The Evolution of Monogamy in Primates: a Phylogenetic Approach

Home , Atelidae, Atelinae, Black lion tamarin, Breeding pair, Cebidae, Cheirogaleidae

THE EVOLUTION OF MONOGAMY IN PRIMATES: A PHYLOGENETIC APPROACH

A thesis submitted

to Kent State University in partial

fulfillment of the requirements for the

degree of Master of Arts

Alana Hope Muhlberger

May, 2011

Thesis written by Alana Hope Muhlberger B.A., Ohio University, 2009 M.A., Kent State University, 2011

Approved by

______, Advisor

Marilyn A. Norconk

______, Chair, Department of Anthropology

Richard S. Meindl

______, Associate Dean, College of Arts and Sciences

John Stalvey

ii TABLE OF CONTENTS

LIST OF FIGURES ...... v

LIST OF TABLES ...... vi

ACKNOWLEDGEMENTS ...... vii

CHAPTER 1: INTRODUCTION ...... 8

1.1 Social System Terminology ...... 11

1.2 Monogamy ...... 12

1.3 Previous Work ...... 19

1.4 Research Questions ...... 22

CHAPTER 2: METHODS ...... 25

2.1 Characters and Coding ...... 25

2.1.1 Social Organization ...... 25

2.1.2 Pair-Bond ...... 26

2.1.3 Duet Vocalizations ...... 28

2.1.4 Paternal Care ...... 29

2.1.5 Territorial Exclusivity ...... 30

2.1.6 Mechanisms of Territorial Defense ...... 31

2.1.7 Sexual Dimorphism in Body Mass ...... 32

2.2 Species Used in the Analysis ...... 33

2.3 Sources of Data ...... 36

2.4 Phylogenetic Reconstruction ...... 37

iii CHAPTER 3: RESULTS ...... 41

3.1 Social Organization ...... 41

3.2 Pair-Bond ...... 45

3.3 Duet ...... 47

3.4 Paternal Care ...... 49

3.5 Territorial Exclusivity ...... 51

3.6 Mechanisms of Territorial Defense ...... 53

3.7 Sexual Dimorphism ...... 56

3.8 Multi-Trait Comparisons ...... 63

CHAPTER 4: DISCUSSION ...... 65

4.1 Potential Confounding Factors ...... 65

4.2 Discussion of Research Questions ...... 66

CHAPTER 5: CONCLUSIONS ...... 77

APPENDICES

Appendix A: Summary Database with Abbreviations ...... 80

REFERENCES ...... 83

iv LIST OF FIGURES

FIG. 1.1 Phylogenetic Reconstruction From Komers And Brotherton (1997) ...... 21

FIG. 2.1 Primate Phylogeny of Species Used in This Study ...... 40

FIG. 3.1 Reconstruction of Social Organization ...... 44

FIG. 3.2 Reconstruction of Pair-Bonding ...... 46

FIG. 3.3 Reconstruction of Duetting ...... 48

FIG. 3.4 Reconstruction of Paternal Care ...... 50

FIG. 3.5 Reconstruction of Territorial Exclusivity ...... 52

FIG. 3.6 Reconstruction of Mechanisms of Territorial Defense ...... 55

FIG. 3.7 Reconstruction of Sexual Dimorphism in Lemuroidea ...... 58

FIG. 3.8 Reconstruction of Sexual Dimorphism in Lemuroidea ...... 59

FIG. 3.9 Reconstruction of Sexual Dimorphism in Tarsiidae ...... 60

FIG. 3.10 Reconstruction of Sexual Dimorphism in Cebidae ...... 61

FIG. 3.11 Reconstruction of Sexual Dimorphism in Atelidae ...... 62

FIG. 3.12 Lineage-Specific Evolution of Monogamy ...... 64

LIST OF TABLES

TABLE 1.1. General Patterns of Primate Social Systems ...... 10

TABLE 2.1 Coding the Category “Social Organization” ...... 26

TABLE 2.2. Coding the Category “Pair-Bond” ...... 27

TABLE 2.3. Coding the Category “Duet Vocalizations” ...... 29

TABLE 2.4. Coding the Category “Paternal Care” ...... 30

TABLE 2.5. Coding the Category “Territorial Exclusivity” ...... 31

TABLE 2.6. Coding the Category “Mechanisms of Territorial Defense” ...... 32

TABLE 2.8. Primate Taxonomy Used in This Study ...... 36

ACKNOWLEDGEMENTS

First, I would like to thank my advisor, Marilyn Norconk, for her openness to my ideas and her support and encouragement throughout the thesis process. Chi-hua Chiu is responsible for my interesting topic, and Mary Ann Raghanti was a patient and helpful sounding board and source of advice throughout my time at Kent. These three women have been inspiring and I am glad to have had the opportunity to work with them. The department of Anthropology would not be the same without our wonderful secretary,

Caroline Tannert, whose organization and desire to help made the road to completion easier for myself and my peers. I would also like to thank Cynthia Thompson, Tremaine

Gregory, Eric Seemiller, and Michael Veres for their input in our advisor meetings. My office-mate Cyndie has been especially invaluable, and I am grateful for her patient answers to my questions and for being a friend. Thank you to my parents, Beth and

Gordon, to my brother, Eric, and to my boyfriend, Randy, for reading my drafts and sending me your love and support. This thesis has been possible and enjoyable because of all the people mentioned here.

vii

CHAPTER 1

INTRODUCTION

1.1 Social System Terminology

In early studies of animal social systems, mating systems were equated with social systems, but observations of extra-group matings, reproductive suppression, and varying mating patterns of solitary foragers have prompted researchers to separate mating behavior from social behavior (Palombit, 1994; Manson, 2011; Goldizen, 1990). This has led to a modern terminology that subsumes mating system under the umbrella term

‘social system’, which also encompasses social organization and social structure (Zinner et al., 2003; Sterling, 1993; Kappeler and van Schaik, 2002). While mating system describes patterns of mating behavior and considers the genetic composition of the group's offspring (Emlen and Oring 1977), social organization is composed of group size, sexual composition, and cohesion of a group (Müller and Thalmann, 2000; Kappeler and van Schaik, 2002), and social structure describes the social relations among individuals

(Zinner et al 2003).

There are several generally accepted types of social systems. A list of mating systems, which are a part of social systems, might include monogamy (one breeding male and one breeding female), polygyny (one breeding male, multiple breeding females), polyandry (one breeding female, multiple breeding males), and polygynandry (multiple breeding males and females) (Bertram and Gorelick, 2009). Kappeler (1997) lists and

describes the characteristics of seven social organizations: solitary, pair-living, polyandrous, single-male, multi-male, male-bonded, and multi-level (Table 1.1).

In solitary species, individuals forage alone but may sleep in multi-adult conspecific groups. According to Kappeler (1997), pair-living species live in closely associated bisexual pairs, but some writers consider there to be two types of pair living, associated and dispersed (i.e., Kappeler and van Schaik, 2002; Mendez-Cardinas and

Zimmermann, 2009). Dispersed pairs share and cooperatively defend a range, but generally forage separately. In contrast, associated pairs are permanently spatially associated (van Schaik and Kappeler, 2003). Kappeler (1990) combines the definitions of social and sexual polyandry so that his description of polyandry consists of a reproductively active female and usually two male mating partners, but technically a polyandrous social group would have one adult female and more than one adult male, and all other members of the group would be immatures (Müller and Thalmann, 2000;

Kappeler and van Schaik, 2002).

The single-male group consists of one adult male and several adult females within a shared territory (Kappeler, 1997). Kappeler (1997) uses the term ‘multi-male’ for social groups of several adult males and females, and while male-bonded species are also composed of this demographic makeup, members create temporary subgroups that have led to the description ‘fission-fusion’ for these societies. Lastly, Kappeler (1997) describes multi-level groups as large conglomerations of many males and females that are subdivided into smaller units, the smallest of which is typically one male and several females (Table 1.1). 10

Table 1.1: General Patterns of Primate Social Systems

Social Social system Mating system Social organization structure Mating Social system, social Patterns of Predicted Sexual relations organization, mating genetic Group size Cohesion* composition between and social behavior paternity individuals structure Polygyny, Female- 1-15 Individuals polygamy, biased Solitary Varies (nocturnal Dispersed may sleep or neighborhood lemurs) together monogamy ** Cohesive 2-5 (titi One male, Monogamy Monogamy 100% or Pair-bonds monkeys) one female dispersed 3-15 One female, Polyandry Polyandry 50% Cohesive Pair-bonds (marmosets) several males Male-female One male, and/or 8 - 20 Single male Polygyny 100% several Cohesive female- (gorillas) females female bonding Female- Multiple female 7 - 53 Multi-male Polygamy Varies males and Cohesive and/or male- (guenons) females male bonding Polygamy 15 - 140 Multiple Fission- Male-bonded or Varies (chimpan- males and Males bond fusion polygyny zees) females Males bond Smallest unit: or several 100% at ≥800 one male, Fission- Multi-level Polygyny females smallest unit (baboons) several fusion bond with a females male Table compiled from Kappeler (1997), Fuentes (1999), Dacanini and Macedo (2008), Gould et al. (2011), Jaffe and Isbell (2011), Norconk (2011), Sussman (2000), Stumpf (2011), Swedell (2011), M. Norconk pers. comm. *Cohesion is defined as a consistently close spatial association between group members. **In neighborhoods, “individuals do not live in distinct social units but are decreasingly familiar with others that overlap increasingly less with their own home ranges” (Kappeler and van Schaik, 2002:711). Female biased neighborhood refers in the fact that the sex ratio in neighborhoods tends to be biased toward females (Norconk, pers. comm.).

1.2 Monogamy

Monogamy is an odd social system according to the expectations of sexual selection theory. According to Stacey (1982), monogamous mating, in which one male mates with one female during the breeding season (Bertram and Gorelick, 2009), is a curious phenomenon because female and male reproductive strategies differ in mammals.

Females have high investment (time and energy) in gestation and lactation relative to the presumed investment of finding a mate by males. As such, it would be beneficial for males to seek out more than one mate to increase reproductive fitness relative to the reproductive constraints imposed on females (Trivers, 1972; van Schaik and Kappeler,

1997).

Sexual selection theory predicts that males have higher reproductive potential because males produce more gametes at lower cost than do females and can achieve greater reproductive output than females via multiple matings. Males are limited by the number of reproductive females that they can gain access to, but females are limited by the costs of internal gestation and lactation. Due to higher costs per reproductive event, females should be much more selective about choosing a mating partner (Stacey, 1982;

Kodric-Brown and Brown, 1987). In a monogamous mating system, males give up their high reproductive potential so that his reproductive success is equal to his mate's. At first glance this appears to be a deleterious situation for monogamous males because of their capacity for inseminating many females at relatively low physiological cost (Trivers,

1972). 12

Monogamy is estimated to occur in 90% of bird species, possibly because paternal care is both non-shareable and necessary for both male and female reproductive success in many birds (Wittenberger and Tilson, 1980; Moller, 2003). However, monogamy exists in low frequencies in invertebrates, fish, amphibians, reptiles, and mammals (Möller, 2003). Kleiman (1977) reports that about 3% of mammalian species appear to mate monogamously, but among primates this mating system is more common.

