ever, other state variables are clearly im- patrick, 1982). This coevolutionary process, portant determinants of fitness as well. between signaler and receiver, has profound There is considerable empirical support implications for sensory ecology. Not only for the importance of energy reserves for would one predict a correlation between reproductive success in fishes (see Sargent male ornament and female preference, but [1997] for review). First, it is well known also a coupling of the underlying physiol- that energy reserves decline during the ogies of male signal production and female breeding season, and that fishes that have signal reception. not reproduced have higher energy reserves We are intrigued by a particular class of at the end of the breeding season that fishes sexual selection models, which are collec- that have reproduced (e.g., Unger, 1983; tively referred to as indicator models (see Sargent, 1985; Reznick and Braun, 1987; Andersson, 1994, for review). In these Chellapa et al, 1989; FitzGerald et al, models, male ornaments evolve to "indi- 1989; Sabat, 1994). Second, many studies cate" or "honestly signal" some aspect of manipulate diet or ration, and these studies male phenotypic quality, genetic quality, or show that individuals that receive more both, and female preference evolves to be supplemental food have higher reproductive correlated with the degree of male orna- success, survival between brood cycles, or mentation (e.g., Zahavi, 1975, 1977; Ham- both (e.g., Townshend and Wootton, 1984; ilton and Zuk, 1982; Hasson, 1989, 1997; Ridgway and Shuter, 1994). Third, Sargent Grafen, 1990a, b; Folstad and Karter, 1992; (unpublished) found with fathead minnows Price et al, 1993; Wolf et al, 1997). These (Pimephales promelas) that "condition in- models provide a conceptual basis for un- dex" (i.e., weight scaled to length) at the derstanding what is being signaled by beginning of the breeding season is posi- males. In addition, these models provide a tively correlated with the amount of stored conceptual link to the dynamics of resource neutral lipids, and with the number of off- acquisition, and subsequent investment of spring produced during the breeding sea- acquired resources into components of fit- son. Thus, acquired resources are clearly ness (e.g., Houston and McNamara, 1988; tied to reproductive output in fishes. Mangel and Clark, 1988). Behavioral strategies are said to be "con- Animals acquire resources throughout dition-dependent" if an individual's best their lives. Although these resources are in- strategy depends on its condition, or on its corporated into the phenotype in a variety condition relative to that of other members of different ways, they ultimately contribute of the population. For example, during to an animal's fitness, or lifetime reproduc- male-male competition for females in fish- tive success (e.g., Houston and McNamara, es, larger males court females, whereas 1988; Mangel and Clark, 1988; Williams, smaller males attempt to mate forcibly or 1992; Sargent, 1990; Sargent et al, 1995). sneakily (see Gross, 1984, 1996 and Farr Behavioral ecologists use the term "condi- 1989, for reviews). Females may benefit by tion" to refer to an animal's overall quality mating with high condition males directly in terms of acquired resources, with the im- (i.e., phenotypic benefits such as more re- plicit assumption that higher condition sources for offspring, lower levels of patho- leads to higher fitness. Within the paradigm gens that could infect the female or off- of dynamic optimization, "condition" can spring), or indirectly (i.e., genetic benefits be thought of as all axes in the state space inherited by the offspring, e.g., Moore, that are relevant to fitness (e.g., body size, 1994). If females do benefit by mating with energy reserves, immunocompetence). high condition males, then sexual selection However, fisheries biologists have tradition- theory predicts that males will "honestly ally used the term, "condition," to refer to signal" their overall quality to prospective 84 R. C. SARGENT ETAL. females, and that females will base their 1993; sticklebacks, Bakker and Milinski, mate choice on these male signals (Zahavi, 1991); and positively correlated with fe- 1975, 1977; Kodric-Brown and Brown, male preference (guppies, Houde, 1987; 1984; Grafen, 1990a, b; Price etal., 1993). Endler and Houde, 1995; sticklebacks, Bak- Honest signaling theory assumes that sig- ker, 1993). Finally, if males of both species nals are costly to produce, and that a given are experimentally infected with parasites, level of signal is more costly for low-con- parasitized males have reduced breeding dition than high-condition males. Many of coloration and are less preferred by females the predictions of honest signaling have than non-parasitized controls (guppies, been supported in fishes (see below). Thus, Houde and Torio, 1994; sticklebacks, Mil- sexual selection theory potentially has inski and Bakker, 