ACCOUNTING FOR INTRASPECIFIC VARIATION TRANSFORMS OUR
UNDERSTANDING OF ARTIODACTYL SOCIAL EVOLUTION
By
Monica Irene Miles
Loren D. Hayes Hope Klug Associate Professor of UC Foundation Associate Professor of Biology, Geology, and Environmental Science Biology, Geology, and Environmental Science (Chair) (Committee Member)
Timothy Gaudin UC Foundation Professor of Biology, Geology, and Environmental Science (Committee Member) ACCOUNTING FOR INTRASPECIFIC VARIATION TRANSFORMS OUR
UNDERSTANDING OF ARTIODACTYL SOCIAL EVOLUTION
By
Monica Irene Miles
A Thesis Submitted to the Faculty of the University of Tennessee at Chattanooga in Partial Fulfillment of the Requirements of the Degree of Master of Science: Environmental Science
The University of Tennessee at Chattanooga Chattanooga, Tennessee
December 2018
ii Copyright © 2018
By Monica Irene Miles
All Rights Reserved
iii ABSTRACT
A major goal in the study of mammalian social systems has been to explain evolutionary transitions in social traits. Recent comparative analyses have used phylogenetic reconstructions to determine the evolution of social traits but have omitted intraspecific variation in social organization (IVSO) and mating systems (IVMS). This study was designed to summarize the extent of IVSO and IVMS in Artiodactyla and Perissodactyla, and determine the ancestral social organization and mating system for Artiodactyla. Some 82% of artiodactyls showed IVSO, whereas 31% exhibited IVMS; 80% of perissodactyls had variable social organization and only one species showed IVMS. The ancestral population of Artiodactyla was predicted to have variable social organization (84%), rather than solitary or group-living. A clear ancestral mating system for Artiodactyla, however, could not be resolved. These results show that intraspecific variation is common in artiodactyls and perissodactyls, and suggest a variable ancestral social organization for Artiodactyla.
iv ACKNOWLEDGEMENTS
First and foremost, I would like to thank my incredibly dedicated advisor, Dr. Loren
Hayes, for the unwavering support and guidance that he has provided throughout my graduate studies. I would also like to thank my committee members, Dr. Hope Klug and Dr. Tim Gaudin, for their invaluable insights. I am extremely thankful for my collaborators: Dr. Carsten Schradin, for his crucial advice during the conception and completion of this thesis; Dr. Marco Festa-
Bianchet, for his knowledge on all things ungulate-related; and, Dr. Adrian Jaeggi, for his expertise and guidance with the phylogenetic work. Finally, I would like to give special thanks to my family, friends, and fellow graduate students who became the best support system one could ask for.
v TABLE OF CONTENTS
ABSTRACT ...... iv
ACKNOWLEDGEMENTS ...... v
LIST OF TABLES ...... viii
LIST OF FIGURES ...... ix
LIST OF ABBREVIATIONS ...... x
LIST OF TERMS ...... xi
CHAPTER
I. A REVIEW OF INTRASPECIFIC VARIATION IN ARTIODACTYLA AND PERISSODACTYLA SOCIAL SYSTEMS ...... 1
Introduction ...... 1 Social Systems ...... 1 Socioecological Theory ...... 3 Intraspecific Variation in Social Systems ...... 4 Artiodactyla and Perissodactyla ...... 5 Thesis Objectives ...... 9 Artiodactyla Social Organization ...... 9 Bovidae ...... 13 Cervidae ...... 16 Suidae ...... 19
Other Families ...... 21 Artiodactyla Mating Systems ...... 24 Bovidae ...... 25 Cervidae ...... 28 Suidae ...... 29 Other Families ...... 30 Summary of Artiodactyla Social Organization and Mating System ...... 31 Perissodactyla Social Organization ...... 32 Equidae ...... 33 Rhinocerotidae ...... 34 Tapiridae ...... 34
vi Perissodactyla Mating System ...... 35 Equidae ...... 35 Rhinocerotidae ...... 36 Summary of Perissodactyla Social Organization and Mating System ...... 36 Discussion ...... 36
II. ACCOUNTING FOR INTRASPECIFIC VARIATION TRANSFORMS UNDERSTANDING OF ARTIODACTYL SOCIAL EVOLUTION ...... 39
Introduction ...... 39 Methods...... 46 Social Organization and Mating System ...... 46 Ecology and Life History ...... 48 Phylogeny ...... 48 Statistical Analysis ...... 49 Results ...... 51 Occurrence of Intraspecific Variation in Social Organization ...... 51 Phylogenetic Reconstruction of Ancestral Social Organization State and Factors Influencing IVSO ...... 51 Occurrence of Intraspecific Variation in Mating System ...... 58 Phylogenetic Reconstruction of Ancestral Mating System State and Factors Influencing IVMS ...... 58 Discussion ...... 61 Phylogenetic Reconstruction of Artiodactyla Social Organization and Mating System ...... 61 Ecological and Life History Predictors of IVSO and IVMS ...... 63 Limitations ...... 65 Need for Long-term Studies and Manipulative Field Studies ...... 66 Conservation Implications and Concluding Remarks ...... 67
REFERENCES ...... 69
APPENDIX
A. SOCIAL ORGANIZATION DATA ...... 85
B. MATING SYSTEM DATA ...... 90
C. ECOLOGICAL AND LIFE HISTORY DATA ...... 93
D. PHYLOGENETIC MODELS ...... 98
VITA ...... 100
vii LIST OF TABLES
1.1 A Breakdown of the Diversity of Mammalian Orders Artiodactyla and Perissodactyla ...... 7
1.2 A Breakdown of Family-level Artiodactyla Social Organization Showing the Number of Species That Were Found to be Solitary, Pair-living, Group- living, or to Exhibit IVSO ...... 10
1.3 Number of Seasonally Breeding Artiodactyl Species Exhibiting Intraspecific Variation in Social Organization by the Season During Which the Variation Occurs ...... 11
1.4 A Breakdown of Family-level Artiodactyla Mating System Classification Showing the Number of Species That Exhibit a Particular Mating System ...... 25
1.5 A Breakdown of Family-level Perissodactyla Social Organization Showing the Number of Species That Were Found to be Solitary, Pair-living, Group- living, or to Exhibit IVSO ...... 32
1.6 A Breakdown of Family-level Perissodactyla Mating System Classification Showing the Number of Species That Exhibit a Particular Mating System ...... 35
2.1 A Breakdown of the Hypotheses and Predictions for Phylogenetic Reconstruction of Artiodactyla Ancestral Social Organization and Mating Systems as Well as Ecological and Life History Predictors of IVSO and IVMS...... 45
viii LIST OF FIGURES
1.1 A flowchart showing the relationships among four interrelated social system components: social organization, mating system, social structure, and care system ...... 2
1.2 Agnarsson and May-Collado (2008)’s phylogenetic tree showing the evolutionary relationship among artiodactyls and perissodactyls ...... 8
1.3 Graphs showing the significant positive correlations between the number of different types of social organizations per species reported and (a) the number of populations studied and (b) the number of studies published on social organization among artiodactyls (data points represent individual species) ...... 12
2.1 A simple ancestral state estimation using discrete traits that predicts a variable ancestral social organization state (99.9%) over a solitary or group-living state (<0.1%) of Artiodactyla ...... 52
2.2 A graphical comparison of the probability of solitary, group-living, and variable social organization at the ancestral node of all Artiodactyla...... 54
2.3 A chart showing the probability of an artiodactyl population exhibiting more than one form of social organization relative to female body mass; the solid line represents the predicted mean, whereas the thin lines show 100 random samples drawn from the posterior distribution to illustrate the degree of uncertainty ...... 55
2.4 Posterior distributions of the habitat level random intercepts (zero indicates the global average in the probability of variable social organization) ...... 56
2.5 A diagram showing the number of social organizations per species in the artiodactyl phylogeny...... 57
2.6 A diagram showing the probability of polygyny (43.0%), promiscuity (24.3%), variable (20.9%), or monogamy (11.8%) mating system at the ancestral node of all Artiodactyla...... 59
2.7 A diagram showing the number of mating systems per species in the artiodactyl phylogeny...... 60
ix LIST OF ABBREVIATIONS
BM, body mass
F, solitary adult female
FF, multiple adult females
FFM, multiple breeding females and one breeding male
FMM, one breeding female and multiple breeding males
FFMM, multiple breeding females and multiple breeding males
IUCN, International Union for Conservation of Nature
IVMS, intraspecific variation in mating system
IVSO, intraspecific variation in social organization
M, solitary adult male
MF, adult male-female pair
MM, multiple adult males
MS, mating system
SO, social organization
x LIST OF TERMS
Care system – describes who cares for dependent young.
Developmental plasticity – emerges as a response to environmental variation that activates the alternate developmental pathways of a single genotype and can lead to IVSO between populations.
Extrinsic factors – environmental disruptors, such as the death of a dominant breeder, that lead to non-adaptive changes in social organization and cause IVSO within a population.
Genetic variation – describes how genotypic differences between individuals influences social behavior and can lead to the expression of different social organizations between populations.
Harem defense polygyny – mating system in which a male holds a group (or harem) of females and mates with the females in that group while those females mate with that male only.
Intraspecific variation in social organization (IVSO) – occurs when a species shows two or more forms of social organization. There are four proposed mechanisms that lead to IVSO: (i) genetic variation, (ii) developmental plasticity, (iii) social flexibility, and (iv) extrinsic factors.
Intraspecific variation in mating system (IVMS) – occurs when a species shows two or more mating systems.
Lekking system – mating system in which males aggregate in a lek and engage in competitive displays while the females choose which male to mate with.
Mating system – describes the mating interactions among conspecifics.