It is estimated to occur in about 15% of species (including our own) spread across numerous primate families (Kleiman, 1977; Wickler and Seibt, 1983; van Schaik and

Dunbar, 1990).

A number of hypotheses have been proposed for the evolution of monogamy, which has attracted much attention in the biological community due to the potential reduction of male fitness (Sommer, 2003; Kleiman, 1977; Wrangham, 1979;

Wittenberger and Tilson, 1980; Rutberg, 1983; van Schaik & van Hooff, 1983).

Hypotheses on the evolutionary pathways that led to monogamy tend to focus on the themes of mate defense (i.e. Wittenberger and Tilson, 1980), resource defense (i.e.

Overdorff and Tecot, 2007), paternal care of offspring (i.e. Kleiman, 1977), and infanticide prevention (i.e. van Schaik and Dunbar, 1990).

The first theme, mate defense, was summarized by Reichard (2003), who wrote that in circumstances where females are widely spaced due to resource competition, males might be resigned to monogamy because they have higher reproductive success guarding and mating with one female than if they continually search for wide-spread mates. Wittenberg and Tilson (1980) added that monogamy due to mate guarding is most 13

likely to evolve when sex ratios are male biased. Then, males would risk low reproductive success competing against each other for scarce females. Even if females do not benefit from being guarded, they might accept this situation if the costs of being guarded do not outweigh the benefits.

Overdorff and Tecot (2007) reviewed the second scenario where monogamy is the result of resource defense. In this case a male defends a territory for himself, one female, and their offspring. Both members of the pair benefit from this arrangement because together they are less susceptible to predation and are less likely to be displaced from feeding sites by other social groups. Further, their joint reproductive success is increased because improved maternal nutrition increases infant survival rates (Fuentes, 2002;

Overdorff and Tecot, 2007). The group does not increase in size beyond the pair because additional males would decrease individual male reproductive success and additional females would create more competition for food (Overdorff and Tecot, 2007).

Kleiman (1977) wrote a classic paper on the third theme of paternal care, proposing that one form of monogamy, which she termed “obligate,” evolved in some species because conspecific aid was necessary for raising offspring but the environment could not support more than one breeding female. The monogamous social system would also reinforce extensive paternal care because infant survival is especially important to males who have a high probability of paternity. van Schaik and Dunbar (1990) added that body size appears to affect group size in primates whose females need extra help in raising offspring: for example, in callitrichines older offspring and even additional males help care for offspring due to the high infant:mother weight ratio, but Aotus (owl 14

monkey) and Callicebus (titi monkey) adults are large enough that assistance from only one group member, the adult male, is necessary.

The fourth theme, infanticide prevention, was reviewed by van Schaik and

Dunbar (1990), who theorized that monogamy may have evolved when close spatial association between a male, a female, and their infant would significantly increase the infant's survival due to the resident male’s protection from outside, infanticidal males.

Palombit (1999) added that the female is expected to invest heavily in maintaining this social organization. Presumably, the male assumes the costs of defending the infant from attacking males because his guarding actions in the past assured his paternity (Kleiman,

1977).

Although a basic definition of monogamy is Wittenberger and Tilson's (1980): “a prolonged association and essentially exclusive mating relationship between one female and one male,” in recent literature the term can refer to social, sexual, or genetic monogamy (Fuentes 1999, Reichard 2003). Gowaty (1996) defines social, or sociographic, monogamy, or as “one female–one male groups,” or a situation in which an individual has only one spatially-associated partner of the opposite sex at a time. Because the definition refers to a spatial association, this type of monogamy is a social organization (Müller and Thalmann, 2000; Kappeler and van Schaik, 2002), which is the focus of this thesis. According to Reichard (2003), sexual monogamy is an exclusive sexual relationship between a male and a female, and Fuentes (1999) writes that genetic monogamy means that each member of the pair contributes to 50% of the genetic 15

composition of each offspring, or that the offspring’s genetic composition is derived from the pair members only.

Because this thesis focuses on correlates of pair-living (a demographic arrangement and therefore a type of social organization), the definition of monogamy used here is Gowaty’s (1996) description of social monogamy, in which monogamy is synonymous with pair living. This study focuses on pair-living and its correlates because an analysis of mating system is difficult due to the need to both observe copulations and determine genetic paternity; thus, mating system has often been inferred from group composition (Fuentes, 2002). Palombit’s (1994) landmark paper spurred researchers to separate mating system from social organization in monogamous species. As a result, recent papers have noted that nuclear family groups do not necessarily also have pair- exclusive mating (e.g. Fietz et al., 2000; Schulke and Kappeler, 2004).

Many primate species exhibit a high degree of variation in their behavioral patterns (including mating behavior) that makes them difficult to place into any one social system category. This has led a number of authors to break down monogamy into two or more types, such as cohesive vs. dispersed pairs (Zinner et al., 2003; Müller and

Thalmann, 2000; Kappeler and van Schaik, 2002), lifetime vs. serial monogamy

(Reichard, 2003), and facultative vs. obligate monogamy (Kleiman, 1977; van Schaik and

Dunbar, 1990). In the Zinner et al. (2003) scheme, cohesive and dispersed pairs differ in their spatial associations in that associated pairs frequently interact with one another while dispersed pairs share a home range, but are not consistently together. Reichard's

(2003) classification distinguishes permanent pairs from temporary ones, and Kleiman 16

(1977) separates those species in which the necessity of paternal care seems to have been the evolutionary impetus for monogamy from those in which monogamy is considered to be the result of very low population densities.

A common approach to studying monogamy has been to treat sexual monogamy, pair-bonding behaviors, and territoriality as inseparable elements of one social system

(van Schaik and Dunbar, 1990). In fact, several suites of traits have been proposed to describe monogamy, such as Fuentes' (1999) definition of a monogamous species as one that exhibits an occurrence of two-adult groups throughout its range, a prolonged association between the two adults in the group, pair-bonding, and a long-term monogamous mating pattern. Other traits that Fuentes (1999) associates with monogamy

include a nuclear family unit, mate guarding, sexual monomorphism, and 50%

contribution to the genetic composition of the offspring by each adult. van Schaik and

Dunbar (1990) created a list of three features common in large, diurnal monogamous

primates that includes territorial defense, solo singing, and duetting by both members of

the bonded pair.

Further, Rothe (1975) proposes that an emotional bond (the pair-bond) is a

requirement for monogamy. According to Fuentes (1999), the social structure of a monogamous pair is expected to be a relationship called a “pair-bond,” which is indicated by “strong mutual attraction, a close spatial relationship, partner-specific behaviors, and signs of distress during separation from the pairmate” (Anzenberger 1992, reviewed in

Fuentes, 1999). Rothe (1975) proposes that the pair-bond is not only associated with monogamy, but is also a requirement for a species to be called “monogamous” because 17

Callithrix jacchus (the common marmoset) appears to breed monogamously in multi- male groups due to an emotional bond between the breeding male and female.

Many primate species have social organizations that are characterized by two or more traits that are associated with monogamy, for example group size limited to the breeding pair and their juvenile offspring (Fuentes, 1999) and shared use and defense of a territory (Fuentes, 1999; Reichard, 2003), but do not conform to some other expectations such as pair-bonding or paternal care of offspring (Fuentes, 1999). An example of a species that displays this variability in monogamous features is Phaner furcifer (the fork- marked lemur). Pairs defend a common territory and usually live in small nuclear family groups, but only spend ¼ of their activity time together and do not demonstrate paternal care (Schulke, 2005). Further, a lack of pair-bonding behaviors in this species is confirmed in a review of primate pair-bonding literature by Fuentes (2002).

Researchers have disagreed over the social system status of many primate species similar to Phaner furcifer because they display some common markers of monogamy but not others. For instance, Fuentes (1999) goes through a list of purportedly monogamous species and dismisses most of them as not monogamous because they do not fit his minimum criteria. These are (1) occurrence in two-adult groups throughout its range, (2) a prolonged association between the two adults in the group (greater than one breeding season, as per Wittenberger and Tilson 1980), (3) pair-bonding (as per Anzenberger,

1992), and (4) a long-term monogamous mating pattern. While Fuentes takes the position that variability in mating behavior removes a species from “monogamous” status, this thesis explores the variability within the social system and treats many species 18

as “partially monogamous.” This phrase encompasses species that consistently exhibit some but not all monogamous traits or exhibit features of monogamy in some populations but not others.

Besides Phaner furcifer, another species that falls under the first category of partially monogamous species is Lepilemur edwardsi (Milne-Edwards’ sportive lemur), which occurs only in two-adult groups (Mendez-Cardenas and Zimmermann, 2009), defends strict territories (Thalmann, 2006), displays behaviors indicative of a pair-bond

(Mendez-Cardenas and Zimmermann, 2009), and is sexually monomorphic in body mass

(Kleiman, 1977; Smith and Jungers, 1997). However, males of this species do not provide any care for their offspring (Thalmann, 2006).

Tarsiers (genus Tarsius) and many other primate species fall under the second category of ‘partially monogamous” primates due to population-level variation in social organization. Some more extreme examples of this are Propithecus verreuxi (Verreaux's

Sifaka) and Leontopithecus chrysomelas (Golden-Headed Lion Tamarin), which have been observed in five types of social organization each. These social organizations are dispersed pairs, associated pairs, one-male, polyandry, and multi-male groups in

Propithecus (Müller and Thalmann, 2000; van Schaik and Kappeler, 2003; Brockman,

1994; Gould and Sauther, 2007; Kappeler et al., 2009) and associated pairs, intersexual

dyads (reproductive suppression), 1-male, polyandry, and multi-male in Leontopithecus

(Rowe 1996, Raboy 2002). These two species also consistently maintain strict territories

(Propithecus: Sussman and Richard, 1974; Pochron et al., 2004; Leontopithecus: Raboy,

2002), defend these territories through loud calls or scent marking (Propithecus: Pochron 19

et al., 2005; Benadi et al., 2008; Leontopithecus: Epple et al., 1993), and display paternal care of infants (Propithecus: Komers and Brotherton, 1997; Bastian and Brockman,

2007; Kappeler et al., 2009; Leontopithecus: Sussman 2000).

1.3 Previous work

Previous researchers have used phylogenetic methods to explore the origins of pair living in primates (e.g. van Schaik and Kappeler, 2003), social systems (e.g.

Kappeler, 1999) and the relationships between two or more social traits that have been associated with monogamy (e.g. Komers and Brotherton, 1997: the evolution of monogamy, paternal care, and discrete female ranges). Harvey and Pagel (1991:50) defined a phylogeny as “a genealogical history of a group, hypothesizing ancestor- descendent relationships.” Ryan (1996) noted that, as of the time of his writing, there seemed to be some consensus among ethologists that phylogenetic studies are a necessary supplement to the field of animal behavior, and McLennan et al. (1988) noted that phylogenetic trees are useful in testing hypotheses of behavioral evolution, such as whether traits are due to homology or analogy.