1990). A clear pattern has broad implications for sensory ecology and emerged; male breeding coloration, energy intraspecific communication. reserves, courtship display rate, parasite load, and attractiveness to females are all Two MODEL SYSTEMS: THE GUPPY AND interrelated. THE THREESPINE STICKLEBACK Considerable information is also known Although there are many excellent stud- about the spectral sensitivities and the vi- ies of sexual selection on a wide spectrum sual ecologies of each species. For example, of fish species, two species stand out as be- based on microspectrophotometry of visual ing especially appropriate for this review: pigments, both species have four sets of ret- 1. the guppy, Poecilia reticulata, which has inal cone cells (guppies, Archer, 1988; internal fertilization and females that give Rush, 1995; sticklebacks, Baube, 1998; birth to fully independent juveniles (see Baube, personal communication), which in- Meffe and Snelson [1989] for review); 2. cludes a set of ultraviolet cones, and three the threespine stickleback, Gasterosteus sets of cones in the "human-visible" wave- aculeatus, which has external fertilization lengths. In sticklebacks, both spectral sen- and male parental care of the developing sitivity and male breeding coloration have eggs and newly hatched fry (see Wootton been shown to correlate with the photic en- [1976] for review). Although these two spe- vironment. cies have very different mating systems and In "tea-stained" lakes in British Colum- reproductive biology, they share much in bia, Canada, the short wavelengths attenu- common in terms of sexual selection and ate rapidly, which creates a "reddish" pho- signaling between the sexes. We caution tic environment; whereas, in mesotrophic that these species exhibit enormous geo- lakes there is a broader spectrum of wave- graphical variation (guppies, Endler, 1977, lengths of light (McDonald and Hawry- 1978; sticklebacks, Bell and Foster, 1994), shyn, 1995; McDonald et al., 1995). There so the results that we cite here are not true is a tendency for male breeding coloration for all populations within a species; we dis- to be black (rather than red) in these tea- cuss some of these "exceptions" below. stained lakes (Reimchen et al., 1985). Us- In both species, males develop a carot- ing optic nerve recording, McDonald and enoid-based, orange to red breeding color- Hawryshyn (1995) found that sticklebacks ation (guppies, Houde, 1987; sticklebacks, in tea-stained lakes have their peak spectral Wootton, 1976), and this breeding colora- sensitivity shifted to longer wavelengths tion is positively correlated with carote- relative to fish in mesotrophic lakes. noids in the diet (guppies, Kodric-Brown, McDonald et al. (1995) hypothesized that 1989; sticklebacks, Bakker, personal com- black breeding coloration may be favored munication, see also Frischnecht, 1993); in tea-stained lakes, due to its higher con- positively correlated with condition index trast against a red background than would (weight scaled to length: guppies, Nicoletto, be the case for red breeding coloration. 1991, 1993; sticklebacks, Milinski and They tested this hypothesis with females Bakker, 1990; Frischknecht, 1993; Bakker from a mesotrophic lake, where males have and Mundwiler, 1994); positively correlated the more typical red breeding coloration. with courtship intensity (guppies, Nicoletto, They examined female preference for red or COURTSHIP AND MATE CHOICE IN FISHES 85 black male video images against a red or contrast of the male ornament), female pref- blue background, which roughly approxi- erence for male coloration disappears (gup- mated the two photic environments. They pies, Long and Houde, 1989; sticklebacks, found that females preferred red males Milinski and Bakker, 1990). It would be in- against a blue background, but black males teresting to conduct artificial selection ex- against a red background, which supports periments where photic environment is ma- their hypothesis (McDonald et al, 1995). nipulated, and to look for evolutionary re- Thus it appears that photic environment can sponses in spectral sensitivity, female pref- affect spectral sensitivity and female pref- erence and male coloration. erence of male breeding coloration. It A common feature of all the above cited would now be interesting to examine con- studies on condition dependence and honest dition dependence and honest signaling in signaling in guppies and sticklebacks is that non-red or black males from these tea- they are all based on visual cues. It would stained lakes. be interesting to see if other sensory mo- In guppies, it appears that geographic dalities play a role in honest signaling in variation in male coloration depends more these species. on predation regime than on photic envi- ronment (Endler, 1977, 1978). Basically, OTHER SENSORY MODALITIES orange breeding coloration is negatively It is well known that fishes send and re- correlated among populations with the in- ceive