Monogamy – mating system in which males and females mate with only one member of the opposite sex.
Polyandry – mating system in which one female mates with several males.
Polygynandry – mating system in which several males defend and mate with a group of several females.
xi Promiscuity – mating system in which males mate with multiple females and females mate with multiple males.
Single-female defense polygyny – mating system in which a male defends a single female from other males until mating has occurred before repeating the process with another female.
Social flexibility – result of individuals reversibly changing social tactics due to short-term changes in their environment which can lead to IVSO within a population.
Social organization – describes the size, composition, and kin structure of groups or social units.
Social structure – describes the interactions between conspecifics and the resulting relationships within a social unit.
Social system – conspecifics that regularly interact more with each other than they do with other conspecifics in the population. There are four main components of a social system: (i) social structure, (ii) care system, (iii) social organization, and (iv) mating system.
Tactic – pattern of behavior where an individual has an option as to which behavioral response is shown.
Territorial defense polygyny – mating system in which males hold a territory or defend an area of resources and mate with the females that enter that territory while those females mate with that male only.
Ultrametric - all paths from the root of the phylogenetic tree are equal in length.
xii CHAPTER I
A REVIEW OF INTRASPECIFIC VARIATION IN ARTIODACTYLA
AND PERISSODACTYLA SOCIAL SYSTEMS
Introduction
Social Systems
Mammalian social systems are extremely complex and diverse, ranging on a continuum from solitary living (non-social) to eusocial societies with complex caste systems (Clutton-Brock
1989, Jarvis and Bennett 1993, Hayes 2000, Silk 2007, Koenig and Dickinson 2016, Rubenstein and Abbot 2017). Examining this diversity in social systems is fundamental in understanding the evolution of social systems and developing effective species management and conservation plans. Part of this diversity can be attributed to the complex interactions among the four main components of a social system: (i) social structure, (ii) care system, (iii) social organization, and
(iv) mating system (Kappeler and van Schaik 2002, Kappeler 2018 in press; Figure 1.1). The term social structure describes the interactions among conspecifics and the resulting relationships within a social unit. These relationships among individuals are a reflection of selected behavioral strategies that maximize individual fitness (van Schaik 1989). Dominance relationships and intraspecific communication are important aspects of a social structure (Kappeler 2018 in press).
The term care system describes who cares for dependent young. There are three main categories of parental care systems: uni-parental (maternal or paternal), bi-parental, and allo-parental. The care system may also involve cooperative breeding, a system characterized by allo-parental care where offspring of a dominant reproductive female are also cared for by other females in the 1 group who do not have offspring of their own (Solomon and French 1997). Four interrelated components of social systems are diagramed in Figure 1.1 (adapted from Kappeler 2018 in press).
Figure 1.1 A flowchart showing the relationships among four interrelated social system components: social organization, mating system, social structure, and care system
The term social organization describes the size and composition of groups or social units.
These types of social organization are relatively easy to identify in the field and usually do not require knowledge about the interactions and relationships between group members. Non-social species are solitary, spending the majority of their time apart from conspecifics. Group sizes can vary greatly among social groups, with the smallest being pairs of individuals and the largest
2 groups containing thousands of individuals (Kappeler 2018 in press). Group composition typically refers to the sex, age, and kin structure of a social unit. Whereas the sex and age composition of a group can generally be assessed in the field for many taxa, genetic analyses are required to assess the kin structure of a group. The term mating system refers to the mating interactions among individuals. When describing the mating system of a species, both the social and genetic components must be considered. Mammals exhibit a wide range of mating systems ranging from obligate monogamy to promiscuity (Clutton-Brock 1989). While the social mating system is usually easy to discern in the field, examining the genetic mating system of a species is more complex and requires assigning paternity via long-term studies. These four components are not entirely independent of one another and must be considered collectively to fully understand a social system.
Socioecological Theory
Of the four social system components, social organization and mating system are intimately linked through socioecological theory, in that the number and spatial distribution of individuals characterizing the social organization can influence the mating tactics of those individuals (Kappeler and van Schaik 2002). Socioecological theory describes how selective forces, such as the distribution of resources and mates, influences the behavior of individuals, in turn shaping the defining characteristics of a social system (Emlen and Oring 1977, Lott 1991,
Kappeler and van Schaik 2002, Clutton-Brock and Lukas 2012). In polygynous species, female spatial distribution, or their social organization, is largely determined by the distribution of predation risk, availability of resources, and openness of habitat (Jarman 1974, Kappeler and van
Schaik 2002). Consequently, the social organization of oestrus females drives the mating strategies and social organization of males (Emlen and Oring 1977, Clutton-Brock 1989,
Kappeler and van Schaik 2002).
3 For example, in southern bamboo rats (Kannabateomys amblyonyx), the mating system varies between polygyny and monogamy, as influenced by food and resource distribution
(Stallings et al. 1994, Silva et al. 2008). Stallings et al. (1994) found that population density and rates of polygyny were high when food was distributed homogenously. In a separate population where food resources were sparse, female densities were low, resulting in male defense of solitary females and a monogamous mating system (Silva et al. 2008). In this way social organization can impose a direct constraint on mating system.
Intraspecific Variation in Social Systems
Decades of research have shown that social systems in mammals can vary within a species across space and time (Lott 1984, 1991, Travis et al. 1995, Moehlman 1998, Yamagiwa et al. 2003, Schradin and Pillay 2005, Schradin 2013, Schradin et al. 2018). Intraspecific variation in social systems describes the variation in the size, sex-age, and kin composition of groups within a species (social organization, Schradin 2013) and variation in breeding tactics to acquire mates within a species (mating system, Lott 1984, 1991). Intraspecific variation in social organization (IVSO) is relatively common in mammals, occurring, for example, in Artiodactyla
(Jarman 1974), Carnivora (Dalerum 2007), Eulipotyphla (Valomy et al. 2015), Primata
(Yamagiwa et al. 2003, Agnani et al. 2018), and Rodentia (Schradin and Pillay 2005, Maher and
Burger 2011). Although less commonly observed, intraspecific variation in mating systems
(IVMS) has been recorded in Artiodactyla (Byers and Kitchen 1988, Thirgood et al. 1999),
Carnivora (Kamler et al. 2004), and Rodentia (Maher and Burger 2011).
Schradin (2013) identified four mechanisms that can lead to intraspecific variation in social organization: (i) genetic variation, (ii) developmental plasticity, (iii) social flexibility, and
(iv) extrinsic factors, or environmental disrupters. Genetic variation describes how genotypic differences among individuals can influence social behavior and contribute to IVSO (Schradin
4 2013). Developmental plasticity emerges as a response to environmental variation that activates the alternative developmental pathways of a single genotype (Piersma and Drent 2003). This mechanism is a response to the environment during ontogeny. Social flexibility is the result of individuals changing social tactics due to short-term changes in their environment (Schradin et al. 2012). These changes are reversible. The most important factor in the evolution of social flexibility is ecological constraint. Social flexibility is thought to have evolved as an adaptation to unpredictable environments which selects for high phenotypic flexibility (Schradin et al.
2012). Extrinsic factors, or environmental disrupters, can lead to non-adaptive changes in social organization and is not due to an individual’s adaptive response to environmental change
(Schradin 2013). The death of a dominant breeder (Anzenberger and Falk 2012), fluctuations in population density (e.g., Jackson 1999, Bothma and Walker 2013), and human exploitation such as hunting (Milner et al. 2007, Festa-Bianchet et al. 2017) are external forces that can change population structure and group composition. A premise of socioecological theory is that social organization influences the mating system (Koenig et al. 2013). Consequently, intraspecific variation in social organization has the potential to lead to intraspecific variation in mating systems within a species or population. Thus, understanding intraspecific variation in social organization and mating systems is important because it has implications for population dynamics, genetic variability, and life-history evolution, as well as potential consequences for human exploitation or conservation.
Artiodactyla and Perissodactyla
The mammalian orders Artiodactyla (even-toed ungulates) and Perissodactyla (odd-toed ungulates) are closely related taxa (Meredith et al. 2011, O'leary et al. 2013) that exhibit great diversity in social systems and experience a variety of ecological conditions (Jarman 1974,
Vaughan et al. 2015). Artiodactyls are more abundant and diverse than perissodactyls (Table
5 1.1). Artiodactyls are widely distributed, being native to every continent except Australia (where they have been introduced) and Antarctica (Vaughan et al. 2015). Perissodactyls, on the other hand, are less widely distributed, occurring as wild species in Central and South America, Africa, and Asia (Vaughan et al. 2015).
Recent studies have suggested that the order Artiodactyla is a paraphyletic group with respect to cetaceans (whales and dolphins). Molecular phylogenetic evidence supports hypotheses that cetaceans and artiodactyls are closely related, with cetaceans now being placed within the order Artiodactyla (Nikaido et al. 1999, Agnarsson and May-Collado 2008, see Figure
1.2). This has prompted some researchers to adopt the term “Cetartiodactyla” to describe the order containing both artiodactyls and cetaceans. For the purpose of this study I used the traditional name Artiodactyla, due to my focus on terrestrial hoofed mammals. I excluded cetaceans from this study because of the extremely different ecological conditions and environments they inhabit relative to their terrestrial artiodactyl relatives. Thus, I only discuss intraspecific variation in social systems the terrestrial artiodactyls and perissodactyls.
6 Table 1.1 A Breakdown of the Diversity of Mammalian Orders Artiodactyla and Perissodactyla
Artiodactyla
Family Number of genera Number of species Common examples
Antilocapridae 1 1 Pronghorn
Antelope, bison, gazelles, Bovidae 50 134 sheep, goats
Cervidae 18 48 Deer, moose, elk
Hippopotamidae 2 2 Hippopotamus
Moschidae 1 6 Musk deer
Suidae 5 14 Wild boar, warthog
Tayassuidae 3 3 Peccaries
Tragulidae 3 8 Mouse deer
Perissodactyla
Family Number of genera Number of species Common examples Equidae 1 7 Zebras, horses, donkeys Rhinocerotidae 4 5 Rhinoceros Tapiridae 1 4 Tapir
Source: Vaughan et al. 2015.