Harvey and Pagel (1991) similarly commented that knowledge of phylogenies and ancestral traits allows for tests of the direction of evolution, which is a subject considered in this thesis. Although Ryan (1996) pointed out that phylogenetic reconstructions are only as robust as the phylogenetic trees they are based on and thus should be viewed with caution, he stated that the history of a behavior is key to fully understanding it, and that if any social science can benefit from phylogenetics it is ethology. It should be emphasized that di Fiore (2003) added that there is no evidence supporting the notion that behavioral 20

traits are not as phylogenetically informative as morphological and genetic characters, as homoplasy (inter-taxa similarity due to convergent evolution) does not appear to occur more often in behavioral systems than others.

There are several examples of primate researchers who have used phylogenetic methods to map ancestral traits and study the evolution of behavioral characteristics. For instance, van Schaik and Kappeler (2003) mapped “variable pairs” and “uniform pairs” onto a strepsirhine phylogeny and concluded that pair-living originated in its “variable” form in the most recent common ancestors of the families Cheirogaleidae, Lemuridae,

Megalapidae, and Indriidae (for primate taxonomy, see table 2.1). The authors defined variably pair-living species as those in which all groups are not socially organized as nuclear families. In contrast, in uniformly pair-living species groups are nearly always composed of a bisexual pair and their immature young.

Similarly, Kappeler (1999) reconstructed the ancestral primate social organization as solitary, with the next most recent to evolve being group-living, and then finally pair- living at the most recent common ancestor of Callicebus (titi monkeys) and Aotus (owl monkeys). Komers and Brotherton (1997) were the first workers to use phylogenetic reconstruction in the study of primate monogamy. In this landmark study, the authors tested Kleiman’s prominent hypothesis on the origin of primate monogamy by mapping three traits (paternal care, discrete female ranges, and monogamy) onto a phylogeny and performing statistic tests on their association (Figure 1.1). Komers and Brotherton (1997) concluded that paternal care was not an important driving force because monogamy evolved significantly more often in the absence of paternal care than in its presence. 21

Figure 1.1: Phylogenetic Reconstruction from Komers and Brotherton (1997)

The Komers and Brotherton (1997) study was very informative and provided inspiration for this thesis, which maps seven traits associated with primate pair-living onto a phylogeny in order to better understand the keystone features and evolutionary history of monogamy. The analysis of seven traits as opposed to three makes the current project applicable to understanding of the complex mosaic evolution of monogamy, as opposed to simply its origin. In order to carry out this goal, phylogenetic methods were used to reveal the evolutionary history and interaction of the following traits: social organization (Kappeler and Van Schaik, 2002), pair-bonding (Fuentes, 2002), duet vocalizations (van Schaik and Dunbar, 1990), paternal care of infants (Reichard, 2003), 22

territorial exclusivity (Bearder, 1987), mechanisms of territorial defense (van Schaik and

Dunbar, 1990), and sexual dimorphism of body mass (Gaulin and Sailor, 1984).

1.5 Research Questions

Komers and Brotherton (1997) demonstrated the usefulness of phylogenetic reconstruction in studying the evolution of primate behavior. The main difference between their study and the current project lies in the number of traits being traced: this analysis traces the evolution of pair-living and six of its correlates, while Komers and

Brotherton (1997) reconstructed the evolution of only three traits. Because of the large number of characters used here, the results of this thesis can provide input on a number of published statements about the evolution of monogamy. I have paraphrased or taken quotations from several papers that make statements about the evolution of monogamy and, in Chapter 4, discuss how the results of this project contribute to those questions and support or refute previous statements. The hypotheses I comment on in Chapter 4 are the following:

1. Monogamy has many forms and has evolved in lineage-specific patterns

(Reichard, 2003:5).

2. The two-adult group or pair-bonding or both may have evolved separately 4–7

times (Fuentes, 2002)

3. “It remains […] unknown whether monogamy or a multi-male system is the

ancestral pattern of primate social organisation” (Müller and Thalmann,

2000:425). 23

4. “The gregarious patterns of social organisation in Aotus [owl monkeys] and Avahi

[woolly lemurs], and the dispersed form in Tarsius [tarsiers] evolved from the

gregarious patterns of diurnal primates rather than from the dispersed nocturnal

type” (Müller and Thalmann, 2000:405).

5. Twinning either evolved at the same time or after pair-bonding [in callitrichids],

when the resulting consistent male presence allowed the evolution of high levels

of male parental care for offspring (Dunbar, 1995).

6. The evolution of extant callitrichine social systems might have followed a

temporal pattern of 1) single births and unknown social system, 2) obligate

monogamy, 3) extensive paternal care, 4) twinning and helping by older

offspring, and 5) facultative polyandry (Goldizen, 1990).

7. It appears that paternal care and monogamy are associated by chance (Komers

and Brotherton, 1997).

8. Male long calls may have evolved to attract females by defending resources

important to them (Wich and Nunn, 2002)

The discussion in Chapter 4 provides input to the above statements as well as answers to some of my own questions, including:

9. What was the social organization of the common ancestor of Ceboidea,

Tarsioidea, and Lemuroidea?

10. Did pair-bonding mechanisms or paternal care evolve first in 'obligately'

monogamous primates (Kleiman 1977)? 24

11. Given the selection of taxa in this thesis, when was the first appearance of

duetting and what were its evolutionary correlates?

12. Did monomorphism re-evolve as a result of pair-bonding?

13. Were pair-bonding behaviors present in the most recent common ancestors of taxa

that demonstrate diversity in social organization, such as Pitheciinae?

CHAPTER 2

METHODS

2.1 Characters and Coding

This project traces the evolutionary history of seven traits in platyrrhines, lemurs,

and tarsiers that have been associated with monogamy in its various forms in the primate

literature. In order to demonstrate the mosaic evolution of social monogamy as complex

phenomenon, various components of the monogamy package were chosen that could be

individually traced to create a clearer picture of its evolution.

2.1.1 Social Organization

The first trait, social organization, was included as part of separating the

elements of the monogamous social system into social organization (pair living) and

social structure (pair-bonding). Although social systems are comprised of three

elements, social organization, social structure, and mating system, mating system was

not included in this thesis because researchers often infer mating system from social

organization in primate studies (Fuentes, 1999).

Because the qualitative data in the literature often needed to be converted to

numeric data for use in the computer program Mesquite (Maddison and Maddison, 2010),

I used various coding methods and decisions to convert my data into numeric form. To

code Social Organization I created seven categories (Table 2.1). These choices were

guided by an emphasis on monogamy, hence two character states designate pair-living

(van Schaik and Kappeler, 2003; Mendez-Cardinas and Zimmerman, 2009). Other possible terms (e.g., fission-fusion and male-bonded groups) were subsumed into the seven categories below (after Kappeler, 1997). The fourth category encompasses both reproductive suppression in callitrichines (Rowe, 1996) and the possibility of multi-pair groups in Eulemur (true lemurs) (Gould and Sauther, 2007) because some researchers have recorded pair-bonding to occur in callitrichine and Eulemur multi-male groups (e.g.

Eulemur: Ostner and Kappeler, 1999; Callithrix jacchus (common marmoset): Evans and

Poole, 1984).

Table 2.1: Coding the Category: “Social Organization”

Social Organization Description Citation Individuals forage alone but may 1. Solitary form sleeping groups with Kappeler, 1997 other adults Pairs forage alone but sleep Mendez-Cardinas and 2. Dispersed pairs together Zimmermann, 2009 3. Associated One adult male and female are Kappeler, 1997 pairs permanently associated Multiple pairs share a territory or 4. Intersexual multi-male groups exhibit female none dyads reproductive suppression Groups consist of one adult male 5. Single-male Kappeler, 1997 and several adult females One adult female is associated Müller and Thalmann, 6. Polyandry with several adult males 2000 Several adult males and females 7. Multi-male Kappeler, 1997 are permanently associated

2.1.2 Pair-Bond

Fuentes (1999) wrote that the two most pronounced concepts associated with monogamous mating are the nuclear family unit and the pair-bond, and for this reason, pair-bonding is the second trait explored in this thesis (Table 2.2). In a follow-up paper,

Fuentes (2002) reviewed the literature on primate pair-bonding and wrote that a generally accepted definition of pair-bonding is a specialized, predictable relationship between an adult male and an adult female. Anzenberger (1992:205) wrote that a pair-bond can be determined by “indications of strong mutual attraction, a close spatial relationship, partner-specific behaviors, and signs of distress during separation from the pairmate.”

Some behaviors that have been interpreted as indications of a pair-bond are:

a. Duetting (Fan et al., 2009; described below)

b. Reduced aggression with the pair partner compared to aggression with other

group members (Overdorff, 1998)

c. Various specialized forms of contact such as tail twining in Callicebus (Fuentes,

1999) van Schaik and Dunbar (1990) emphasize that exclusive mating and pair-bonding are separate traits and do not necessarily imply each other, which is another reason for including pair-bonding in this thesis.

Table 2.2: Coding the Category: “Pair-Bond”

Pair-Bond Description Citation Multi-male groups, 1. Absent statement of absence in Fuentes, 1999, 2000 literature, or no information Statement of presence in 2. Present none literature Some studies have reported bonds and others have not; van Schaik and 3. Variable some groups appear to have Kappeler, 2003 bonded pairs and others do not

If there is no mention in the literature whether a species exhibits pair-bonds or

not, I coded that species as (1) absent. This is because, as stated Fuentes (2002) (and

supported by my results), pair-bonding is a derived trait. Therefore, if any assumption is

to be made, species should be assumed to have the primitive condition of not displaying

pair bonds. Pair-bonding is coded as (2): present in species which have been described as

pair-bonded and for which there is no contention over whether or not adult males and females exhibit special pair-specific behaviors indicative of bonding.

”Variable” bonds are considered to exist in species 1) for which some studies have reported bonds and others have not, or 2) in which some groups appear to have

bonded pairs and others do not. An example of a variably pair-bonded species is Eulemur

fulvus (the brown lemur), which van Schaik and Kappeler (2003) coded as living in

‘variable pairs’, Gould and Sauther (2007) reported as exhibiting ‘strong affiliative

dyadic relations’, and Overdorff (1998) considered to live in multi-male groups

containing various types of subgroups, including bisexual pairs. This is an example of a

species that was coded as variable because there is contention in the literature over their 29

pair-bonded status. Eulemur mongoz (the mongoose lemur), on the other hand, received a code of 3) “variable” because Fuentes (2002) found that pair bonding behaviors in this species were inconsistent between populations.

2.1.3 Duet Vocalizations

The third character traced in this thesis is duetting (Table 2.3), which Mendez-

Cardenas and Zimmermann (2009: 523) define as “an interactively organized pair display in which one pair partner coordinates its vocalizations in time with those of the other.”

Duetting was included in this thesis because it is common in large monogamous primates

(van Schaik and Dunbar, 1990) and has been interpreted as a mechanism to strengthen pair-bonds in some species (Fuentes, 1999; Fan et al., 2009). For example, Mendez-

Cardinas and Zimmerman (2009) concluded that duetting serves a pair-bonding function in Lepilemur edwardsi (Milne-Edwards’ sportive lemur) because pairs use duets to synchronize locomotion, pair partners participate equally in duetting, and there was no difference in which pair member started or terminated a duet sequence. van Schaik and

Dunbar (1990) added that in “facultative” monogamy (originating from widely dispersed female ranges), territoriality is often associated with duetting as a form of joint advertisement. For coding of duetting, see Table 2.3 below.