acoustical, low frequency mechano- tensity of predation on guppies. Female sensory, chemical, and electrical signals, in preference for male orange coloration is addition to visual signals (see Atema et al., stronger in populations with lower preda- 1988, for review). Moreover, cues other tion intensities (Endler and Houde, 1995). than visual cues are known to play a role In addition, Endler and Houde (1995) also in courtship and agonistic encounters in found that male orange coloration correlates many species. However, it is not known with the photic environment; orange col- whether these other sensory cues act as oration increases with the water orange ra- condition indicators. Because the active tio {i.e., the relative transmission of long production of electrical signals is relatively wavelengths through the water, which is restricted taxonomically in fishes, we calculated as the integral of 400-550 nm choose not focus on this sensory modality; absorbance divided by the integral of 550- however, there are many excellent examples 700 nm absorbance; see Endler and Houde and reviews of courtship and mate choice 1995) among populations. Interestingly, using electrical cues {e.g., Hagedorn and this appears to be the opposite trend found Heiligenberg, 1985; Heiligenberg, 1993; in sticklebacks. In sticklebacks, redder pho- Moller, 1995; Tricas et al, 1995). Instead, tic environments are correlated with black we briefly review literature on acoustical breeding coloration, and female preference cues, low frequency mechanosensory cues, for black males over red males (McDonald and chemical cues, and discuss their poten- and Hawryshyn, 1995; McDonald et al, tial relevance to the phenomena of condi- 1995; Reimchen et al, 1985). In guppies, a tion dependence and honest signaling. redder photic environment is correlated with stronger preference for orange colored Acoustical cues males (Endler and Houde, 1995). A possi- Most research on fish acoustical com- ble resolution to this disparity is that tea- munication focuses on the mechanisms of stained stickleback habitat attenuates the sound production and detection (see Tav- short wavelengths more completely than olga et al, 1981; Hawkins, 1993, for re- comparable guppy habitat (guppy habitat, views). Acoustical communication is taxo- Endler, 1991; stickleback habitat, Mc- nomically widespread in fishes. Here we fo- Donald et al, 1995). In both guppies and cus on a small set of species for which there sticklebacks, when the color of the ambient are data on acoustical cues and courtship. light is manipulated to coincide with male breeding coloration (thus reducing color Vocalization in fishes requires modifica- tion of the swimbladder, pectoral fins or 86 R. C. SARGENT ET AL pharyngeal teeth (Tavolga, 1971; Sand and ic muscle is induced by steroid hormones Hawkins, 1973; Schwartz, 1974; Kratoch- (Brantley et al, 1993&; Connaughton and vil, 1977; Crawford, 1986; Ladich, 1989; Taylor, 1995). One might expect sound pro- Hawkins, 1993; Connaughton and Taylor, duction to be constrained by body size, be- 1996; Ladich, 1998). Low frequency cause, in general, larger fish will have larg- sounds are produced by drumming muscles er swimbladders with lower resonant fre- attached to the swimbladder (Tavolga, quencies (Fine et al, 1977). Thus one 1971; Brantley and Bass, 1994; Connaugh- might expect the fundamental frequency of ton and Taylor, 1996). High frequency a fish vocalization to be negatively corre- sounds are produced by bony attachments lated with body size. Interestingly, this ap- to the pectoral fin, or scraping of the pha- pears not to be the case for drumming. With ryngeal teeth (Schwartz, 1974; Kratochvil, drumming, the fundamental frequency de- 1977; Torricelli et al, 1990; Fine et al, pends on sonic muscle contraction rate 1996). The specialization of the sound pro- (Fine et al., 1977), which in turn is con- duction organs are usually confined to trolled by a central nervous system vocal males and may vary intrasexually based on circuit (Bass and Baker, 1990, 1991). In the size, and possibly age. In water, low fre- midshipman {Porichthys notatus), there two quency sounds travel farther and are more types of sexually mature males: large, ter- easily localized than high frequency sounds ritorial, egg-guarding males {i.e., Type-I (Dusenbery, 1992). This suggests that low males), and smaller males that "sneak" fer- frequency sounds should be used to court tilizations (i.e., Type-Il males, Brantley and at a distance, whereas high frequency Bass, 1994). The larger Type-I males have sounds should be used during interactions much larger sonic muscles, have much larg- that involve close contact between individ- er motoneurons and pacemaker neurons in uals. However, such bimodal sound produc- their vocal sonic circuits, and produce high- tion has never been reported. One possibil- er fundamental frequencies than do the ity is that it is costly to possess dual struc- smaller Type-II males (Bass and Marcha- tures (drumming muscles and stridulation terre, 1989; Bass and Baker, 1990). Al- of pectoral fin or pharyngeal teeth) for though it appears that fundamental frequen- sound production. Another possibility is cy is independent of body size for Type-I that if fish were to produce an intense sound males (Bass and Baker, 1990, Figure 2), it type at a long distance and another less in- would now be interesting to see if funda- tense sound type when the receiver is near- mental frequency, or the duration of the call by (Kenyon, 1994), then the signal sender (e.g., Fine, 1978), is correlated with con- can attract mates at both long and short dis- dition (weight scaled to length) or some tance without investing in dual structures other index of energy reserve. for two specific types of sound production. Finally, the energy required to produce a Unlike drumming muscles, pharyngeal low frequency sound of equal intensity is teeth and pectoral fin structures may not greater than that for a high frequency sound have the same relationship between body (Dusenbery, 1992). This suggests that the size and signal capabilities. However, it is cost of sonic communication among fishes likely that larger pectoral fins or larger pha- may vary depending on the type of sound ryngeal teeth will produce higher amplitude producing organ. sounds as well. It is possible that high fre- quency communication might be an exam- Let us first consider drumming. Sonic ple of sensory drive or sensory bias while muscle size is tightly associated with body lower frequency communication is an ex- size in larger males; immature males show ample of condition-dependent mate-choice. very little enlargement of sonic muscles, More work needs to be done on the rela- whereas adult males is season show radi- tionship between body size and frequency cally enlarged muscle tissue (Templeman of stimuli. Kratochvil (1977) and Ladich and Hodder, 1958; Bass and Marchaterre, and Yan (1998) report that high frequency 1989; Brantley et al, 1993a; Connaughton sound production in croaking gouramis is and Taylor, 1995). The enlargement of son- correlated with body size, with smaller fish COURTSHIP AND MATE CHOICE IN FISHES 87 producing higher frequency sounds than along the substrate with little attenuation. larger fish. Furthermore croaking gouramis This channel would stimulate the upper have relatively larger sonic muscle mass for reaches of the lateral line and the lower their body size (Kratochvil, 1977). range of the auditory system. Sound reception in most teleosts is most In general the physiological, neurobio- efficient in the low frequencies, which cor- logical, and morphological aspects of fish relates with the sound producing organ of vocalization have outstripped research on the fishes (Popper and Fay, 1973). However the functional bases of communication, be- several fishes have modifications of the yond a small set of specific examples (e.g., acoustical system that increases sensitivity Myrberg, 1981; Crawford, 1986; Brantley to high frequencies. In fish with swimblad- and Bass, 1994; Whang and Janssen, 1994; ders, air filled tubes or bones directly at- Ladich, 1998) that have been studied in de- tached to the bladder increase the sensitivity tail. The functional relationship between of the ear to high frequency sounds (>1 sound production as a signal and the re- khz) (Schuster, 1989; Hawkins, 1993). Sim- sponse of the receiver is unclear. Future re- ilar air filled passages around the gill are search should focus on signal transmission used in anabantoid fish to increase their through the environment, which is compli- sensitivity to high frequency sounds. Re- cated by thermoclines and the body tem- moval of air filled bubbles produces a dra- peratures of the fish (both for sound pro- matic decline in the sensitivity of these fish duction and hearing). Similarly, we need (Yan, unpublished). Researchers have more field and laboratory studies of how shown a general correlation between sound fish use sound. Research in the future production organs and acoustical sensitivity should examine the relationship between in fishes for low frequency sounds. Ladich age, body size, and sonic muscle mass. Be- and Yan (1998) have shown a similar re- cause signal production requires a large ex- lationship for fish that produce high fre- penditure of energy to maintain and pro- quency signals. It would be interesting to duce, they have the prerequisites to be hon- see if the correlation between high frequen- est signals of condition. Correlations be- cy sound production and sound reception is tween condition, sound production, and also correlated with condition. mate choice should be easy to acquire. It is The function of sound production has re- clear that in the last few years the gap be- ceived less attention than has its physiol- tween functional and proximate mecha- ogy. Work on sound production and sound nisms of acoustical communication has nar- interception in the