7
Figure 1.2 Agnarsson and May-Collado (2008)’s phylogenetic tree showing the evolutionary relationship among artiodactyls and perissodactyls
Artiodactyls and perissodactyls are good taxonomic groups for investigating the extent of intraspecific variation in social systems because these orders are characterized by great diversity in social systems, ecology, and life history traits. One might expect a large amount of
8 intraspecific variation in social organization in artiodactyls due to their wide distribution, utilization of a variety of habitats, and frequent expression of sexual dimorphism and seasonal breeding. Intraspecific variation in social organization is relatively common in artiodactyls (see
Jarman 1974, Isvaran 2007) and perissodactyls (see Moehlman 1998). Although less common, intraspecific variation in mating systems also has been observed in artiodactyls (see Langbein and Thirgood 1989, Adamczak and Dunbar 2008). Despite these observations, we lack a comprehensive review of intraspecific variation in social organization and mating system in
Artiodactyla and Perissodactyla.
Thesis Objectives
My main goal for this thesis is to describe the extent to which intraspecific variation in social organization and mating system occurs in Artiodactyla and Perissodactyla, and to determine evolutionary transitions in artiodactyl social systems. My objective for this introduction is to conduct a comprehensive review of the literature and discuss the extent to which intraspecific variation in social organization and mating system has been documented in
Artiodactyla and Perissodactyla. By first understanding the extent to which intraspecific variation in social organization and mating systems has been observed in these groups, I can then use the assembled dataset to analyze the evolution of artiodactyl social systems.
Artiodactyla Social Organization
After a comprehensive search of the literature, I found field data on the social organization of 45% of artiodactyl species (100/221 species). The majority (82%) of species for which field data exists showed intraspecific variation in their social organization, with five species being strictly solitary (5%), one species being strictly pair-living (1%), and twelve
9 species exhibiting only one form of group-living (12%; Table 1.2). I did not find field data on the male-female social organization for any extant species in the families Tragulidae or Tayassuidae.
Table 1.2 A Breakdown of Family-level Artiodactyla Social Organization Showing the Number of Species That Were Found to be Solitary, Pair-living, Group-living, or to Exhibit IVSO
Species Solitary Pair-living Group-living IVSO Unknown
Antilocapridae (n=1) - - - 1 0 Bovidae (n=134) 3 1 11 54 65
Camelidae (n=3) - - - 3 0
Cervidae (n=48) - - 1 17 30
Giraffidae (n=2) - - - 1 1
Hippopotamidae (n=2) - - - 1 1
Moschidae (n=7) 2 - - - 5
Suidae (n=14) - - - 5 9 Note: n = total number of extant species; “-” indicates no data from the primary literature.
Among species with seasonality and social organization data, 54 species were seasonal breeders and 22 species were non-seasonal breeders. For seasonally breeding species, intraspecific variation in social organization occurred during the breeding season in 13% of species, during the non-breeding season in 33% of species, both during the breeding and non- breeding seasons in 50% of species, and between breeding and non-breeding seasons in 4% of species (Table 1.3).
10 Table 1.3 Number of Seasonally Breeding Artiodactyl Species Exhibiting Intraspecific Variation in Social Organization by the Season During Which the Variation Occurs
Family Breeding Season Non-Breeding Season Both Between
Antilocapridae (n=1) 1 - - 0 Bovidae (n=35) 4 13 17 1
Camelidae (n=3) - 2 1 0 Cervidae (n=14) 2 3 8 1
Suidae (n=1) - - 1 0
Note. n = total number of seasonally breeding species; “-” indicates no data from the primary literature.
The number of different types of social organizations reported per species ranged from 1-
6 and increased with the number of studies published (range: 1-16, rs=0.370, p=0.01) and the number of populations studied (range: 1-11, rs=0.350, p=0.01; Figure 1.3). While study effort was significantly correlated with the reporting of intraspecific variation in social organization, the low R2 values indicate that study effort alone does not explain the frequent occurrence of intraspecific variation in social organization among artiodactyls.
11
Figure 1.3 Graphs showing the significant positive correlations between the number of different types of social organizations per species reported and (a) the number of populations studied and (b) the number of studies published on social organization among artiodactyls (data points represent individual species)
12 The remainder of this section provides an in-depth look at specific examples of species that exhibit one form of social organization (solitary, pair-living, or group-living) and species exhibiting intraspecific variation in social organization within the major artiodactyl families.
Bovidae
The primary literature search revealed data on the social organization of 52% of bovid species (69/134). Of the 69 species with field data, only three (4.4%) were reported as strictly solitary. A study of yellow-backed duikers (Cephalophus silvicultor) in Moukalaba-Doudou
National Park, Gabon, reported solitary individuals but never groups of adults (Nakashima et al.
2013). Similarly, Novellie et al. (1984) observed that cape grysbok (Raphicerus melanotis) in the
Jonkershoek Valley southeast of Stellenbosch, South Africa were typically solitary during the three month study period. Out of a total of 40 sightings, 38 were of solitary individuals. The remaining observations consisted of an adult female with an infant and one association of a male-female pair (Novellie et al. 1984). Adult four-horned antelope (Tetracerus quadricornis), in the tropical forests of southern India, were also observed to be solitary. Upon the conclusion of a six month study (September 1998 to February 1999), 62% of observations were of solitary individuals, and all groups sighted were composed of an adult with fawns and/or subadults
(Baskaran et al. 2011).
One bovid species, Kirk’s dik-dkik (Madoqua kirkii), is reported as pair-living. In Etosha
National Park, Namibia, Kirk’s dik-dik were almost exclusively found in adult male-female pairs
(Brotherton and Rhodes 1996, Brotherton and Manser 1997, Brotherton et al. 1997). While
Brotherton and Manser (1997) reported four instances of a group containing one adult male and two females, these groups were rare. Single male/multi-female groups formed when an unrelated dispersing female joined an already established male-female pair. This grouping typically persisted until one of the females died, returning to a pair-living form of social organization
13 (Brotherton and Manser 1997). A separate population of Kirk’s dik-dik in Tsavo East National
Park, Kenya were also observed to live in male-female pairs for the majority of the year
(Brotherton et al. 1997).
Eleven species (16%) with known social organization were characterized as group-living with only one form of social organization. For example, a study of roan antelope (Hippotragus equinus) at the Lambwe Valley Game Reserve in Kenya revealed that the main social unit of the population consisted of a group of adult females headed by a single adult male (Allsopp
1979). A study on a second population of roan antelope, in South Africa, found that herd composition consisted of a single dominant adult male, a subordinate male, six adult females, and a number of subadults (Perrin and Taolo 1998). Adult male Heptner’s markhors (Capra falconeri heptneri) in the Kugitang Nature Reserve in Turkmenistan were typically solitary and occupied elevations higher than 1,800m. Females, on the other hand, appeared to be social and occurred in female-only groups of up to 44 individuals at elevations below 1,800m (Weinberg et al. 1997).
The majority of bovid species (78%, 54/69 species) exhibit some form of intraspecific variation in social organization. Thirty-one percent of these species showed intraspecific variation in social organization within a population, but not between populations. For example, the tamaraw (Bubalus mindorensis) is a critically endangered species endemic to the Philippine island of Mindoro, with ~90% of remaining individuals belonging to one subpopulation in
Mount Iglit-Baco National Park (Boyles et al. 2016). Kuehn (1986) studied the tamaraw at
Mount Iglit-Baco National Park and found that 82% of observations consisted of solitary males.
Female tamaraw were encountered alone or with 1-3 calves. The largest aggregation seen during the study period consisted of an adult male, adult female, and a calf (Kuehn 1986). The population dynamics and herd behavior of the same population of tamaraw was studied each
14 April from 2006-2011(Ishihara et al. 2007, Ishihara et al. 2015). In these studies, 10% of tamaraw were solitary males or females, whereas 90% formed groups with a mean group size of
3.57 individuals/group. The majority of groups contained one or two adult females with half of those groups also including a single adult male (Ishihara et al. 2015).
Hirola (Beatragus hunter) also showed intraspecific variation in social organization within a population during the non-breeding season. A combination of aerial and ground surveys of hirola in Tsavo East National Park, Kenya, revealed that adults were either solitary or in groups with an average size of 7.5 individuals. Bachelor herds consisting of one to three males were observed but were temporary associations. Groups mainly consisted of either a single adult male with multiple females or multiple males with multiple females (Andanje and Ottichilo
1999). Probert et al. (2015) studied the same population of hirola in May-June of 2011, and observed a mean group size of 6.6 individuals. Females were found in nursery herds or in groups accompanied by one or two adult males. Male hirola were found either alone, in a bachelor herd, or accompanying a female nursery herd (Probert et al. 2015).