Table 2.3: Coding the Category: “Duet Vocalizations”

Duets Description Citation Absent from literature or 1. Absent none Norconk pers. comm. Fuentes, 2002; Haimoff, 1986; Listed in a review article 2. Present Mendez-Cardenas on primate duetting and Zimmermann, 2009 30

2.1.4 Paternal Care

This project explores the history of paternal care of infants (Table 2.4) because the need for paternal investment in offspring has been interpreted as an incentive for the evolution of monogamy (e.g. Kleiman, 1977; Rutberg, 1982). Further, Fuentes (1999) referred to paternal care as part of the “monogamy package.” Paternal care can take many different forms, including infant guarding, warming, food sharing, grooming, and carrying (Wright, 1990; Fernandez-Duque et al., 2009). Different levels of male parental investment are also present in different species, which led van Schaik and Dunbar (1990) and van Schaik and Kappeler (2003) to define “direct” male parental care as activities targeted directly at the infant such as carrying and provisioning.

Table 2.4: Coding the Category: “Paternal Care”

Paternal care Description Citation 1. Absent No mention in literature none Wright, 1990; protection, warming, 2. Indirect Fernandez-Duque playing, grooming et al., 2009 Carry infants and/or provision them with Komers and 3. Direct food, or described as Brotherton, 1997 “extensive” in the literature

Often the term “extensive” paternal care was used in the literature, which I coded as 3): direct. The data cells for Allocebus trichotis (hairy-eared dwarf lemur) and Callithrix aurita (white-eared marmoset) are blank because information on male parental care in these species is not present in the literature.

2.1.5 Territorial Exclusivity

The fifth character explored here is territorial exclusivity (Table 2.5), or defense of the entire group range (Fuentes, 1999). The inclusion of this trait was inspired by models of the evolution of monogamy in which wide spread, exclusive female territories prevented males from monopolizing more than one mate (reviewed in Fuentes, 2002, and

Reichard, 2003). Fuentes (1999) also considers exclusive territoriality to be part of the monogamy package because cooperative defense of an exclusive territory is present in most monogamous species, and Komers and Brotherton (1997) supported this hypothesis using phylogenetic reconstruction.

Table 2.5: Coding the Category: “Territorial Exclusivity”

Degree of overlap Description Citation Range overlap under 25%, 1. Minimal literature description, or none literature diagram Range overlap over 25%, 2. Extensive literature description, or none literature diagram

Territorial exclusivity here refers to the percentage of range overlap between two or more groups, which I coded as 1) minimal, and 2) extensive. Because in most cases a

specific percentage of range overlap was not available, I utilized descriptions from field studies and review articles, which often use phrases like “extensive home range overlap”

(e.g. Microcebus rufus [brown mouse lemur]: Atsalis, 2008). In instances where a percentage was available, I considered an overlap under 25% to be “minimal.” Another source of information was diagrams of home range overlap from field studies, from which it was sometimes necessary to make a subjective decision. 32

2.1.6 Mechanisms of Territorial Defense

Because exclusive territories must be maintained through some form of defensive behaviors, calling and scent marking are the territorial mechanisms traced in this reconstruction.. I chose these two traits because my research revealed that territorial species nearly always use vocalizations, olfactory cues, or both in range maintenance

(Table 2.6).

Table 2.6: Coding the Category: “Mechanisms of Territorial Defense”

Mechanism Description Citation 1. Absent No mention in literature none Wright, 1990; Long calls, territorial 2. Calls Fernandez-Duque et vocalizations al., 2009 Placement of olfactory cues near territorial borders or Komers and 3. Scent marking literature description such as Brotherton, 1997 “territorial scent marking”

The category “calls” includes long calls and any territorial vocalizations, such as

whistling (Cheirogaleus major [greater dwarf lemur]: Rowe, 1996) and long call

choruses (Alouatta seniculus [red howler monkey]: Crocket and Eisenberg 1987). Scent

marking behaviors include marking with feces (Cheirogaleus major: Rowe, 1996), urine

(Aotus nigriceps [black-headed owl monkey]: Rowe, 1996), and scent glands (Tarsius

bancanus [Horsfield’s tarsier]: Niemitz, 1979) at range borders. If data were unavailable

on the placement of scent marks, descriptions such as “territorial scent marking” (e.g.

Propithecus diadema edwardsi [Milne-Edwards’ sifaka]: Pochron et al., 2005) were

coded as 3). Scent marking behaviors in primates with minimum range overlap were

assumed to have a territorial component unless the literature states that a territorial 33

function had not been found for scent marking behaviors (e.g. Leontopithecus rosalia

[golden lion tamarin]: Heymann, 2006; Norconk pers. comm.).

2.1.7 Sexual Dimorphism in Body Mass

Sexual dimorphism in body mass, or the difference in mean body mass of males and females of a species, is the last trait and was included because a lack of sexual dimorphism is correlated with monogamy (Short, 1994; Fuentes, 1999). Kappeler (1990) wrote that sexual size dimorphism in primates has usually been interpreted as the result of sexual selection, which is considered to be strongest in species with the most male-male competition (reviewed in Gaulin and Sailor, 1983; Plavcan, 2001). Therefore, monogamous species with little male intrasexual competition are expected to be sexually monomorphic (Short, 1994; Plavcan, 2001).

Although dimorphism can occur in a number of other traits, here dimorphism is measured in body mass because while body size has been demonstrated to correlate with monogamy, canine size has not (Plavcan, 2001). Further, mass is a reliable measure of body size and is widely available in the literature (Kappeler, 1990; Smith and Jungers,

1997). Body mass was entered into the phylogenetic mapping program Mesquite

(Maddison and Maddison, 2010) in continuous data form, so no coding was necessary.

However, my sources provided both means and ranges of male and female body mass, which required different treatment to find the percentage of sexual dimorphism. For example, when using ranges, I calculated the mean weight for males and females respectively then divided female mass by male mass. If means were presented with standard deviations, I calculated dimorphism without the deviations by dividing the 34

female mean by the male mean. Female mass is shown as a percentage of male mass in order to emphasize female weight in relation to male weight. In this thesis, there is no cutoff percentage for what is considered “dimorphic” or not; rather, dimorphism in each species or clade is presented in comparison to other species or clades, so that dimorphism is always relative.

2.2 Species used in the analysis

The first clade studied here, Lemuroidea (Table 2.7), is an ideal group in which to trace the evolution of monogamous traits because the majority of lemurs have either a solitary or a pair-living social organization (Kappeler and Heymann, 1996). According to

Overdorff and Tecot (2006), Madagascar contains a higher proportion of pair-bonded species than both New and Old World anthropoid taxa. Malagasy strepsirhines are also unique because of their 45 million year-old isolation on the island (Purvis, 1995).

According to Kappeler (1997), Lemuriformes have a variable social organization, life history, and ecological adaptations unseen elsewhere in the Primate order.

Tarsiers are another interesting group in which to study the evolution of monogamy, both because of the clade's early emergence in the Eocene (Gunnell and

Rose, 2002) and its variety of social systems, including solitary, pair-living, polygynous, and multi-male groups (Rowe, 1996; Merker et al., 2005; Gursky, 2011). Further, Tarsius spectrum (the spectral tarsier) and T. dianae (Dian’s tarsier) perform male-female duets, a behavior that is rare in primates and may support an emotional pair-bond (Geissmann and

Orgeldinger, 2000; Fan et al., 2009). 35

Within the platyrrhines, the cebids exhibit an especially diverse array of social system variation, particularly within Callitrichinae (Goldizen, 1990; Peres, 1997).

Callitrichines have a combination of several features, such as twinning, female reproductive suppression, and frequent polyandry, which make them unique from all other primates (Kinzey, 1989). Twinning could possibly be the result of a combination of dwarfism and selective pressure for high reproductive output due to predation (Goldizen,

1990). Callitrichines are also known for their variable mating patterns, which include monogamy, cooperative polyandry, polygyny, and polygynandry, not only between species but also within individual populations (Goldizen, 1990). According to a phylogenetic reconstruction by van Schaik and Kappeler (2003) that traces the evolution of pair living on a primate taxonomy, the cebid genera Pithecia (saki monkeys),

Callicebus (titi monkeys), and Aotus are all variably or uniformly pair living. Finally, the antiquity of Platyrrhini, as a clade that has been confined to the new world for about 40 million years (Purvis 1995), has resulted in a highly diverse group of primates that includes species unique among all living primates (Fleagle, 1999).

Table 2.7: Primate Taxonomy Used in This Study

Suborder Infraorder Superfamily Family Subfamily Genus

Daubentoniidae Daubentonia

Cheirogaleus Cheirogaleidae Microcebus Indri Strepsirhini Lemuriformes Lemuroidea Indriidae Propithecus Avahi Lemur Eulemur Lemuridae Hapalemur Varecia Lepilemur Megalapidae Phaner* Tarsiiformes Tarsioidea Tardiidae Tarsius Callithrix Callimico Callitrichinae Leontopithecus Cebidae Saguinus Cebinae Cebus Saimiri Haplorhini Platyrrhini Ceboidea Aotinae* Aotus Alouatta Atelinae Ateles Callicebus Atelidae Cacajao Pitheciinae Chiropotes Pithecia * Phaner is part of Megalapidae based on Roos et al. (2004). **Aotinae is part of Cebidae based on Goodman et al. (1998: Figure 1)

2.3 Sources of data

Qualitative data were gathered from primary and secondary literature with an emphasis on reviews. Reviews were ideal for my purpose because they synthesize data from several studies, producing new data that more accurately describes a species as a 37

whole. Information from captive primates was only included if no wild studies were available due to the possibility of abnormal behaviors in captive animals (Trollope,

1977).

2.4 Phylogenetic Reconstruction

The phylogenetic reconstruction was performed in Mesquite version 2.74, a modular software designed to help evolutionary biologists analyze comparative data

(Maddison and Maddison, 2010). Since Mesquite is downloadable to any personal computer free of cost (Maddison and Maddison, 2000), I chose to use it instead of

MacClade or other phylogenetic analysis software. The advantage of Mesquite over other programs is its modular form, which allows for considerable flexibility in the analyses that can be constructed by individual researchers. MacClade includes some analyses and tree printing options not available in Mesquite (Maddison and Maddison, 2000), but this thesis did not require further abilities other than a simple ancestral states reconstruction.

Although the Mesquite modules allow reconstructions using parsimony, Bayesian, and likelihood methods, only parsimony was an available method for my data and number of trees. Specifically, Bayesian methods utilize a number of trees, while my project only has one. Also, Maximum Likelihood methods use branch lengths (Glor, 2008; Maddison and

Maddison, 2010), which were not available because I constructed the tree by hand.