bicolor damselfish (Ste- rowed; now there is an opportunity to nar- gastes partitas) indicates that vocalization row the gap further. in this fish is functionally similar to bird song. Males exhibit responses to "intruder Low frequency mechanosensory cues vocalizations" and "stranger vocaliza- A common feature in both courtship and tions" (Myrberg, 1981; Myrberg et al, agonistic encounters in fishes is lateral dis- 1986; Myrberg et al, 1993). Females are play and quivering (Bleckmann, 1993; Nel- attracted to both the visual display and the issen, 1991). A signaling fish aligns itself acoustical signature of a male (Myrberg, beside a recipient, often within a few cen- 1981; Myrberg et al, 1986). Sound pro- timeters, and vibrates its body with fins duction in midshipman (Porichthys notatus) erect. Although it would appear that this be- is thought to have a similar function; the havior generates a low frequency mechano- vocalizations of large calling males is at- sensory stimulus that the recipient of the tractive to females (Brantley and Bass, display could detect with its lateral line sys- 1994). Substrate drumming is exhibited by tem, there have been surprisingly few tests the mottled sculpin (Cottus bairdi), which of this hypothesis (see Bleckmann, 1993). knocks its head against the substrate (Bar- Satou et al. (1994a, b) have examined ber and Mowbray, 1956; Whang and Jans- mechanosensory stimuli generated by fe- sen, 1994). This low frequency signal, from male hime salmon (Oncorhynchus nerka) a fish with no swimbladder travels rapidly during spawning. They examined male re- 88 R. C. SARGENT ETAL.

sponses to vibrational and visual compo- pheromones in goldfish, Carassius auratus, nents of female courtship and spawning be- has been an active area of research. Most havior using dummy females. If both com- research has focused on male detection of ponents were present, males spawned; how- females, rather than vice versa. ever, if the dummies did not vibrate, then Dulka et al. (1987) demonstrated that en- males did not spawn (Satou et al, 1994a). dogenous steroid hormones act also as sex If males' lateral lines were blocked with co- pheromones that increase physiological and balt, which is known into interfere with the behavioral competence and synchrony of function of lateral line hair cells, then males gamete release in goldfish. Sorensen (1992) failed to spawn to vibrating dummies (Sa- and Sorensen and Scott (1994) envision tou et al, 1994ft). These experiments indi- three stages in the evolution of chemical cate the importance of the lateral line in sex signals, which require only minor re- perceiving vibrational cues. Now it would organization of pre-existing compounds and be interesting to examine male mechano- receptors. First, reproductive hormones are sensory cues as potentially honest signals released into the surrounding water as a to females. mechanism for clearing them from the We have undertaken such a study with blood. At first, these water-borne hormones the green swordtail (Xiphophorus helleri). do not function as pheromones. Second, the Our data are very preliminary; however, us- expression of pre-existing receptors from ing posterior lateral line trunk nerve record- the endocrine system on external chemo- ing we found that the lateral line system of sensory cells give the fish the ability to de- the female swordtail was most sensitive to tect water-borne hormones. Thus, fish could frequencies between 20—50 Hz, and a high 'spy' on the physiological state of conspe- speed video analysis of male courtship sug- cifics and respond accordingly. Third, true gests they generate a particle acceleration pheromonal 'communication' is achieved well within the peak of female sensitivity when controlled and reciprocal exchange of (Rush et al, unpublished data). We suggest chemical signals occurs. Sorensen and Scott that some component of the male lateral (1994) did not find a strong correlation be- display {e.g., amplitude, frequency) in the tween steroid production by female goldfish green swordtail may be an indicator of con- and their detection by males, which led dition, and we intend to pursue this further. them to conclude that hormonal sex pher- It is noteworthy that male display rate omones are an example of chemical spying (evaluated visually by human observers) is rather than a co-evolved system of recip- correlated with condition and female pref- rocal signal production and detection. Nev- erence in guppies (Poecilia reticulata, Ken- ertheless, water-borne pheromones could nedy et al., 1987; Nicoletto, 1993), three- serve as condition indicators. spine sticklebacks (Gasterosteus aculeatus, Gross and Franck, 1979; Ridley, 1986; but The female preovulatory hormone, 17a, see Rowland, 1995), and bicolor damselfish 20|3-dihydroxy-4-pregnen-3-one (17a, 20(3- {Stegastes partitas, Knapp and Kovach, P) has received the most attention. Expo- 1991). Undoubtedly, much of the signaling sure to 17a, 20f$-P induces males to in- during male courtship display in these spe- crease plasma levels of 17a, 2O|3-P and go- cies is visual; however, it would now be nadotropin, and to increase milt volume in interesting to see if visual and mechanosen- salmonids (Olsen and Liley, 1993; Dittman sory stimuli in combination produce a larg- and Quinn, 1994; Scott et al., 1994) and er female response than either stimulus cyprinids (Dulka et al., 1987; Yamazaki, alone. 