Sixty-nine percent of bovid species with variable social organization showed intraspecific variation in social organization both within and between populations. One well-documented example of such intraspecific variation is the oribi (Ourebia ourebi). In the Serengeti National
Park in Tanzania, average group size for adult oribi was 3.1 individuals. Adult male social organization was highly variable, with some adults holding territories as solitary individuals and others forming male-only groups of up to three individuals. Twenty-seven percent of observed groups contained multiple adult males and multiple adult females. There were no observations of female-only groups. Male-female pairs made up 21% of observations, but the most common type of social organization was a group consisting of a single adult male and multiple adult females
(Arcese et al. 1995). A two-year study of oribi located in Lake Mburo National Park in Uganda
15 revealed that animals within this population lived in male-only groups, female-only groups, or in mixed sex groups of varying composition (Averbeck et al. 2012). Rowe-Rowe et al. (1992) studied oribi on seven properties in Natal, South Africa that varied in habitat type. Across the seven sites, the majority of observations were of male-female pairs. Solitary males and females, as well as female-only, male-only groups, and mixed sex groups consisting of one adult male and multiple adult females were also recorded. Average oribi group size was smallest in montane grasslands (1.89±0.85) and highest in the tropical grassland habitats (2.92±1.34). Single individuals and male-female pairs were more common in the montane grasslands. Larger groups, including one male and multiple females, were more frequent in the tropical grassland areas
(Rowe-Rowe et al. 1992).
Similarly, the Tibetan antelope or chiru (Pantholops hodgsonii) shows intraspecific variation in social organization during the non-breeding season. Sexual segregation was observed among chiru at Qiangtang Nature Reserve in China, where female-only groups were found in different locations than male-only groups. If adult males were not part of a male-only group, they were often found alone (Schaller et al. 1991). During the breeding season, however, chiru in
Arjinshan Nature Reserve in China were see in herds containing several females headed by one adult male (Buzzard et al. 2008).
Cervidae
I found data on the social organization for 38% of cervid species (18/48). Only one species, the barasingha (Rucervus duvaucelii), was categorized as group-living only (Tewari and
Rawat 2013). The remaining cervid species with known social organization showed some form of intraspecific variation in social organization. Four cervid species with variable social organization (24%) showed intraspecific variation in social organization within a population only. The Indian muntjac, or barking deer (Muntiacus muntjak), is often solitary, but also forms
16 male-female pairs. Seidensticker (1976) studied Indian muntjac populations in the Chitawan
Valley of Nepal, and found that they were primarily solitary. A male-female pair was sighted once, and the remaining pairs consisted of an adult female with young (Seidensticker 1976).
Indian muntjac in Margalla Hills National Park, Pakistan are also primarily solitary, but do occasionally group together, mainly as an adult male-female pair. Pairs of adult females grazing together, as well as single adult females accompanied by one fawn, were also observed (Hameed et al. 2009). Barrette (1977) studied a subspecies of Indian muntjac (Muntiacus muntjak malabaricus) in Wilpattu National Park in Northwest Ceylon, and found that individuals were solitary, apart from occasional male-female pairs and single adult females with young (Barrette
1977).
Argunov and Safronov (2013) studied the demographic structure of a population of
Siberian roe deer (Capreolus pygargus) in central Yakutia from 1998 to 2011. The frequency of occurrence for solitary individuals, both male and female, was 45.6%, whereas the frequency for pairs of varying composition was 32.2%. Siberian roe deer were also observed to occur in groups of three to five individuals, but the sex and demographic composition of these groups was largely unknown. The composition of one group consisted of an adult male, two adult females, and two calves (Argunov and Safronov 2013).
Sambar (Rusa unicolor) in the Chitawan Valley in Nepal were frequently found alone or in small groups of up to 4 individuals. Groups of two or three males were observed on occasion, and a group of two females with fawns was observed twice. The largest group was observed in a clearing at dusk, and consisted of two adult males, four adult females, and several sub-adults and young (Seidensticker 1976). Sambar in the Ranthambhore Tiger Reserve in western India were found to be both solitary and to live in groups, with a mean group size of 3.4±0.3 individuals; however, the sex and demographic composition of those groups was not reported. Sambar
17 formed larger groups in open habitats, whereas smaller groups were more common in forests
(Bagchia et al. 2008). Group sizes of sambar in a separate population in the Pathri Rao
Watershed in the Shivalik Ecosystem of India were smaller, and averaged 1.56±0.18, with a range of 1-4 individuals (Dar et al. 2012). Details regarding the composition of observed groups were not reported.
Thirteen species (72% of species with social organization data) showed intraspecific variation in social organization both within and between populations. In Doñana National Park,
Spain, fallow deer (Dama dama) lived in single-sex groups for the majority of the year, outside the breeding season. The average group size was 8.67±1.44 individuals for female-only groups, and 5.21±0.91 individuals for male-only groups. Mixed sex groups of varying size and composition were observed to form during the rutting season (Braza et al. 1990). Fallow deer on the San Rossore Preserve, west of Pisa, Italy, were frequently solitary during the autumn months, and tended to form groups during winter and spring. Females were typically in groups with subadults and/or fawns. Males were mainly solitary, but did form unstable bachelor herds of adult males. Mixed sex groups of multiple adult males and females were observed in open grassland habitats (Apollonio et al. 1998).
Group size dynamics of red deer (Cervus elaphus) were studied in the Białowieża
Primeval Forest in Poland. Males were primarily solitary in all seasons. Females were found in groups of two or more individuals during autumn and winter, but were solitary more frequently during the summer. The composition of groups included male-only groups, female-only groups, and mixed sex groups of unspecified composition (Jedrzejewski et al. 2006). Red deer at Lousã
Mountain in central Portugal exhibited segregation of the sexes into male-only and female-only groups throughout the year, except during the rut and breeding seasons. During the rut, males
18 and females aggregated in mixed sex herds that varied in demographic composition and size
(Alves et al. 2013).
Huemul deer (Hippocamelus bisulcus) also exhibit intraspecific variation in social organization both within and between populations. In Nevados de Chillán, Chile, groups ranged in size from 1-3 individuals. Solitary individuals were observed most frequently, with solitary males being more common than solitary females. Adult male-female pairs were also observed during the breeding season (Povilitis 1983). A study on the same population also recorded solitary individuals and a mean group size of 1.9±0.9, with a range of 1-5 individuals. Povilitis
(1985) reported the most common pattern of social organization as adult male-female pairs.
Although most sightings were of solitary individuals and pairs, one group of an adult male with two females was found (Povilitis 1985). A more recent publication reporting on the social ecology of huemul deer in Torres del Paine National Park in Chile also observed male-female pairs and solitary males and females (Garay et al. 2016).
Suidae
The primary literature search yielded data on the social organization of 36% of suid species (5/14). All five species for which the social organization was examined showed some form of intraspecific variation in social organization. Two species showed intraspecific variation in social organization both within and between populations. Babirusa (Babyrousa babyrussa) in the Paguayaman Forest of North Sulawesi, Indonesia were found to occur both as solitary individuals and in groups ranging from 2-13 individuals. About half of all observations were of solitary individuals, with 68.9% of those being adult males. Adult females were typically observed either alone, with young or immatures, or with other adult females and young. Adult male-female pairs were recorded in 1.8% of observations (Clayton and MacDonald 1999).
Babirusa of the Paleleh Mountain range in North Sulawesi, Indonesia were also solitary in about
19 half of the recorded observations. Adult male-female pairs were observed, but males were never seen with more than one female unless young were present. Females were almost never alone, and were most commonly accompanied by young or other adult females and young. Multiple females with young were sometimes accompanied by a single adult male or two adult males
(Patry et al. 1995).
Wild boar (Sus scrofa) in the Tour du Valat Reserve in France were found to occur in groups ranging from 1-23 individuals. Only 8.2% of observations were of solitary adults whereas
91.8% of observations were of groups averaging about 4 individuals. Group sizes were found to increase in the breeding season while solitary individuals, particularly solitary males, were more common in the non-breeding season (Dardaillon 1988). The social organization of wild boar was also studied in Doñana National Park in Spain during the early 1990s. Wild boar were reported in groups ranging from 1-11 individuals, with a mean group size of 3.21±0.69 individuals. Three main types of groups were found: male-only groups (including solitary males), female-only groups (including solitary females), and mixed sex groups consisting of multiple adult males and females. Male-only groups were common year-round, whereas female-only groups increased in frequency after the breeding season, during the gestation period. Mixed sex groups of varying size and composition were more common during the breeding season (Fernández-Llario et al.
1996). The social organization of wild boar was studied in the National Park of Cilento e Vallo di Diano in southern Italy. Maselli et al. (2014) found a mean group size of 4.14±0.21 individuals. Family groups of one or more adult females with young were usually seen during the summer and autumn months, whereas solitary females were common during spring and winter.
Male-only groups were only observed during the spring; however, solitary males were observed year-round. Mixed sex groups of multiple males and multiple females occurred more frequently during the winter (Maselli et al. 2014).
20 The remaining three species showed intraspecific variation in social organization within a population only. Bush pigs, or red river hogs (Potamochoerus porcus), in the Kibale Forest,
Uganda were recorded both as solitary individuals and in groups, with a mean group size of 3.2 individuals. Larger groups contained one adult male with one or more females, either with or without young (Ghiglieri et al. 1982). A separate population of red river hogs was studied more recently on Tiwai Island, Sierra Leone. This study revealed a mean group size of 2.46±0.28 individuals, but the sex and demographic compositions of those groups was not reported
(McCollum et al. 2017).
Group structure and social behavior of warthogs (Phacochoerus aethiopicus) were studied in the Andries Vosloo Kudu Reserve in South Africa. The field survey revealed 45% of warthogs to be solitary males or females. Bachelor groups were observed to be formed either of sub-adults, or more than one adult male. Female warthogs were observed to form matriarchal groups, including one or more adult females (Somers et al. 1995). Common warthogs
(Phacochoerus africanus) in Hluhluwe-iMfolozi Game Reserve in South Africa were found to be solitary or to live in groups of up to 8 individuals. Adult female-only groups were typically larger than adult male-only groups (White 2010). A separate study found that female common warthogs lived both as solitary individuals and in groups. Males were sighted in groups of varying size and composition, but were more often accompanied by other warthogs during the mating season (White et al. 2010). Female common warthogs also formed breeding groups providing communal care of young (White et al. 2010, White and Cameron 2011).