In the Ancestral State Reconstruction module, two separate projects were created, the first for discrete characters (the first six traits) and the second for continuous characters (sexual dimorphism). For the discrete characters project, I transformed my qualitative data into quantitative data with scores ranging from 1 to 7 (see Tables 2.1 to 38

2.7), and input these into a character matrix that I had previously filled in with species names and character names. In the continuous characters project I input two-digit numbers that should be read as percentages: for example, 93.5 means the sexual dimorphism of that species or clade is 93.5%. I selected the ‘Color Matrix Cells’ by

‘Character State’ option from the ‘Matrix’ menu to visualize the data categories. To perform the reconstruction, I selected ‘Trace Character History’ from the ‘Analysis’ menu under the ‘Tree Window’ tab. I used parsimony as a reconstruction model instead of maximum likelihood because the latter was unavailable for my data. The model used was Squared Parsimony, which presents a reconstruction that minimizes the total change of the feature in question by reducing the squared distance between the numerical values of the traits [(x-y)2] as much as possible (Maddison and Maddison, 2010).

Before mapping the seven traits onto a phylogenetic tree in Mesquite, I generated

the tree by hand through a number of steps (Figure 2.1). I first generated a generic,

alphabetically-organized phylogenetic tree by selecting New Tree Window: With “Tree

to Edit by Hand” from the Taxa and Trees menu in the Character Matrix tab. To create an

informative tree, I modified it by dragging branches to accord with several published

phylogenies. The structure of Strepsirhini (Table 2.7) is generally based on Roos et al.

(2004) and van Schaik and Kappeler (2003), while Haplorhini is based on Goodman et al.

(1998). Specifically, the position of Indriidae and Lemuridae as sister clades is based on

van Schaik and Kappeler (2003) and Roos et al. (2004). Roos et al. (2004) includes a

polytomy of Indriidae/Lemuridae, Megalapidae, and Cheirogaleidae that I did not find

useful because the polytomy represents unresolved evolutionary relationships (Roos et 39

al., 2004; Chang and Eulenstein, 2006), so I moved Megalapidae to be more ancestral than Cheirogaleidae, which in turn is more ancestral than the sister clades Indriidae and

Lemuridae in a nested format. This positioning is derived from van Schaik and Kappeler

(2003), but the placement of Phaner (the fork-marked lemur) as a sister genus to

Lepilemur is from Roos et al. (2004), whose phylogeny is based on genetic data.

The positions of Daubentonia (the aye-aye) and Tarsius (tarsiers) are derived from van Schaik and Kappeler (2003), while the relatedness of species within Tarsius is from Shekelle et al. (2008). Eulemur (true lemur) species are interrelated based on Wyner et al. (2000). In Haplorhini, the relationships between clades are identical to those in

Goodman et al. (1998: Figure 1) (consensus of four maximum parsimony trees for 45 ε- globin gene sequences), but the species differ in some cases. For example, the relationships between the Aotus (owl monkey) species included in this thesis are based on those in Menezes et al. (2010).

Figure 2.1: Primate Phylogeny of Species Used in This Study

Cebidae

Atelidae

Tarsiidae

Daubentoniidae Megalapidae

Cheirogaleidae

Indriidae

Lemuridae

CHAPTER 3

RESULTS

3.1 Social Organization

In reading the trees with painted branches produced by Mesquite, I interpret a lineage with multiple colors (multiple character states) as having any one or a combination of these states. For example, the social organization reconstruction (Figure

3.1) shows that the most recent common ancestor (MRCA) of the three superfamilies studied in this thesis, Ceboidea, Tarsioidea, and Lemuroidea, could have had several social organizations: solitary, dispersed pairs, associated pars, and/or multi-male. I interpret the results to mean that any one of these social organizations, or a combination of them, could have been the social organization(s) of the most recent common ancestor.

The ancestral organization of Lemuroidea is the same as the common ancestor of all three superfamilies: solitary, dispersed pairs, associated pars, and/or multi-male.

Within the superfamily Lemuroidea, the family Daubentoniidae is shown as ancestrally solitary, while the MRCA of Cheirogaleidae could have lived in dispersed pairs, associated pairs, and/or multi-male groups. Also within Lemuroidea, the common ancestor of Megalapidae lived in dispersed pairs, while Indriidae and Lemuridae each

evolved from an associated pair-living ancestor.

Solitary, associated pairs, and/or multi-male social organizations appear to have

been present in the shared ancestor of Cebidae and Tarsiidae. These three organizations 41

were also ancestral to just Tarsiidae, but only associated pairs and/or multi-male groups were present in the lineage leading to Platyrrhini. The ancestors of the two families within Platyrrhini, Atelidae and Cebidae, both lived in multi-male groups and/or associated pairs. Within Atelidae, Atelinae evolved from a multi-male grouping ancestor, and Pitheciinae had an ancestor that lived in multi-male groups and/or associated pairs.

Within Cebidae, the ancestor of Callitrichinae lived in associated pair, intersexual dyads, and/or multi-male groups. Here, the term ‘intersexual dyads’ refers to pair-bonding behaviors and/or monogamous mating within multi-male groups of marmosets and tamarins. The ancestral Cebine lived in only multi-male groups.

Each type of social organization followed a different evolutionary path..

Solitariness is ancestral to the three superfamilies but was lost in the lineage leading to

Ceboidea. In the lemurs, solitary living was lost at the base of Indriidae-Lemuridae.

Dispersed pair-living follows the same pattern of evolution. Associated pair-living, on the other hand, was continually present from the base of the tree to the tip in several places

(e.g. Aotus [owl monkeys], Callicebus [titi monkeys], and Indriidae-Lemuridae).

Intersexual dyads evolved several times independently, most notably in the shared ancestor of Aotus and the callitrichines. One-male groups and polyandrous groups evolved only in tip taxa, while multi-male groups, like associated pairs, were continually present from base to tip over much of the tree.

An interesting lineage-specific evolutionary history of social organization can be seen in the path leading to the sister genera Leontopithecus and Saguinus. Here, the social organizations of the ancestor at each node, leading from the MRCA of the three 43

superfamilies to the four tip taxa (L. chrysomelas golden-headed lion tamarin]), L. rosalia

[golden lion tamarin], S. fuscicolis [saddle-back tamarin] , and S. oedipus [cotton-top tamarin]), can be listed as follows: 1) solitary, dispersed pairs, associated pairs, and/or multi-male, 2) solitary, associated pairs, and/or multi-male, 3) associated pairs and/or multi-male, 4) associated pairs and/or multi-male, 5) associated pairs, multi-male, and/or intersexual dyads, 6) multi-male and/or intersexual dyads, 7) multi-male and/or intersexual dyads, and 8) multi-male and/or intersexual dyads. Only in individual tip taxa did polyandrous and 1-male groups appear, while associated pairs re-evolved once, in L. chrysomelas (the golden headed lion tamarin).

Figure 3.1: Reconstruction of Social Organization

1 = Solitary 2 = Dispersed pairs

3 = Associated pairs 4 = Intersexual dyads

5 = 1-male 6 = Polyandry

7 = Multi-male

3.2 Pair-Bond

According to the reconstruction (Figure 3.2), it appears that the MRCA of

Ceboidea, Tarsioidea, and Lemuroidea did not display pair-bonding behaviors. The base of Lemuroidea did not pair-bond, but absence of bonding, presence of bonding, and/or variable bonding could have been present where Megalapidae split off from the lineage leading to Cheirogaleidae, Indriidae, and Lemuridae. Variable bonding is defined in this thesis as situations in which 1) some studies have reported bonds and others have not, or

2) some groups appear to have bonded pairs and others do not.

In Platyrrhini, pair bonding evolved three times (in the ancestors of Aotinae-

Callitrichinae, Callicebus [titi monkeys], and Pithecia [saki monkeys]) in either variable or present form. In tarsiers, variable bonds evolved in T. syrichta (the Philippine tarsier) while bonding in its full form evolved in T. spectrum (the spectral tarsier). To summarize the evolution of pair-bonding, bonds and variable bonds each evolved five times independently. Present and variable pair-bonding evolved together at the shared ancestor of Aotinae and Callitrichinae, as well as at the common ancestor of Cheirogaleidae,

Indriidae, and Lemuridae.

Fig. 3.2 Reconstruction of Pair-Bonding

1 = Absent 2 = Present 3 = Variable

3.3 Duet Vocalizations

Duetting is only ancestral to one genus, Callicebus (titi monkeys), and is present in the tip taxa Tarsius spectrum (spectral tarsier), Lepilemur edwardsi (Milne-Edwards’ sportive lemur), Indri indri (indri), and Hapalemur aureus (golden bamboo lemur)

(Figure 3.3). Hence, duet vocalizations evolved once in platyrrhines, once in tarsiers, and in three lineages of lemurs.

Figure 3.3 Reconstruction of Duet Vocalizations

1 = Absent 2 = Present

3.4 Paternal Care

According to the Figure 3.4, the MRCA of Ceboidea, Tarsioidea, and Lemuroidea did not provide paternal care for infants. In lemurs, indirect and direct (e.g. carrying and provisioning) male parental care evolved together when Indriidae-Lemuridae split from

Cheirogaleidae. Direct care was then lost three times within Indriidae and Lemuridae and re-evolved once, in Eulemur rubriventer (the red-bellied lemur). Indirect care (e.g. grooming, warming, guarding, and playing) evolved independently twice in lemurs: in

Cheirogaleus medius (the fat-tailed dwarf lemur) and in the common ancestor of

Indriidae and Lemuridae. In tarsiers, indirect care evolved once, in Tarsius spectrum (the spectral tarsier). In platyrrhines, direct paternal care evolved three times: in the common ancestor of Aotinae and Callitrichinae, in Callicebus, and in and Pithecia pithecia (the white-faced saki). Also in platyrrhines, indirect care evolved five times in every subfamily except Cebinae, so therefore some form of male parental care is present in all but one platyrrhine subfamily.

Figure 3.4 Reconstruction of Paternal Care

1 = Absent 2 = Indirect 3 = Direct

3.5 Territorial exclusivity

The lineage leading to Ceboidea, Tarsioidea, and Lemuroidea appears to have lived in relatively exclusive territories (Figure 3.5). In fact, this type of territoriality is pervasive in all three featured superfamilies and is only broken nine times. For example, the only lemurs that live in extensively overlapping ranges are Daubentonia madagascariensis (the aye-aye), Lepilemur ruficaudatus (the red-tailed sportive lemur),

Microcebus spp. (mouse lemurs), Avahi occidentalis (the western woolly lemur), and

Eulemur spp. (true lemurs). Tarsius syrichta is the only tarsier species analyzed in this thesis to live in extensively overlapping ranges, and similarly the majority of platyrrhines have exclusive territories. Only species of the genera Callithrix, Saimiri, Cebus,

Chiropotes, and Cacajao do not maintain relatively discrete ranges. While in five cases extensive range overlap was ancestral to poly-specific groups, in the other four events extensive overlap evolved in individual extant species.

Figure 3.5 Reconstruction of Territorial Exclusivity

1 = Minimum

2 = Extensive

3.6 Mechanisms of Territorial Defense

According to the reconstruction, it seems that although many extant species both scent-mark and call to defend their territories, calling is the basal mechanism of defense for Ceboidea, Tarsioidea, and Lemuroidea (Figure 3.6. Territorial vocalizations are found at the base of Lemuroidea, but defensive mechanisms involving olfactory cues evolved independently 11 times in this superfamily. Only two of the lemur species analyzed in this project do not defend territories from other groups, and a lack of defense is not ancestral to any lemur clades. All tarsiers defend territories, but all three species independently evolved scent-marking defense behaviors while maintaining an ancestral state of territorial calling.