1990; DeFraipont and Sorensen, 1993; Sta- cey et al, 1994; Sorensen et al, 1995; Bjer- Chemical cues selius et al, 1995a, b). The medial olfac- Chemical cues have been long suspected tory tract of the male seems to be the lo- to have an important function in the repro- cation of the pheromone receptors, without ductive behavior of fishes (Noble, 1939) which the full complement of spawning be- and in the past decade the study of sex havior does not proceed (Yu and Peter, COURTSHIP AND MATE CHOICE IN FISHES 89

1990; Dulka and Stacey, 1991; Resink et aggression against gravid females (Segaar al, 1989). et al., 1983). Cardwell et al. (1995) report that field- In several species of gouramis female caught male minnows Puntius schwanen- pheromones attract males, initiate nest con- feldi, bearing tubercles (a transient second- struction by males, and stimulate the de- ary sex character under androgen control velopment of male breeding coloration (Lil- developed by males during the breeding ey, 1982). A pheromone produced by males season) showed greater sensitivity to a fe- inhibits nest building behavior by subordi- male sex pheromone than males without tu- nate males and also attracts females (Liley, bercles. Further investigation with P. gon- 1982). Pheromones released by male Tri- ionotus revealed an important activational chogaster trichopterus induce female ovar- effect of androgen on olfactory receptors, ian maturation and increased plasma levels leading to greater intensity of courtship be- of steroid hormones, including 17a, 20p-P havior (Cardwell et al., 1995). (Degani and Schreibman, 1993). Females in a number of poeciliid species In summary, most chemical signaling release a sex pheromone (see Liley [1982] during fish reproduction appears to origi- for review). Female guppies Poecilia reti- nate from females; although, there is some culata, have a sex pheromone, probably evidence of male signaling as well. Al- hexestrol dipropionate, produced by the though chemical cues seem to indicate re- ovary shortly after parturition (Amouriq, productive state or receptivity, their poten- 1967 in Liley, 1982; Gandolfi, 1969; Crow tial role as condition indicators is unknown. and Liley, 1979). Sex pheromones of fe- It would be interesting to tease apart the male poeciliids generally stimulate male ac- separate effects of chemical cues from those tivity, attract males and increase male court- of other sensory cues as determinants of the ship. Sumner et al. (1994) found that chem- outcome of courtship and mate choice. ical cues from female sailfin mollies, when in combination with visual cues, resulted in SUMMARY AND DIRECTIONS FOR FUTURE large males (but not small males) prefer- RESEARCH entially courting females that had recently Behavioral ecology theory, particularly giving birth {i.e., fertile), over females that sexual selection theory and resource acqui- are gravid with embryos {i.e., not fertile). sition theory, makes specific predictions on Given that large males typically court fe- communication between the sexes during males whereas small males "sneak," fe- courtship and mate choice. If signals are males may use chemical cues to reduce sex- costly to produce, then theory predicts that ual harassment; large males attracted by the signalers should produce signals in direct sex pheromone repel subordinate males. proportion to their condition. Receivers Information on male pheromones is should be well adapted to discriminate the much more limited. In swordtails {Xipho- level of signal being produced, and thus the phorus), females appear to be able to use signaler's condition. Sensory ecology pro- male chemical cues in species recognition vides a wealth of information on physiolog- (Crapon de Crapona and Ryan, 1990). ical mechanisms underlying signal produc- Chemical stimuli from male fathead min- tion and signal detection; thus, a great deal nows in breeding condition attract females remains to be learned by integrating behav- to a greater degree than stimuli from re- ioral and sensory ecology. gressed males or females (Cole and Smith, It appears that male visual cues do hon- 1992). Male threespine sticklebacks {Gas- estly signal condition to females in many terosteus aculeatus) release a sex phero- cases; however, this issue has not been ad- mone during courtship displays that attracts dressed explicitly for other sensory modal- gravid females and repels non-territorial ities. It seems plausible that acoustical and males (Waas and Colgan, 1992). Also in mechanosensory cues may also be