Other Families
This section will focus on families with few extant species or few species with available data on social organization. The lone extant representative of the family Antilocapridae, the pronghorn (Antilocapra americana), exhibits intraspecific variation in social organization both
21 within and between populations. On the Sheldon National Antelope Refuge in Nevada, USA, pronghorn occurred in groups containing one adult male and 1-8 adult females during the breeding season. Males that did not hold a harem of females were solitary (Maher 1991). This variation in social organization was present during the breeding season. In the northern portion of Yellowstone National Park in Wyoming, USA, the typical group size ranged from 4.7 to 42.0 individuals. Mixed sex groups of varying composition were recorded throughout the year, but occurred at the lowest frequency during May and June. The specific sex and demographic composition of the groups observed was not reported (White et al. 2012).
Hippopotamidae comprises two extant species; however, I found information on the social organization of only one species, the hippopotamus (Hippopotamus amphibius). Karstad and Hudson (1986) reported that, in the Mara River in Kenya, adult male hippos were either solitary or accompanied a group of females. The majority of groups contained one to multiple males and several females (Karstad and Hudson 1986). The remaining publications that report the social organization of hippopotami report group sizes but do not report group composition.
For example, hippos in Gonarezhou National Park in Zimbabwe were typically found in groups with a mean group size of 9.8; however, the sex and demographic composition of those groups was not reported (Zisadza et al. 2010). A separate population in Haut Niger National Park in the
Republic of Guinea had a mean group size of 3.3 individuals, but, again, group composition was unknown (Brugiere et al. 2006).
Of the seven extant species in the family Moschidae, I found information on the social organization of two species, both of which were classified as strictly solitary. Musk deer
(Moschus cupreus) in the eastern forests of Afghanistan was found to be primarily solitary.
There were five sightings of musk deer during the study, which included a solitary male sighted three times, a solitary female, and a female with a juvenile (Ostrowski et al. 2016). In a field
22 survey of Himalayan musk deer (Moschus leucogaster) in Gilgit-Baltistan, Pakistan, solitary individuals were observed in all but one instance, where a group of two was found (Fakhar-i-
Abbas et al. 2015).
Social organization data was found for only one of the two extant species in the family
Giraffidae. The giraffe (Giraffa camelopardalis) showed intraspecific variation in social organization both within and between populations. A 34-year study of Thornicroft’s giraffe
(Giraffa camelopardalis thornicrofti), a subspecies of giraffe endemic to the Luangwa Valley of
Zambia, found an overall mean herd size of 3.6±3.5, with an average herd size of 5.2±3.6 when solitary individuals were excluded. Males were more likely to be solitary than females which were alone in 8% of observations. Solitary individuals were more common in riverine and thicket habitats, whereas groups were more common in open and woodland habitats (Bercovitch and Berry 2010). Male-only herds, female-only herds, and groups containing one male and multiple females were also observed (Bercovitch and Berry 2013, 2015, Berry and Bercovitch
2015).
All three species in the family Camelidae were found to exhibit intraspecific variation in social organization. Wild Bactrian camels (Camelus bactrianus) in the Annanba Nature Reserve in China were studied during the non-breeding season. Surveys revealed that 4.7% of individuals were solitary, and 95.37% were found in groups with a mean group size of 3.2. Male-only groups, multi-male/multi-female groups, and groups containing one male and multiple females were also observed (Luzhang et al. 2005). The remaining two species showed intraspecific variation in social organization both within and between populations. Guanaco (Lama glama guanicoe) in the Ischigualasto Provincial Park in northwestern Argentina were observed in male- only groups, groups containing one male and multiple females, and as solitary males (Acebes et al. 2013). In Torres del Paine National Park in the Chilean Patagonia, guanaco were found in
23 male-only groups, as solitary males, and in family groups consisting of one male and multiple females. Female-only groups were also observed (Ortega and Franklin 1995). This variation in social organization was observed during both the breeding and non-breeding seasons. Vicuña
(Vicugna vicugna) were studied during the non-breeding season in the Los Andes Reserve of
Argentina. Solitary males, male-only groups, and single male/multi-female groups were observed (Torres and Puig 2012, Torres et al. 2015). In a separate population at the Laguna
Blanca Reserve in Argentina, vicuña were observed in male-only groups and groups containing one male and multiple females, but no solitary individuals were observed (Vila and Roig 1992, d'Arc et al. 2000).
Artiodactyla Mating Systems
I found information on the mating system for 36 of 221 species (16%) of artiodactyls
(Table 1.4). Of those species, 11 (31%) showed intraspecific variation. Nineteen species (53%) showed some form of polygyny, five species were promiscuous (14%), and one species was exclusively monogamous (3%). Information on the mating systems for species within the families Hippopotamidae or Moschidae was unavailable.
24 Table 1.4 A Breakdown of Family-level Artiodactyla Mating System Classification Showing the Number of Species That Exhibit a Particular Mating System
Territorial Defense Harem Defense Single-female Defense Lek Promiscuity Monogamy IVMS Unknown
Antilocapridae (n=1) ------1 0
Bovidae (n=134) 6 2 2 2 2 1 6 113
Camelidae (n=3) - 1 - - - - - 2
Cervidae (n=48) 1 2 3 - 1 - 2 39
Suidae (n=14) - - - - 1 - 1 12
Tayassuidae (n=3) - - - - 1 - - 2
Tragulidae (n=8) ------1 7
Note. n = total number of extant species; “-” indicates no data from the primary literature.
Bovidae
Information on mating systems was available for 16% of bovid species (21/134 species).
Twenty-nine percent of species (6/21) with mating system data showed intraspecific variation in mating system. One species, the kob (Kobus kob), showed within-species variation in mating systems between populations. Kob in Queen Elizabeth National Park, Uganda exhibited a lekking polygynous system (Balmford et al. 1992, Deutsch 1994), whereas kob in Comoe
National Park in West Africa showed a territorial defense polygynous mating system (Fischer and Linsenmair 1999, Fischer and Linsenmair 2007). The Japanese serow (Capricornis crispus) exhibited intraspecific variation in mating system within a population. In the Akita Prefecture of
Japan, the main mating unit was a monogamous pair, with only 20% of territorial males exhibiting polygyny. Kishimoto and Kawamichi (1996) noted that the main mating strategy of
25 males appeared to be polygynous, but female territories were so dispersed that the number of available mates for territorial males was low, leading to monogamy.
Studies on five sub-populations of oribi (Ourebia ourebi) in Ghana showed that intraspecific variation in mating strategies stemmed from female response to availability of resources, and subsequent male response to variation in female social organization. Male oribi actively defended territories (territorial defense polygyny) when female home ranges were small, but defended a single mate (single-female defense polygyny) when female home ranges were larger (Brashares and Arcese 2002). Adamczak and Dunbar (2008) studied oribi in northern
KwaZulu-Natal, South Africa, and observed both monogamous pairs and polygynous groups.
The polygynous groups, however, appeared to be unstable and dependent on seasonal food availability (Adamczak and Dunbar 2008).
The remaining fifteen species (71%) exhibited only one stable mating system. Among the polygynous species, six exhibited territorial defense polygyny. Murray (1982) found that just prior to the start of the mating period, impala (Aepyceros melampus) males would begin to clear small territories of any additional adult males. Males would then defend these territories from neighboring males and attempt to mate with groups of females that entered their territory
(Murray 1982). Bushbuck at Queen Elizabeth National Park in Uganda also showed a territorial defense polygynous mating system. Adult male bushbuck were observed to hold and defend territories during the breeding season, whereas young-adult males used surreptitious tactics to try to mate with females being courted by a territorial male (Apio et al. 2007).
Two bovid species showed a harem defense polygyny mating system. Male grey rhebok
(Pelea capreolus) at Sterkfontein Dam Nature Reserve in South Africa defended a harem of females during the breeding season (Taylor et al. 2006a, Taylor et al. 2006b). Abruzzo chamois
(Rupicapra pyrenaica ornata) also exhibited a harem defense polygynous system in which older
26 males would hold and mate with a harem of females during the breeding season (Lovari and
Cosentino 1986).
Three bovid species exhibited single-female defense polygyny. Greater kudu males
(Tragelaphus strepsiceros) at Kruger National Park in South Africa did not attempt to herd females. Instead, they defended one female at a time during courtship (Owen-Smith 1984). At
Cape au Moine in the Swiss Alps, dominant male alpine ibex (Capra ibex) monopolized and defended individual females during the breeding season. Subordinate males showed an alternate reproductive tactic, and would try to gain temporary access to a female defended by a dominant male when the female would attempt to run away (Willisch and Neuhaus 2009).
The mating system two bovid species was characterized as a lekking polygynous system.
Buzzard et al. (2008) found that at the beginning of the rutting period, the majority of chiru
(Pantholops hodgsonii) were aggregated on three separate rutting grounds. Male chiru showed territorial site fidelity and attempted to hold harems on small, closely spaced territories when aggregated with other conspecifics (Buzzard et al. 2008). Blackbuck (Antilope cervicapra) also exhibited a lekking mating system, where males actively defended territories within and around the lek-center and females visited the lek alone or in pairs. There were little to no feeding resources in the lekking area, suggesting that females were not attracted to the area by feeding opportunities, but instead visited the leks for the purpose of mating (Isvaran and Jhala 2000).
Only two bovid species were found to exhibit a promiscuous mating system. A study of mountain goats (Oreamnos americanus) at Caw Ridge in Alberta, Canada found that, during the rut, both males and females would mate with multiple partners, indicating a promiscuous mating system. Multiple mating events for the same female all occurred within two days (Mainguy et al.