In Ceboidea, a lack of territorial defense behaviors is ancestral to two clades: the subfamily Cebinae and the sister genera Cacajao and Chiropotes. Scent marking to defend territories evolved independently 15 times in New World monkeys, while the primitive trait of territorial vocalizations was retained throughout most of the ceboid superfamily. In total, scent marking for defense seems to have been lost and subsequently re-evolved an amazing 28 times across the whole tree, which is especially surprising given the use of parsimony as the method of reconstruction. Most of these 28 evolutionary events occurred in tip taxa, but scent marking is ancestral to the genera

Cheirogaleus (dwarf lemurs) and Propithecus (sifakas) as well as two pairs of sister species, Eulemur rubriventer-E. fulvus rufus (red-bellied lemur and red-fronted lemurs) and Callithrix jacchus-C. geoffroyi (common marmosets and Geoffroy’s marmosets). An 54

absence of any territorial defense mechanisms evolved only four times, in the ancestors of Cebinae, Chiropotes-Cacajao, Phaner furcifer, and Avahi laniger.

Figure 3.6 Reconstruction of Mechanisms of Territorial Defense

1 = Absent 2 = Calling 3 = Scent marking

3.7 Sexual Dimorphism

A lack a significant sexual body mass dimorphism seems to be ancestral to the superfamilies studied in this thesis: specifically, the MRCA degree of dimorphism was

92%. The ancestral lemur was more monomorphic, at 95% (Figure 3.8), while the ancestral platyrrhine was less so, exhibiting dimorphism of 88% (Figure 3.7). Tarsiers evolved from a very similarly dimorphic ancestor with a dimorphism of 89% (Figure

3.9). Within Platyrrhini, dimorphism increased at the base of Cebidae to 88%, while within Cebinae and Callitrichinae dimorphism steadily decreased at each node (Figures

3.7 and 3.10).

Specifically, in Aotinae dimorphism decreased from 93.00% at the ancestor shared with Callitrichinae to 95.89% at the base of the genus. In Callitrichinae, dimorphism decreased from 95.75% at the base of the radiation to 97.01% at the MRCA of Saguinus and Leontopithecus and 96.60% at the base of Callimico-Callithrix. Negative dimorphism, in which females are larger than males (Ford, 1994), occurred for the first time in the ancestors of both Saguinus and the sister species Callithrix geofroyii and C. jacchus. Dimorphism in Cebinae increased from 81.66% at the shared ancestor of Cebus and Saimiri to 81.22% at the ancestral squirrel monkey and 76.22% at the basal capuchin

(Figure 3.10). The ancestral tarsier is inferred to have had an 88.02% degree of dimorphism (Figure 3.9), while lemurs generally evolved fewer intersexual body mass differences over time to culminate in an extremely high degree of negative dimorphism

(i.e., females larger than males), 126%, in Cheirogaleus major. The common ancestor of

Daubentonia and the other lemurs was slightly dimorphic at 95.11%, but the ancestors of 57

Lemuridae, Phaner-Lepilemur, Cheirogaleidae, and Indriidae are reconstructed at

99.53%, 103.15%, 103.49%, and 105.27% respectively (Figure 3.8).

Figure 3.7 Reconstruction of Sexual Dimorphism in Lemuroidea, Tarsioidea, and

Ceboidea

Figure 3.8 Reconstruction of Sexual Dimorphism in Lemuroidea

Fig. 3.9 Reconstruction of Sexual Body Mass Dimorphism in Tarsioidea

Fig. 3.10 Reconstruction of Sexual Body Mass Dimorphism in Cebidae

Fig. 3.11 Reconstruction of Sexual Body Mass Dimorphism in Atelidae

3.8 Multi-trait Comparisons

On the basis of this study, pair living, territorial exclusivity, and territorial defense via vocalizations were present in the MRCA of Ceboidea, Lemuroidea, and Tarsioidea

(Figure 3.12). Subsequently, in the platyrrhines paternal care and pair-bonding evolved simultaneously three times, while in Lemuroidea paternal care evolved before bonding, which later evolved four times independently. In tarsiers, paternal care and bonding behaviors evolved together in Tarsius spectrum, while the other two tarsier species included in this analysis are not pair-living (Figure 3.12). Together, these patterns indicate that pair-living and minimum territorial overlap are the ancestral characters of monogamous species, while paternal care, pair-bonding, and duetting and derived traits.

From Figure 3.12 and the dimorphism figures (3.7 through 3.11) the reader can also discern the evolutionary patterns of monogamy in specific lineages. For example, in

Aotus (owl monkeys) the first monogamous traits to evolve (in the common ancestor of the three superfamilies) were cohesive pair-living and relatively exclusive territories, which were maintained via vocalizations. Later in the evolution of this lineage, pair- bonding and paternal care evolved together. Further, dimorphism decreased twice after the split from Cebinae so that the lineage became increasingly monomorphic in body mass (Figure 3.11)

Figure 3.12: Lineage-Specific Evolution of Primate Monogamy

Pair-living

Pair-bonding Duetting

Paternal care Minimal

territorial overlap

Territorial scent-marking Territorial vocalizations

CHAPTER 4

DISCUSSION

4.1 Potential confounding factors

In this thesis, confounding factors could lie with the sources of data and the

coding, either of which could be incorrect or incomplete. This is an especially prominent

source of error because much of the coding is subjective. Also, characters that are readily

influenced by ecology, such as territorial exclusivity, are not necessarily predictable traits

because degree of overlap can change from region to region within the same population

(Cowlishaw and Dunbar, 2000; for an example see Saimiri sciureus (common squirrel

monkey): Rowe, 1996, Boinski et al., 2002). Another source of inaccuracy lies in the

analysis. The composite phylogeny is a conglomeration of information from many studies

which have been condensed in turn by Roos et al. (2004), Goodman et al. (1998), and van

Schaik and Kappeler (2003), and in the end, a phylogenetic reconstruction is only as

accurate as the phylogeny it is based on (Ryan, 1996).

Another potential problem could be the use of parsimony as the model of

inference. Parsimony is based on the principle of Occam's Razor, and thus considers the

tree with the simplest historical explanation for a data set to be the correct one (Barton et

al., 2010). Because parsimony is based on philosophy and not statistics, it should not be

relied on uncritically to provide true patterns of evolution (Ryan, 1996). Encouragingly,

Hills et al. (1992) carried out an experiment on the accuracy of five phylogenetic

techniques in inferring the true evolutionary history of a lineage of bacteriophages, and found that all techniques, including parsimony, accurately predicted ancestral states.

4.2 Discussion of Research Questions

The major findings of Chapter 3 were that monogamy evolved in a mosaic pattern such that pair-living and territorial exclusivity evolved before paternal care, pair-bonding, and duetting. This chapter applies the lineage-specific results from Chapter 3 to a number of hypotheses that have been proposed about the evolution of monogamy. While two sections are applicable to one of the widely accepted theories on the origins of monogamous mating (Kleiman’s 1977 paternal care hypothesis), most of the following hypotheses are simple proposals of evolutionary patterns. The benefit of using so many traits can be seen in this chapter, where studying of three or more evolutionary pathways in combination clarifies some of the details of the evolution of monogamy.

1. “Monogamy has many forms and has evolved in lineage-specific patterns” (Reichard,

2003:5).

In the introduction to the book ‘Monogamy: Mating strategies and partnerships in

birds, humans and other mammals’, Reichard (2003) discussed the social, sexual, and

genetic variation covered by the term ‘monogamy’ and reviewed hypotheses for the

origins of social monogamy. The present results agree with his statement that monogamy

evolved along different pathways in different lineages: for example, in callitrichines and

tarsiers paternal care and bonding evolved at the same time, but in lemurs bonding

evolved before paternal care (see Figure 3.12). In pitheciines, paternal care and bonding

evolved together in two separate evolutionary events (Figure 3.12). This comparison of 67

the temporal appearance of just two traits associated with pair living suggests the great variation in monogamous primates. However, since the three superfamilies studied here shared a territorial pair-living ancestor, monogamy can be described as a complex phenomenon that began with two keystone characters and diversified in different lineages to form the complex whole that is manifested uniquely in each extant clade.

2. “…The two-adult group or pair-bonding or both may have evolved separately 4-7

times” (Fuentes, 2002:953)

Fuentes (2002) reviewed the behavior and ecology of species reported to occur in two-adult or pair-bonded groups (or both), proposed definitions for a social and a sexual pair-bond, and assessed various models for the evolution of primate two-adult groups

(here, “pair living” groups). His list includes 26 species in the genera Eulemur (true lemurs), Hapalemur (bamboo lemurs), Varecia (ruffed lemurs), Cheirogaleus (dwarf lemurs), Phaner (fork-marked lemurs), Avahi (woolly lemurs), Indri (indri), Aotus (owl monkeys), Callicebus (titi monkeys), Presbytis (Mentawai langurs), and Hylobates

(gibbons). From behavioral and ecological data, Fuentes proposes that the two-adult group or pair-bonding or both may have evolved separately four to seven times, and the present results partly support this proposition. For instance, Figures 3.1 and 3.2 show that the two-adult group appears to have evolved once in the ancestor of Ceboidea,

Lemuroidea, and Tarsioidea, but that pair-bonding in one form or another evolved a total of nine times in the species studied here. Specifically, variable bonding evolved independently four times, while uniform bonding evolved five times (Figure 3.2) . 68

Therefore, my results provide a slightly higher estimate than that in Fuentes (2002), but generally support his proposal that pair-bonding evolved several times independently.

3. “It remains […] unknown whether monogamy or a multi-male system is the ancestral

pattern of primate social organisation” (Müller and Thalmann, 2000:425).

In an attempt to clarify the diverse social systems present in so-called solitary prosimians (“prosimians” instead of “strepsirhines” due to the inclusion of tarsiers),

Müller and Thalmann (2000) created a classification system for the social organizations of solitary foragers and hand-reconstructed the prosimian ancestral social organization.

The authors challenged the accepted notion that the primitive prosimian social organization was a “dispersed harem,” and instead suggested that the most probable ancestral organization was “dispersed multi-male” (here: ”multi-male”).

The ancestral strepsirhine (excluding tarsiers) could have had any of four possible social organizations (multi-male, dispersed pairs, associated pairs, and/or solitary) or displayed a combination of these (Figure 3.1). As is apparent by the variety observed in extant primates, one species, one population, and even one group in different years can use varying grouping patterns. Therefore, my thesis does not help clarify Müller and

Thalmann’s (2000)’s statement of uncertainty pertaining to the prosimian ancestral social organization.