condi- sticklebacks, the olfactory nerve appears to tion dependent. However, chemical cues play an important role in nest building be- primarily seem to signal a fish's sex and havior, onset of courtship, and suppressed reproductive state. It may well be that dif- 90 R. C. SARGENT ETAL. ferent sensory modalities signal different 2. Search for condition indicating traits aspects of overall condition. It is clear, We suggest that empiricists determine however, that integration of behavioral and whether or not any of the traits that they sensory ecology, with regard to the ques- study (e.g., morphology, signal production, tion of sexual selection and resource acqui- signal detection) are correlated with condi- sition, is still in its infancy. Below we make tion (e.g., weight scaled to length). Condi- some specific suggestions for directions for tion can be estimated as Weight/Lengthb future research. where b represents the allometric coeffi- 1. Other measures of condition cient between weight and length, which can be estimated by non-linear regression of W Throughout this discussion, we have fo- versus L, or by log-log regression (Bolger cused primarily on stored energy reserves and Connolly, 1989). Alternatively, condi- (measured directly or estimated as being tion can be estimated as the residuals about proportional to weight scaled to length) as a W versus L regression line, or one can our measure of condition; however, body compute partial correlations between poten- size and immunocompetence may also be tial condition indicators and weight, while important determinants of lifetime repro- holding the effects of length constant. Pre- ductive success. liminary studies in our laboratories suggest First, consider body size. It has been well that components of fin morphology and of documented in fishes that survival and fe- breeding coloration may be correlated with cundity depend more on body size (i.e., condition, in some cases in both sexes of mass) than on age (e.g., Werner and Gil- fishes. We are pursuing this further. liam, 1984; Sargent etal, 1987). Large fish have higher rates of fecundity, mating suc- 3. Honest signaling in both sexes cess, and survival than small fish (Werner and Gilliam, 1984; Gross and Sargent, In most genetical models of sexual selec- 1985; Andersson, 1994). Thus, body size is tion (e.g., Lande, 1980, 1981; Kirkpatrick, clearly an important component of overall 1982), the limiting sex exhibits the mating condition in fishes. preference and the limited sex exhibits the Second, consider immunocompetence ornament. For this reason, most empirical (Hamilton and Zuk, 1982; Folstad and studies have focused on sexual selection in Karter, 1992). In many fishes, females the limited sex, typically males (see An- avoid parasitized males (see Andersson dersson [1994] for review). However, in re- [1994] for review). In guppies and stickle- cent game theoretical models, Crowley et backs, certain parasites result in a reduction al. (1991) and Johnstone et al. (1996) found of male orange or red, carotenoid-based that under certain conditions it pays both breeding coloration (Houde and Torio, sexes (i.e., the limiting and limited sexes) 1994; Milinski and Bakker, 1990; but see to be choosy. Even though females are the Folstad et ah, 1994), and in Arctic charr, limiting sex in sticklebacks (e.g., Sargent male red breeding coloration is positively and Gebler, 1980), male sticklebacks do ex- correlated lymphocyte density in the blood hibit mate choice based on female body size (Skarstein and Folstad, 1996). How one and fecundity (Rowland, 1982, 1989; Sar- measures immunocompetence may be prob- gent et al., 1986), and females adopt a lematic, but future research on immuno- breeding coloration that signals when they competence, sexual selection, and the po- are receptive to males (Rowland et al., tential role of carotenoids should be very 1991). Furthermore, in several species of rewarding. We suggest that empiricists ex- the biparental cichlid genus, Cichlasoma, plore how body size, energy reserves, and females are the more colorful sex (Turner, immunocompetence interact to determine 1993). Finally, most sex pheromone signals lifetime reproductive success, and that the- seem to be produced by females. We sug- oreticians explore the implications of these gest that theoreticians develop genetical interactions for multi-modality honest sig- models of intersexual selection for both naling. sexes simultaneously, and explore the co- COURTSHIP AND MATE CHOICE IN FISHES 91 evolution of honest signaling in both sexes. Also, it would be interesting to see if the We suggest also that empiricists look for strength of female preference is correlated condition dependence and honest signaling with mean male sword length among spe- in both the limited and limiting sexes. cies of Xiphophorus, which may indicate a coevolution between female preference and 4. Sensory or pre-existing bias versus male ornament in addition to the pre-exist- condition