2008). The Barbary sheep (Ammotragus lervia) also exhibited a promiscuous mating system
(Habibi 1997).
27 Only one bovid species exhibited a monogamous mating system. Roberts and Dunbar
(2000) observed monogamous pairs in two populations of klipspringer (Oreotragus oreotragus), one population in Kenya and the other in Zimbabwe. In a third population in South Africa, monogamous pairs were found to stay together for the entirety of the 17-month study (Tilson
1980).
Cervidae
Mating system data was available for 19% (9/48) of cervid species. Of the nine species with mating system data, two showed intraspecific variation in mating system. A study of natural populations of fallow deer (Dama dama) in southern England found variation in polygynous mating strategies within separate populations. Some adult males held territories during the breeding season and mated with groups of females which entered these territories, whereas other males displayed single-female defense polygyny. This variability in mating system appeared to be influenced by habitat structure and the density of males and females in the study populations
(Langbein and Thirgood 1989). Other studies on fallow deer mating behavior have observed leks and harem defense polygyny in addition to territorial defense and single-female defense polygyny (Thirgood et al. 1999).
Sika deer (Cervus nippon) also have been observed to exhibit intraspecific variation in mating systems. A study of sika deer in Nozaki Island off the coast of Japan revealed that 10 out of 22 females observed experienced multiple copulations during the breeding season, suggesting a promiscuous mating system (Endo and Doi 2002). In a separate population of sika deer in northern Austria, males were not associated with fixed territories, but rather took part in a lekking mating system (Bartos et al. 2003).
The remaining seven species exhibited only one mating system. Two species showed harem defense polygyny. Moose (Alces alces) in Denali National Park and Preserve in Alaska,
28 USA were found to have a harem defense polygynous mating system, in which a dominant male defended and mated with a harem of females. The average number of females per harem was
4.4±1.8 individuals for this population (Bowyer et al. 2011). Red deer (Cervus elaphus) were also observed to exhibit harem defense polygyny. Studies of red deer in Europe revealed that dominant males hold and defend harems of females during the mating season (Bonenfant et al.
2004, Perez-Gonzalez and Carranza 2011).
Three cervid species exhibited single-female defense polygyny. Chinese water deer
(Hydropotes inermis) at the Poyang Lake National Nature Reserve in China were characterized by this mating system. Males were observed pursuing females before initiating mating, and were found to mate with an average of 1.75 females (Sun and Dai 1995). Desert mule deer
(Odocoileus hemionus crooki) also exhibited single-female defense polygyny. Adult males were never observed defending harems or territories, but rather formed tending bonds in which one female was courted at a time. A few dominant males were responsible for the majority of matings in the study population (Kucera 1978).
One cervid species, the roe deer (Capreolus capreolus), showed a promiscuous mating system. Male roe deer are typically territorial and exhibit a low degree of polygyny (Vanpé et al.
2007). A genetic study of roe deer in Sweden, however, found evidence of multiple paternity in
13.5% of all litters. They also reported that, for 20.5% of litters, a half-sibling relationship was more likely than a full-sibling relationship, suggesting promiscuity (Vanpé et al. 2009).
Suidae
In the family Suidae, two species had mating system data available (14% of species). One species, the wild boar (Sus scrofa), showed intraspecific variation in mating systems among populations. A genetic study of the mating system of wild boar in Chateau villain-Arc-en-Barrois
National Forest in France revealed a low level of polygyny in the population, with several
29 females mating with multiple males. The absence of dominant males, due to hunting pressure, could have broken up what used to be a highly polygynous system (Poteaux et al. 2009). A separate genetic study of wild boar in southwestern Australia found that males in the population fathered multiple litters. There was no evidence of multiple paternity within any litters indicating, a polygynous mating system (Hampton et al. 2004). Wild boar in Texas, USA, however, seem to exhibit a promiscuous mating system. Delgado-Acevedo et al. (2010) found evidence of multiple paternity in 33% of litters from seven different sampling sites. This, coupled with evidence of single males fathering multiple litters, indicated a promiscuous mating system (Delgado-Acevedo et al. 2010).
The remaining species, the warthog (Phacochoerus aethiopicus), showed only one type of mating system. In the Andries Vosloo Kudu Reserve in South Africa, male warthogs
(Phacochoerus aethiopicus) were found to mate with multiple females, and females mated with more than one male, indicating a promiscuous mating system (Somers et al. 1995).
Other Families
The only extant species in the family Antilocapridae, the pronghorn (Antilocapra americana), did exhibit intraspecific variation in mating systems among populations. At Sheldon
National Wildlife Refuge in Nevada, USA, there was no evidence of male pronghorn defending a territory. Instead, polygynous males were observed to defend a harem of females (Maher 1991).
Pronghorn at the National Bison Range in Montana, USA were observed to exhibit territorial defense polygyny. Males defended a territory from neighboring males, and mated with a group of females clustered on that territory (Byers and Kitchen 1988).
There was mating system data available for only one species in the family Camelidae.
Vicuñas (Vicugna vicugna) showed harem defense polygyny. Svendsen and Bosch (1993) observed breeding herds usually consisting of one resident male and three adult females.
30 Resident males were observed to defend a group of females from neighboring and bachelor males during the breeding season (Svendsen and Bosch 1993).
One species in the family Tayassuidae had information available on mating system (33% of species). A study on the genetic relationships of collared peccary in Texas, USA revealed a promiscuous mating system. After collecting tissue samples and genetically assigning parentage to offspring, it was found that multiple males within a herd sired offspring and that some litters had multiple sires. This evidence indicated a promiscuous mating system for collared peccary
(Cooper et al. 2011).
Information on the mating system was available for only one species in the family
Tragulidae (13% of species). The lesser mouse-deer (Tragulus javanicus) showed intraspecific variation in mating system within a population. Matsubayashi et al. (2006) studied the mating system of lesser mouse-deer using home rang overlap. The core areas for neighboring females and neighboring males were completely separate. Adult male-female pairs, however, had highly overlapping home ranges, suggesting a monogamous mating system. The core area of some females also overlapped with multiple males which may suggest a polygynous mating system
(Matsubayashi et al. 2006).
Summary of Artiodactyla Social Organization and Mating System
Only 14% of all extant artiodactyl species (32/221) had field data on both the social organization and mating system. Of those species, 25% (8/32 species) showed both intraspecific variation in social organization and mating systems, and 69% (23/32 species) showed IVSO only. Two species, Kirk’s dik-dik (Madoqua kirkii) and the lechwe (Kobus leche), showed a stable form of social organization (pair-living and group-living, respectively) and intraspecific variation in mating system (single-female defense polygyny and monogamy, and territorial defense polygyny and lekking, respectively) within and between populations.
31 Perissodactyla Social Organization
I found information on the social organization of 63% (10 of 16 species) of perissodactyls. Eighty percent of species (8/10) showed intraspecific variation in social organization, whereas one species was strictly solitary and one strictly group-living (Table 1.5).
Fifty percent of species were seasonal breeders. For seasonally breeding species, intraspecific variation in social organization occurred during the breeding season in one species, during the non-breeding season in one species, and during both the breeding and non-breeding seasons in three species.
Table 1.5 A Breakdown of Family-level Perissodactyla Social Organization Showing the Number of Species That Were Found to be Solitary, Pair-living, Group-living, or to Exhibit IVSO
Family Solitary Group-living IVSO Unknown
Equidae (n=7) - 1 5 1
Rhinocerotidae (n=5) - - 2 3
Tapiridae (n=4) 1 - 1 2 Note. n = total number of extant species; “-” indicates no data from the primary literature.
There was not a significant correlation between study effort (i.e., the number of studies reported and the number of populations studied) and the presence of intraspecific variation in social organization among perissodactyls. This is in contrast to the significant correlations found among artiodactyls. The remainder of this section focuses on describing the occurrence of intraspecific variation in social organization as well as stable social organizations within the three perissodactyl families.
32 Equidae
Of the seven extant species in the family Equidae, I was able to find social organization data for all species except one. Five species with social organization data showed intraspecific variation in social organization. The plains zebra (Equus burchellii) showed intraspecific variation in social organization both within and between populations. At the Ol Pejeta
Conservancy in Kenya, herds of plains zebra consisted of multiple harems of one adult male and multiple females (Fischhoff et al. 2007, Fischhoff et al. 2009). A five-year study of plains zebra at a wildlife reserve in Moolmanshoek, South Africa revealed that female-only groups were the main stable social unit for the population. Some female groups contained one or multiple adult males, whereas only one all-male group was observed during the study period (Simpson et al.
2012). The onager (Equus hemionus) is a seasonal breeder that exhibits intraspecific variation within a population. Klingel (1998) studied onager during the non-breeding season at the
Badchys Reserve in Turkmenistan. Almost all solitary individuals observed were adult males.
Onager were also found in groups of varying sizes. Smaller groups were male-only groups, female-only groups, or groups containing one adult male and multiple females. The larger groups contained multiple males and multiple females (Klingel 1998).
One species, the mountain zebra (Equus zebra), was categorized as group-living, showing a single form of social organization. In two separate populations of South African mountain zebra, one in De Hoop Nature Reserve and the other in Mountain Zebra National Park, breeding herds consisting of one adult male and multiple adult females were the main form of social organization (Penzhorn 1982, Penzhorn 1984, Lloyd and Rasa 1989, Smith et al. 2008). Male- only bachelor groups were also observed; however, these groups consisted of young males that could not hold and defend a harem of females (Penzhorn and Novellie 1991).