4. “The gregarious patterns of social organisation in Aotus and Avahi, and the dispersed

form in Tarsius evolved from the gregarious patterns of diurnal primates rather than

from the dispersed nocturnal type” (Müller and Thalmann, 2000:405). 69

The genus Aotus (owl monkeys) is descended from a lineage living in associated pairs and/or intersexual dyads (multi-male groups with pair-bonding), Avahi (woolly lemurs) evolved from a cohesive pair-living ancestor, and the ancestral Tarsius (tarsier) lineage was solitary, lived in associated pairs, and/or had a multi-male society (Figure 3.1).

Therefore, my results support the conclusions made by Müller and Thalmann (2000).

5. Twinning either evolved at the same time or after pair-bonding, when the resulting

consistent male presence allowed the evolution of high levels of male parental care

for offspring (Dunbar, 1995).

Dunbar (1995) writes that the traditional view of the relationship between monogamy and twinning is that the former evolved to allow the latter: once twinning had become a fixed trait, females enacted strategies such as widespread dispersal and cryptic ovulation to prevent males from realizing a roving strategy, and this eventually resulted in strong bonds between the monogamously reproducing pair. In his 1995 paper, Dunbar provides an alternate explanation: that bonding allowed the evolution of twinning because of a consistent male presence.

My analysis demonstrated the co-evolution of male care and bonding in

Callitrichinae (Figure 3.12), and there is also a general trend of decreasing sexual dimorphism (increasing monomorphism) in body mass in this subfamily (Figure 3.10).

Together, these results agree with Dunbar’s model that twinning evolved in a bonded species which provided constant male presence because my results of a steady decrease in dimorphism can be interpreted as natural selection increasing female body size due to 70

the energetic demands of their high rate of reproduction, while males retained the species’ ancestral mass.

6. The evolution of extant callitrichine social systems might have followed a temporal

pattern of 1) single births and unknown social system, 2) obligate monogamy, 3)

extensive paternal care, 4) twinning and helping by older offspring, and 5) facultative

polyandry (Goldizen, 1990).

Goldizen (1990) proposes a continuum for the evolution of monogamy which includes the above additive stages, and then places various clades along this pathway.

She postulates that the ancestor of modern callitrichines gave birth to singletons, mated monogamously, and had significant male parental care for offspring. Twinning might have then been favored partly because the extensive paternal care allowed the groups to raise twins successfully, but the remaining high costs of twinning and the presence of groups without older offspring to be helpers led to a mating system of facultative polyandry in some species. Polyandry is an unexpected mating system because males generally have potentially higher reproductive rates than females, so two males competing for mating access to a single female would potentially constrain their individual reproductive success (Huck et al., 2005). Goldizen’s (1990) model provides an explanation for how and why this odd mating system might have evolved in marmosets and tamarins.

The results of this thesis do not provide information on mating systems or birthing patterns, but the dimorphism data in Figure 3.10 supports the hypothesis proposed by both Goldizen (1990) and Dunbar (1995, see discussion above), that paternal care might 71

have allowed the evolution of twinning. Further, Figure 3.2 shows that the social system of polyandry evolved three times independently in tip species, which supports Goldizen’s model that facultative polyandry evolved in some species under certain circumstances

(although loosely due to her use of the term polyandry as a mating system).

7. “The associated evolution of [monogamy and paternal care appears to have] occurred

by chance” (Komers and Brotherton, 1997:1266).

Komers and Brotherton (1997) performed the first phylogenetic reconstruction of sexual monogamy in mammals to test the hypothesis that the mating system evolved in response to a need for paternal care (Kleiman, 1977). They found that monogamy evolved significantly more often in the absence of paternal care than in its presence, and that a stronger correlation exists between small, discrete female ranges and monogamy.

Komers and Brotherton also concluded that monogamy preceded paternal care 1-3 times, a finding that does not support models that propose monogamy resulted from the need for paternal care. According to the authors, the associated evolution of monogamy and paternal care occurred by chance.

Figure 3.12 shows that the form of monogamy studied in this thesis, pair-living, evolved well before paternal care in the three superfamilies studied here. In Cebidae, paternal care is instead correlated with pair bonding, but bonding itself is not the same as social monogamy. In lemurs, the evolution of paternal care at the MRCA of

Cheirogaleidae and Indriidae-Lemuridae (Figure 3.4) seems to be random, as pair-living was present earlier in evolutionary time and pair-bonding did not evolve until later. As for the number of times monogamy preceded paternal care, according to my 72

reconstruction pair living evolved before paternal care at the most recent common ancestor of all lineages (once), which agrees with Komers and Brotherton’s (1997) result that monogamy preceded paternal care 1-3 times.

Overall these patterns seem to agree with Komers and Brotherton’s (1997) conclusion that the association of monogamy and paternal care occurred by chance in primate evolution, although in this thesis monogamy is defined as a social and not a mating system. The term ‘monogamy’ in Komers and Brotherton (1997) means “a social bond implying mating exclusivity,” while here pair-bonds and pair living are two separate categories. Because of this difference in terms, my results must be compared cautiously with those in the Komers and Brotherton paper.

8. Male long calls may have evolved to attract females by defending resources important

to them (Wich and Nunn 2002).

Wich and Nunn (2002) performed a phylogenetic reconstruction of male long calls and tested two questions: 1) if they function in territorial spacing for mate defense, and 2) if they function to attract females by defending necessary resources. My finding that calling is the ancestral territorial mechanism of the MRCA of Ceboidea, Lemuroidea, and Tarsioidea agrees with Wich and Nunn’s (2002) result that male long-distance calls are the ancestral state of 158 primate species from both Strepsirhini and Haplorhini. None of their tests supported the hypothesis that male long calls function in mate defense, while some tests gave credence to the mate attraction and resource defense hypothesis.

Because resource defense is theoretically expected in polygynous or monogamous societies, and the reconstruction in Figure 3.1 shows that pair-living was present in the 73

ancestor of Ceboidea, Lemuroidea, and Tarsioidea, my findings agree with Wich and

Nunn’s tests that support the resource defense hypothesis. However, my thesis and the article use different species in the reconstructions, and so cannot be directly compared.

9. What was the social organization of the common ancestor of Ceboidea, Tarsioidea,

and Lemuroidea?

Combining my findings with those of other researchers can provide a more complete picture of the earliest primates. For example, Kappeler and Heymann (1996) reconstructed the activity period of the earliest primate as nocturnal, and this information combined with the results in Chapter 3 of this project create the image of a solitary, pair living, or multi-male primate species (Figure 3.1) that was nocturnal, defended its territory with vocalizations (Figure 3.6) , was not sexually dimorphic (Figure 3.7), and in which males did not care for their offspring (Figure 3.5).

10. Did pair-bonding mechanisms or paternal care evolve first in 'obligate'

monogamy? (Kleiman 1977).

One of the goals of this thesis was to test Kleiman’s proposed obligate/facultative dichotomy, and several primate clades or species in the reconstruction avail themselves to this task. For example, although Cheirogaleus medius (the fat-tailed dwarf lemur) can be considered “obligately” monogamous because of the necessity of male warming and guarding for infant survival (Fietz 1999), bonding appears to have preceded the evolution of paternal investment in infants (Figure 3.12). This is the opposite order expected of monogamy that evolved due to the need for male parental care. The callitrichines and 74

Aotinae do conform to Kleiman’s obligate monogamy category, as here bonding and paternal care evolved together at the common ancestor of the two groups (Figure 3.12).

Pitheciinae and Tarsius spectrum (the spectral tarsier) also conform to the expectations of obligate monogamy, while the lemurs, in which bonding appears before paternal care (Figure 3.12), do not. Kleiman (1977) further writes that in “facultatively” monogamous primates, one would expect neither a strong pair-bond nor extensive paternal care, and this pattern is seen in many species, including Allocebus trichotis

(hairy-eared dwarf lemur) and Microcebus murinus (brown mouse lemur), lemur sister species that frequently live in dispersed pairs but display neither bonds nor paternal investment in young (Figures 3.1, 3.2, and 3.4). Phaner furcifer (fork-marked lemur),

Propithecus edwardsi and P. verreauxi (Milne-Edwards’ and Verreaux’s sifakas),

Lepilemur ruficaudatus and L. edwardsi (red-tailed and Milne-Edwards’ sportive lemurs), and Tarsius bancanus (Philippine tarsier) are other species that live in pairs but do not display behaviors indicative of an emotional bond (Figures 3.1 and 3.2). Also,

Propithecus edwardsi is the only primate in this list to display any paternal care, and in this species the care takes an indirect form.

11. Given the selection of taxa in this thesis, when was the first appearance of

duetting and what were its evolutionary correlates?

Duetting is a form of calling that has been suggested as a form of mate defense, resource defense, a pair-bond reinforcing mechanism, and a method of maintaining group cohesion (Fan et al. 2009). The reconstructions indicate that duetting evolved concurrently with bonding at the ancestor of Callicebus (titi monkeys), in Tarsius 75

spectrum (the spectral tarsier) it evolved at the same time as bonding and paternal care, and in Indri indri (the indri) and Hapalemur aureus (the golden bamboo lemur) it evolved well after both paternal care and bonding (Figures 3.2, 3.3, and 3.4). These results seem to indicate that bonding and paternal care are either necessary or instrumental for the evolution of duetting, which in turn supports the proposed pair- bonding function of duetting. The association between male care and duetting might also be incidental, as the reconstruction indicates that bonding might be necessary for both paternal care and duetting.

12. Did monomorphism re-evolve as a result of pair-bonding?

Because of the association of sexual monomorphism and pair living (Fuentes,

1999), I was interested in whether there was a cause and effect relationship between pair- bonding and monomorphism. This appears to be the case in Callitrichinae-Aotinae, where paternal care and bonding evolved together in the common ancestor of these two subfamilies, and then after this co-evolution, dimorphism began to steadily decrease

(Figures 3.9 and 3.12). This took place after dimorphism had been steadily increasing from the base of the phylogeny (92%) to the ancestor of Cebidae (88%).

13. Were pair-bonding behaviors present at the most recent common ancestors of taxa

that demonstrate multiple social organizations, such as Pitheciinae?

It appears that the answer to this question is a partial yes. In pitheciines, bonding evolved once at the base of Callicebus (titi monkeys) and once at the base of Pithecia

(saki monkeys), but was not an ancestral trait to the whole subfamily (Figure 3.2).

Bonding is ancestral to Callitrichinae-Aotinae, although these monkeys have highly 76

varying social organizations including pairs, 1 male groups, and multi-male groups.

Bonding is also ancestral to the common ancestor of the lemur families Cheirogaleidae,

Indriidae, and Lemuridae, despite varying social organizations from solitary to multi- male (Figure 3.2).

CHAPTER 5

CONCLUSIONS

My primary conclusion follows Reichard (2003): in primates, monogamy evolved

in lineage-specific patterns. The basal characters of monogamy are pair-living and the

maintenance of minimally overlapping territories, while other traits associated with

monogamy (pair-bonding, paternal care, duetting, and sexual monomorphism) evolved

later in different lineages at different times. McLennan et al. (1988) wrote that

phylogenetic trees can be used to discover whether traits are due to homology or analogy,

and in the case of monogamy we can see that extant pair-living species demonstrate some

of both. For example, monogamous primates share the homologous traits of pair-living

and minimally overlapping territories, while some have analogous characters such as paternal care that evolved independently. Since the basal characters of monogamy in my reconstruction are explicit territoriality and living in pairs (two-adult groups), I consider these two features to be keystone characters at the heart of the concept of primate monogamy.