indicators ing bias. Throughout our discussion we have em- phasized a coevolution between female 5. Empirical studies that explore more preference and male ornament. There is ev- than one sensory modality idence in swordtails (Xiphophorus) that the Fish ethologists who study visual cues "sword" (i.e., a ventral extension of the have traditionally separated their stimulus caudal fin that develops as males reach ma- and focal fish with transparent glass or plas- turity) may have evolved through a sensory tic partitions (e.g., Sargent and Gebler, or pre-existing bias in female preference 1980). Users of transparent partitions are (Ryan and Wagner, 1987; Basolo, 1990a, b, cautioned that not only do these partitions 1995a, b). Female Xiphophorus prefer block chemical cues and the particle move- males with swords, whether or not the ment that is generated by low frequency males of their species have swords; in ad- mechanosensory cues (e.g., during a lateral dition, female Priapella olmecae (the out- display), but most of them are also effective group genus to Xiphophorus) also prefer filters of ultraviolet light, and many fishes males with swords (Ryan and Wagner, are known be able to see ultraviolet light 1987; Basolo, 1990a, b, 1995a, b), even (Jacobs, 1992; Archer, 1988; Rush, 1995). though swords are not known in this genus. In fact, we have preliminary data for a poe- Whether or not phylogenetic comparative ciliid that males have UV breeding colora- data within the genus, Xiphophorus, sup- tion, and that females prefer males behind ports the pre-existing bias hypothesis is UV transparent over UV filtering partitions controversial (Meyer et al, 1994; Basolo, (Rush et al., unpublished). 1995a; Wiens and Morris, 1996); however, We suggest that empiricists who study Basolo's (19956) recent demonstration of communication between the sexes explore female preference for males with swords in two or more sensory modalities in combi- the "sword-less" outgroup genus, Priapel- nation. For sensory ecologists, this may re- la, does favor this hypothesis. What about quire collaboration among research labora- condition dependence in swordtails? tories; however, behavioral ecologists might Basolo (1998) found that male green approach the problem with simple factorial swordtails (Xiphophorus helleri) on restrict- experimental designs. If factorial-design ex- ed diets produced swords as large as males periments of mate choice indicate that sen- that were fed ad libidum, despite the fact sory cues from two sensory modalities pro- that males on the restricted diet had reduced duce a greater response in the receiver than growth in body size. These data suggest either cue alone (either additively or mul- that swords may not be honest indicators of tiplicatively), then it becomes interesting to male quality. To our knowledge, sword investigate how these modalities interact at length has not been compared to condition both ethological and physiological levels. index or energy reserves within a species. Alternatively, sensory biologists who have It appears that morphological traits such as already determined that two sensory mo- fin size reflect the conditions that prevailed dalities interact on a physiological level can when their development was initiated. As set the stage for behavioral ecological ex- such, they may be relatively fixed and less periments. reliable as "instantaneous" condition indi- cators than an ephemeral color pattern (see ACKNOWLEDGMENTS Kodric-Brown, 1998), which can reflect We thank Lee Drickamer for organizing more short-term fluctuations in condition. this symposium, for soliciting our partici- This is certainly worth further investigation. pation, and for coordinating the publication 92 R. C. SARGENT ETAL. of this volume. We thank the following for Basolo, A. L. 1998. Shift in investment between sex- ually selected traits: Tarnishing of the silver advice and discussion: Theo Bakker, spoon. Anim. Behav. (In press) George Barlow, Alexandra Basolo, Andrew Bass, A. H. and M. A. Marchaterre. 1989. Sound- Bass, Charles Baube, Edmund D. Brodie generating (sonic) motor system in a teleost fish III, David Crews, John Endler, Patricia Go- (Porichthys nolatus): Sexual polymorphism in the waty, Astrid Kodric-Brown, Allen Moore, ultrastructure of myofribils. J. Compar. Neurol. Stephen Nowicki, John Phillips, William 286:141-153. Bass, A. H. and R. Baker. 1990. Sexual dimorphisms Rowland, Frode Skarstein, Paul Verrell, Ja- in the vocal control of system of a teleost fish: son Wolf and an anonymous reviewer. Morphology of physiologically identified neurons. Manuscript preparation was supported by a J. Neurobiol. 21:1155-1168. Bridge Grant to RCS from the Vice Chan- Bass, A. H. and R. Baker. 1991. Evolution of homol- cellor for Research and Graduate Studies at ogous vocal control traits. Brain, Behav. Evol. 38: 240-254. the University of Kentucky, by a Seed Bateman, A. J. 1948. 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