33 Rhinocerotidae
There are five extant species in the family Rhinocerotidae, but social organization data was available for only two. Both species were found to exhibit intraspecific variation in social organization. The Indian rhino (Rhinoceros unicornis) exhibited intraspecific variation in social organization within a population. In the Chitawan Valley of southern Nepal, solitary males and solitary females were most commonly observed, and adult individuals rarely associated with adults of the same sex. However, there were sightings of male-only groups, female-only groups, and male-female pairs (Laurie 1982). The critically endangered black rhinoceros (Diceros bicornis) showed intraspecific variation both within and between populations. In Masai Mara
Game Reserve, the majority of black rhinos sighted were solitary individuals (Mukinya 1973).
Black rhinos at the Sweetwaters Rhinoceros Sanctuary in Kenya were found in adult male- female pairs, or in groups consisting of one adult male and multiple adult females (Tatman et al.
2000).
Tapiridae
There are four species within the family Tapiridae, but information on social organization was available for only two of the four species. Baird’s tapir, (Tapirus bairdii) is a non-seasonal breeder that was found to exhibit a solitary social organization. A study of Baird’s tapir in the northern region of Los Chimalapas in southeastern Mexico, found that individuals were solitary in 90% of observations (Perez-Irineo and Santos-Moreno 2016). The Asian tapir (Tapirus indicus) is a seasonal breeder, and was also found to exhibit intraspecific variation in social organization. Holden et al. (2003) studied Asian tapir during the non-breeding season at Kerinici
Seblat National Park, and observed solitary males and solitary females, as well as male-female pairs.
34 Perissodactyla Mating System
I found information on the mating system for 31% (5 of 16 species) of perissodactyls
(Table 1.6). Of species with available mating system data, only one species showed intraspecific variation in mating system. The four remaining species all exhibited a polygynous mating strategy. One of these four species exhibited single-female defense polygyny, whereas the other three species exhibited harem defense polygyny. Information on the mating systems for species within the family Tapiridae was not available.
Table 1.6 A Breakdown of Family-level Perissodactyla Mating System Classification Showing the Number of Species That Exhibit a Particular Mating System
Family Territorial Defense Harem Defense IVMS Unknown
Equidae (n=7) - 3 1 3
Rhinocerotidae (n=5) 1 - - 4 Note. n = total number of extant species; “-” indicates no data from the primary literature.
Equidae
Only one species in the family Equidae showed intraspecific variation in mating systems.
Two populations of wild asses (Equus asinus) were found to exhibit two different polygynous mating strategies. Moehlman (1998) found that, in an arid environment where resources were patchy, wild asses exhibited a territorial defense polygyny mating system. In a mesic environment where resources were more readily available, a separate population of wild asses showed a harem defense polygyny mating strategy (Moehlman 1998). The remaining three species with mating system data (Equus burchellii, E. caballus, and E. zebra) all exhibited a
35 harem defense polygynous mating system (Salter and Hudson 1982, Penzhorn 1984, Lloyd and
Rasa 1989, Cameron et al. 2003, Fischhoff et al. 2007, Kampmann et al. 2013).
Rhinocerotidae
Mating system information was available for only one species in the family
Rhinocerotidae, which did not exhibit intraspecific variation in mating system. A study on the critically endangered black rhino (Diceros bicornis) at the Save Valley Conservancy in
Zimbabwe revealed a single-female defense polygynous mating system (Garnier et al. 2001).
Summary of Perissodactyla Social Organization and Mating System
Out of the 16 extant species in the mammalian order Perissodactyla, only five species
(31%) had field data on both the social organization and mating system. Three species showed intraspecific variation in social organization but did not exhibit a variable mating system. One species, the mountain zebra (Equus zebra), did not show any variability in social organization or mating system. Only one species, the wild ass (Equus asinus), exhibited intraspecific variation in both social organization and mating system.
Discussion
This review highlights the importance of focusing on primary literature rather than secondary sources, and demonstrates that a consideration of intraspecific variation in comparative studies can better our understanding of Artiodactyla and Perissodactyla social systems. I found that only 18% of artiodactyl species showed a single form of social organization
(either solitary, pair-living, or group-living), whereas the majority (82%) showed intraspecific variation in social organization. Only 20% of perissodactyl species showed just one form of social organization, and 80% exhibited variable social organization.
36 My findings contrast with other analyses that relied heavily on secondary literature and did not consider intraspecific variation (Lukas and Clutton-Brock 2013). My literature review revealed that, although intraspecific variation in social organization is very common in both artiodactyls and perissodactyls, a surprisingly small percentage of species (5%) were reported as strictly solitary. In contrast to prior reports. Lukas and Clutton-Brock (2013) provided data on
187 artiodactyl species, 56% of which are categorized as solitary, with much of the data (72%) coming from secondary sources such as Walker’s Mammals of the World (Nowak 1999). These secondary sources tend to make generalized assumptions for entire genera based on one species when species-specific field data on social behavior is not available. My analysis suggests that reliance on such secondary sources that use taxonomic inference doesn’t always provide accurate data.
Comparative studies utilizing large datasets might feel pressure to achieve maximum taxonomic breadth for high profile journals and, thus, sacrifice quality of data for quantity.
Reliance on secondary source data, and the exclusion of information on intraspecific variation, could lead to spurious conclusions about the evolution of social systems. For example, Lukas and
Clutton-Brock (2013) reported on 90% of Eulipotyphla species (399/445), with >99% of species assigned a solitary social organization. However, Valomy et al. (2015) found reliable data on only 16 species in the primary literature, nine of which were social, whereas seven showed
IVSO. Similarly, Dalerum (2007) used a dataset that included intraspecific variation and found that the long-held hypothesis that social organization in carnivorans involved transitions from a solitary ancestor to various derived forms of group-living was not supported. Instead, an ancestor with variable social organization was found to be just as likely (Dalerum 2007). Thus, using datasets built from reliable primary source data that includes intraspecific variation is essential in gaining an accurate understanding of the social systems of any higher taxon.
37 Aside from this, the rarity of truly solitary species in my dataset may also be due to investigator bias, which favors the study of charismatic, social megafauna over traditionally cryptic, solitary species in the field of mammalian behavioral ecology. Although IVSO was relatively common in both orders examined in the present study, I was only able to find field data on social organization for 45% of artiodactyls and 63% of perissodactyls. Data on mating systems was even less available, with reliable information uncovered for only 16% of artiodactyl species and 31% of perissodactyls. In order to fully understand the evolution of mammalian social systems, it is necessary to have reliable field data on as many extant species as possible.
Only 25% of artiodactyl species with field data showed intraspecific variation in both social organization and mating systems and just one perissodactyl species showed both IVSO and IVMS. Thus, there is not enough data available to establish a clear link between IVSO and
IVMS. Intraspecific variation in mating system (present in 31% of artiodactyls with data and
31% of perissodactyls with data) appears to be less common in artiodactyls and perissodactyls than IVSO (present in 82% and 80%, respectively). However, this may be due to less intensive study of mating systems within these taxa. One only has to count and sex individuals to determine the social organization, but to classify mating systems one must observe who mates with who over a period of time, and perform genetic paternity analyses. To fully understand the diversity of Artiodactyla and Perissodactyla social systems, more observations on the social organization and mating systems of less commonly studied species is crucial.
By classifying species that show more than one form of social organization or mating system as exhibiting intraspecific variation, I have built a novel, high-resolution dataset that allows other researchers to extract more detailed information about the social systems of these species. Accounting for intraspecific variation permits researchers to use more accurate information to study the evolution of social systems.
38 CHAPTER II
ACCOUNTING FOR INTRASPECIFIC VARIATION TRANSFORMS
UNDERSTANDING OF ARTIODACTYL SOCIAL EVOLUTION
Introduction
Examining the evolution of animal social systems is a hallmark of behavioral ecology and is an important aspect to consider in species management and conservation. Understanding the diversity of animal social systems has been challenging because they are characterized by four interrelated components (Kappeler and van Schaik 2002, Kappeler 2018 in press): (i) social organization (i.e., the size, composition, and kin structure of groups), (ii) mating system (i.e., who mates with who), (iii) social structure (i.e., relationships that emerge from repeated interactions among group members and between solitary individuals), and (iv) the parental care system. These components are intimately linked with one another. For example, the number and spatial distribution of individuals comprising the social organization can directly constrain the mating tactics of those individuals (Kappeler and van Schaik 2002). Across mammals, there is remarkable interspecific variation in animal social organization and mating systems due to ecology and evolutionary history (Emlen and Oring 1977, Clutton-Brock 1989, Krause and
Ruxton 2002, Rubenstein and Abbot 2017). Sophisticated comparative analyses hold great potential to determine the extent to which this social variation is attributed to evolutionary history (phylogeny) or ecology (Kappeler 2018 in press).
Examining evolutionary transitions in social systems is important, because these transitions explain how the current diversity of social systems evolved from a single ancestral
39 state. There have been numerous attempts to examine the evolutionary transitions (i.e., the transitions from an ancestral social state to a more derived social state) in mammalian social organization (e.g., Dalerum 2007, Lukas and Clutton-Brock 2013, Kappeler and Fichtel 2016), but inconsistent results have emerged from these studies. For example, comparative studies of primates and carnivorans have suggested different evolutionary transitions in social organization.
In primates, it has been suggested that pair-living species evolved exclusively from solitary ancestors (Lukas and Clutton-Brock 2013), or from both solitary and group-living ancestors
(Shultz et al. 2011, Kappeler and Fichtel 2016). In carnivorans, the long-held hypothesis that social evolution involved transitions in social organization from a solitary ancestor to more derived forms of group living (solitary ancestor hypothesis; see Gittleman 1989, Creel 1995) has not been supported by at least one subsequent study (Dalerum 2007). Given these different conclusions, there remains a critical need to study the evolution of social organization in mammals to achieve a comprehensive understanding of the evolution of social systems as a whole.