I agree with Fuentes (2002) that pair-bonding evolved several times independently, possibly under different selective pressures. However, I disagree with his

(1999) suggestion that the minimum requirements for a species to be considered

‘monogamous’ are that 1) all groups contain one adult male and one adult female only, 2)

the two adults associate longer than one breeding season, 3) the adults pair-bond, and 4) the adults engage in long term sexual fidelity. This is a very strict definition, and accordingly Fuentes considers very few primates to be monogamous. I take a different approach, viewing monogamy as a variable system that is present in many species in different forms. This includes “partial monogamy,” in which only some criteria are met.

The concept of partial monogamy can be better understood by examining the reconstructions presented in this thesis, which reveal when the different aspects of the monogamy package evolved independently. For example, one can see that the fact that the pair-living fork-marked lemur (Phaner furcifer) does not pair bond is not surprising because pair-bonding is not an ancestral state in Megalapidae, the family to which

Phaner belongs.

Phylogenetic reconstruction is a valuable tool for ethologists and primatologists, and here I have demonstrated how the technique can elucidate the complex evolution of a multi-faceted trait like monogamy. Workers have another option in creating models of evolution besides methods of logic (e.g. Dunbar, 1995, on Goldizen, 1990), hand reconstructions (e.g. Müller and Thalmann, 2000), or mathematical payoff matrices

(Dunbar, 1995). The use of phylogenies broadens behavioral scientists’ repertoires and provides a viable method for discerning keystone traits of phenomena such as monogamy.

Phylogenetic reconstruction has its limits, however, because the reconstruction is only as accurate as the phylogeny it is based on. Future researchers should take care to use as robust a phylogeny as possible and as many species as possible to provide the most 79

accurate view of evolution. Avenues of research might include mapping traits shared by humans and other primates, whether genetic, morphological, or behavioral, to discover the origins of the trait. Also, a future reconstruction of the traits used here onto a phylogeny with branch lengths would not only permit a reconstruction of the timeline of this mosaic evolution, but also permit the use of a maximum likelihood model to determine the probability of each character state at each node.

APPENDIX A

Summary Database with Abbreviations

Social Family Na Genus P.B.b Duetc P.C.d T.E.e M.D.f S.D.g org DP1 Allocebus ID2 A8 A A M13 C15 0.91 MM3 DP Cheirogaleus P9 A I11 M C S16 0.91 Cheirogaleidae 5 AP4 S5 DP M C Microcebus A A A 1.03 M6 E14 S MM Daubentoniidae 1 Daubentonia S A A A M C 0.98 DP Avahi P P A M C 1.17 CP 1M M Indri P A I S 1.08 MM E Indriidae 5 DP AP S Propithecus 1M A A I M 1.03 C PA MM S AP A A ID A M S Eulemur P I 0.93 1M P E C V10 D12 PA MF Lemuridae 8 AP P S Hapalemur 1M A I M 1.01 V C MM S Lemur MM A A A M 1.01 C AP S Varecia V A I M 0.97 MM C DP A M Lepilemur ID A A S 1.04 P E Megalapidae 3 1M C Phaner DP A A A M 0.93 S S DP A A M C Tarsiidae 3 Tarsius CP P A 1.06 I E S 1M V MM

1M A M S Alouatta A A 0.98 MM I E C S Ateles MM A A A M 0.74 C Cacajao MM A A M M A 0.76 S Callicebus AP P A E M 0.94 Atelidae 12 C ID M Chiropotes A A A C 1.05 MM E AP ID A Pithecia V A A M M 0.81 1M C MM A S Aotus AP P D M 0.88 P C ID S Callimico 1M V A I M 0.91 C PA ID A A A I M Callithrix 1M P S 0.97 P D E MM V C 1M Cebus A A A E A 0.84 MM Cebidae 15 AP ID S Leontopithecus 1M V A E M 0.9 C PA MM ID 1M M Saguinus V A E C 0.94 PA E MM S Saimiri MM A A A M 1.07 C

Appendix Coding Top row Social organization Other character states a = number of species DP = dispersed pairs 8 = absent b = pair bond ID = intersexual dyads 9 = present c = duet MM = multi-male 10 = variable d = paternal care AP = associated pairs 11 = indirect e = territorial exclusivity S = solitary 12 = direct f = mechanisms of territorial 1M = one male 13 = minimum defense PA = polyandry 14 = extensive g = sexual body mass dimorphism 15 = calls 16 = scent marking

Sources Allocebus: Smith and Jungers, 1997; Nowak, 1999; Fuentes, 2002; Bieouw, 2009; Gould et al., 2011; http://www.theprimata.com/allocebus_trichotis.html Cheirogaleus: Haimoff, 1986; Rowe, 1996; Smith and Jungers, 1997; Fietz, 1999; Muller, 1999; Muller and Thalmann 2000; Fuentes, 2002; Fietz and Dausmann 2003; Lahann, 2008 Microcebus: Haimoff 1986; Smith and Jungers 1997; Fietz 1999; Fuentes 2002; Damnhahn and Kappeler 2005; Eberle and Kappeler 2006; Garbutt 2007; Atsalis 2008 Daubentonia: Kappeler, 1990; Sterling, 1993b; Ancrenaz et al., 1994; Sterling, 1995; Sterling and Richard, 1995; Fuentes, 2002; Fernandez-Duque et al., 2009; Gould et al., 2011 Avahi: Haimoff, 1986; Harcourt and Thornback, 1990; Kappeler, 1990; Wright, 1990; Harcourt, 1991; Komers and Brotherton, 1997; Warren and Crompton, 1997; Fuentes, 1998; Thalmann, 2001; Fuentes, 2002; Schulke et al., 2003; Thalmann, 2006 Indri: Wright, 1990; Smith and Jungers, 1997; Fuentes, 1998; Garbutt, 1999; Fuentes, 2002; van Schaik and Kappeler, 2003; Glessner and Britt, 2005; Gould and Sauther, 2007 Propithecus: Sussman and Richard, 1974; Wright, 1988; Kappeler, 1990; Brockman, 1994; Komers and Brotherton, 1997; Smith and Jungers, 1997; Kappeler, 1999; Muller and Thalmann, 2000; Fuentes, 2002; Pochron and Wright, 2003; van Schaik and Kappeler, 2003; Pochron et al., 2004; Pochron et al., 2005; Bastian and Brockman, 2006; Gould and Sauther, 2007; Benadi et al., 2008; Kappeler et al., 2009; Morelli et al., 2009 Eulemur: Wright, 1990; Overdorff, 1993; Burton, 1995; Overdorff, 1996a; Kappeler, 1997; Smith and Jungers, 1997; Curtis and Zaramody, 1998; Overdorff, 1998; Fuentes, 2002; van Schaik and Kappeler, 2003; Bayart and Simmon, 2005; Overdorff and Tecot, 2007; Gould and Sauther, 2007; Overdorff, 1998; Fernandez-Duque et al., 2009 Hapalemur: Meier et al., 1987; Glander et al., 1989; Wright, 1990; Komers and Brotherton, 1997; Tan, 1998; Fuentes, 2002; Tan, 2006; Gould and Sauther, 2007; Lemur: Kappeler, 1990; Pereira and Kappeler, 1997; Fuentes, 2002; Gould and Overdorff, 2002 Varecia: Pereira et al., 1987; Smith and Jungers, 1997; Fuentes, 2002; Vasey, 2006; Gould and Sauther, 2007 Lepilemur: Smith and Jungers, 1997; Muller and Thalmann, 2000; Fuentes, 2002; Zinner et al. 2003; Thalmann, 2006; Gould and Sauther, 2007; Hilgartner et al., 2007; Mendez- Cardenas and Zimmermann, 2009 Tarsier: Haimoff, 1986; Crompton, 1987; Crompton and Andau, 1987; Rowe, 1996; Fuentes, 2002; Neitsch, 2003; Gursky, 2007; Gursky, 2011 Aotus: Wright, 1985; Wright, 1990; Wright, 1994; Rowe, 1996; Fuentes, 1998; Fuentes, 2002; van Schaik and Kappeler, 2003; Gursky, 2007; Fernandez-Duque et al., 2011 Alouatta: Mack, 1979; Thorington et al., 1979; Sekulic, 1981; Haimoff, 1986; Crocket and Eisenberg, 1987; Rowe, 1996; Smith and Jungers, 1997; Biedzicki de Marques and Ades, 2000; Fuentes, 2002; Hirano et al., 2008 83

Ateles: Mittermeier and van Roosmalen, 1981, Fedigan, 1984; van Roosmalen, 1985; Haimoff, 1986; Symington, 1988; van Roosmalen and Klein, 1988; Rowe, 1996; Smith and Jungers, 1997; Fuentes, 2002; Campbell, 2008; di Fiore et al., 2011 Cacajao: Fontaine, 1981; Ayres and Johns, 1987; Cox et al., 1987; Smith and Jungers, 1997; Fuentes 2002; Deffler 2004; Barnett, 2005 Callicebus: Robinson and Ramirez, 1982; Robinson et al., 1987; Wright, 1990; Rowe, 1996; Komers and Brotherton, 1997; Fuentes, 1999; Fuentes, 2002; van Schaik and Kappeler, 2003 Chiropotes: Robinson et al ., 1987; Rowe, 1996; Fuentes, 1999; Norconk, 2011 Pithecia: Robinson et al., 1987; Fuentes, 1999 ; Norconk, 2011 Callimico: Heltne et al., 1981; Masataka, 1982; Rowe, 1996; Smith and Jungers, 1997; Porter et al., 2005; Porter, 2007 Callithrix: Soini, 1982; Whitten, 1982; Evans and Poole, 1984; Kleiman, 1985; Haimoff, 1986; Harrison and Tardif, 1988; Soini, 1988;Tardif, 1988; Olmos and Martuscelli, 1995; Ferrari et al., 1996; Rowe, 1996; Komers and Brotherton, 1997; Smith and Jungers, 1997; Nowak, 1999; Sussman, 2000; Fuentes, 2002; Snowdon and de la Torre, 2002; van Schaik and Kappeler, 2003; Ferrari, 2009; Yamaguchi et al., 2010; Digby et al., 2011 Cebus: Wright, 1990; Rowe, 1996; Crowfoot, 1997; Fuentes, 2002; Fernandez-Duque et al., 2009 Leontopithecus: Kleiman, 1985; Haimoff, 1986; Peres, 1989; Baker et al., 1993; Epple et al., 1993; Rothe and Darms, 1993; Rowe, 1996; Peres, 2000; Fuentes, 2002; Raboy, 2002; Miller et al., 2003 Saguinus: Epple, 1981; Garber, 1988; Wright, 1990; Garber, 1993; Rowe ,1996, Komers and Brotherton, 1997; French and Schaffner, 1999; Fuentes, 2002; Epple et al., 2003; van Schaik and Kappeler, 2003 Saimiri: Robinson and Janson, 1987; Wright, 1990; Rowe, 1996; Boinski et al., 2002; Fuentes, 2002; Jack, 2011

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