Similar shortcomings exist for our understanding of mammalian mating systems. The ancestral mating system, and evolutionary transitions between different types of social organization in extant species were found to be taxon specific (Pérez‐Barbería et al. 2002, Shultz et al. 2011, Lukas and Clutton-Brock 2013, Mabry et al. 2013, Opie et al. 2013). For example, monogamy has been suggested as the ancestral mating system in the mammalian orders
Artiodactyla, Perissodactyla, and Proboscidea (Pérez‐Barbería et al. 2002). In contrast, Lukas and Clutton-Brock (2013) suggested that social monogamy in all non-human mammals resulted from 60 separate transitions from solitary ancestors, and that the ancestral state was polygynandry. In primates, there is evidence that the ancestral mating system was polygynandry, and that harem-polygyny and monogamy evolved late in primate evolution (Opie et al. 2013).
40 Inconsistent results in the study of mammalian social systems likely occurred because studies have relied on different datasets, methods of analysis, and conceptual frameworks
(Kappeler and Fichtel 2016, Kappeler 2018 in press). In some studies, confusing terminology or conflation of social organization and mating system terms complicated matters (Kappeler 2018 in press). For example, some studies have included cooperative breeders as socially monogamous species (Lukas and Clutton-Brock 2013), whereas others have used male-female pairs (social organization) to infer social monogamy (mating system) (e.g., Pérez‐Barbería et al.
2002, Shultz et al. 2011). Conflicting definitions of the main components of a social system can also lead to inconsistent results among comparative studies. Pérez‐Barbería et al. (2002) assumed that the ancestral mating system for Artiodactyla was monogamy; however, their definition of a monogamous species differs from that of many other studies. The above study defines a monogamous species as being found in groups during the breeding season of “one male and one or two adult females” (Pérez‐Barbería et al. 2002). This is in contrast to other studies which define monogamy as occurring when males and females mate with only one conspecific of the opposite sex during the breeding season (Clutton-Brock 1989, Kappeler and van Schaik
2002). Mating interactions between one male and more than one female would typically be classified as polygynous (Clutton-Brock 1989). Although social organization likely predicts the mating system to some extent, these components of the social system should not be studied together, but in separate comparative analyses using accurate and consistent definitions
(Kappeler 2018 in press).
Another problem is that intraspecific variation has not been considered in previous comparative studies, even though it is an important component of animal social systems.
Intraspecific variation in social organization (IVSO) is relatively common in mammals, occurring in Artiodactyla (Jarman 1974), Carnivora (Dalerum 2007), Eulipotyphla (Valomy et al.
41 2015), Primata (Yamagiwa et al. 2003, Agnani et al. 2018), and Rodentia (Maher and Burger
2011). Evidence for intraspecific variation in mating systems (IVMS) is less common than for social organization, though this may be due to less intensive study of mating systems across mammals. Social organization is generally easy to determine in the field by counting and sexing individuals. However, to classify mating systems, mating interactions must be observed over multiple breeding seasons, and genetic analyses should be conducted to assign paternity to offspring.
Ignoring intraspecific variation in social organization and mating systems in comparative studies can increase statistical type II error rates (Harmon and Losos 2005, Garamszegi 2014,
Sandel et al. 2016) and lead to spurious conclusions about social evolution (Kappeler 2014,
Schradin et al. 2018). For example, in carnivorans (Order Carnivora) and shrews (Order
Eulipotyphla) it was long believed that the ancestral state was solitary, but after taking intraspecific variation into account, a variable ancestral state was found to be equally likely
(Dalerum 2007, Valomy et al. 2015). Thus, the inclusion of data on intraspecific variation in comparative phylogenetic analyses will provide better insights into evolutionary transitions among social systems. Whereas previous tools for phylogenetic comparative analyses required a single trait value for each species, modern methods, such as phylogenetic mixed-effects models or measurement-error models (de Villemereuil and Nakagawa 2014, Garamszegi 2014), can easily incorporate intraspecific variation. As such, I incorporate IVSO in two ways: (i) different populations of the same species exhibiting different social organizations, resulting in variable social organization at the species level, and (ii) different populations of the same species exhibiting variable social organization within the populations themselves, i.e., population-level
IVSO (e.g., between breeding and non-breeding seasons, or in different habitats).
42 In comparison to morphological or physiological traits, social systems tend to have relatively weak phylogenetic signals (Blomberg et al. 2003, Kamilar and Cooper 2013, Strier et al. 2014, Kappeler 2018 in press), in that they tend to be less constrained by evolutionary history and respond more flexibly to current ecology (but see Difiore and Rendall 1994, Thierry 2013).
This might be attributable to the fact that social systems are the joint product of evolved individual social tactics which, in turn, are often context dependent. That is to say, a species’ evolutionary history may have contained a range of environments with a corresponding range of optimal social strategies (Jaeggi et al. 2016). If this is true for the evolution of mammalian social systems, then factors influencing the extent to which individual social tactics are expected to be context dependent (e.g., habitat heterogeneity and seasonality of breeding) also need to be incorporated into comparative studies (Lukas and Clutton-Brock 2017).
Intraspecific variation in social organization may have evolved in instances where flexible social organization allowed individuals to respond to harsh or unpredictable ecological conditions (Schradin 2013). Intraspecific variation in group size and composition is also expected in seasonal breeders. During the breeding season, reproductive competition can cause the exclusion of some individuals from groups, changing group composition and thus causing intraspecific variation in social organization. Alternatively, relaxed or reduced competition during the non-breeding season may allow for the formation of larger groups, particularly if grouping has survival benefits (e.g., anti-predator behavior; see Hamilton 1971, Jarman 1974,
Van Schaik 1983). Thus, I expect greater variability in social organization than in mating systems among seasonal breeders.
The mammalian order Artiodactyla (even-toed ungulates) is a good taxonomic group for investigating evolutionary transitions in social organization and mating system because it is characterized by diversity in social systems, ecology, and body sizes (Jarman 1974). Habitat
43 heterogeneity and availability of protective cover are associated with intraspecific variation in social organization of many artiodactyls, with group sizes being small in areas of dense vegetative cover and large in open areas with high visibility (Jarman 1974, Hirth 1997). These factors are also associated with intraspecific variation in mating systems among artiodactyls, with non-territorial, harem-defense polygyny found in open habitats and single territorial systems common in closed forested habitats (Langbein and Thirgood 1989). Sexual dimorphism and seasonal breeding, common in artiodactyls, are also associated with variation in social systems
(Pérez‐Barbería et al. 2002). Many species are sexually dimorphic, living in unisex groups or as solitary individuals most of the year, but forming mixed sex groups during the breeding season
(Ruckstuhl and Neuhaus 2002, Mooring et al. 2005, Loe et al. 2006, Ruckstuhl and Neuhaus
2009), but see (Clutton-Brock et al. 1982, Kie and Bowyer 1999). Monomorphic species may live alone, in pairs, or in mixed sex groups (Ruckstuhl and Neuhaus 2009).
The main goals of this study were to determine the ancestral state and evolutionary transitions in the social organization and mating systems of artiodactyls, using a dataset that accounts for intraspecific variation, and to investigate the potential drivers of this variation
(Table 2.1). This allowed me to re-evaluate the following hypotheses about the phylogeny of artiodactyl social systems: (i) the ancestral mating system was social monogamy, which then transitioned to greater polygyny (Jarman 1974, Pérez‐Barbería et al. 2002), and (ii) the ancestral social organization was pair-living, with a transition to greater sociality (Lukas and Clutton-
Brock 2013). My hypothesis, in contrast, is that the ancestral state was variable (i.e., exhibiting more than one form of social organization), with subsequent transitions to more specific social organizations (e.g., group-living only, Dalerum et al. 2006, Dalerum 2007). Since habitat type and sexual dimorphism are thought to be linked to IVSO and IVMS (Jarman 1974, Pérez‐
Barbería et al. 2002) I considered these factors as well. Finally, I tested whether the same factors,
44 as well as seasonal breeding (which can lead to seasonal sexual segregation) could lead to intraspecific variation (Table 2.1).
Table 2.1 A Breakdown of the Hypotheses and Predictions for Phylogenetic Reconstruction of Artiodactyla Ancestral Social Organization and Mating Systems as Well as Ecological and Life History Predictors of IVSO and IVMS
Hypothesis Prediction Supported? Objective 1: Determine ancestral social organization state ancestral social organization was pair-living H1a: Pair-living ancestral with a transition to greater sociality (Pérez‐ Ø state Barbería et al. 2002) H1b: Variable ancestral ancestral state was variable with transitions to P state more specific social organizations Objective 2: Ecological and life history predictors of IVSO more variable social organization in species H2: Seasonal Breeders Ø with seasonal breeding variable social organization increases with H3: Sexual Dimorphism Ø increasing male:female body mass ratio more variable social organization in species H4a: Habitat Breadth Ø using multiple habitats less variable social organization in species H4b: Closed Habitats using closed forest habitats than in species P using open habitats Objective 3: Determine ancestral mating system state ancestral mating system was social monogamy H5a: Monogamous with transitions to polygyny (Pérez‐Barbería et Ø ancestral state al. 2002) H5b: Variable ancestral ancestral state was variable with transitions to Ø state more specific mating systems Objective 4: Ecological and life history predictors of IVMS variable mating system increases with H6: Sexual Dimorphism Ø increasing male:female body mass ratio more variable mating system in species using H7: Habitat Breadth multiple habitats than in species using one Ø habitat
45 Methods
Social Organization and Mating System
Searches were conducted using Web of Science and Google Scholar to find primary literature reporting the social organization and mating system for all 221 extant species in the order Artiodactyla (Wilson and Reeder 2005). Domesticated species were not considered in this study due to potential human influence and manipulation of social systems. I did not include the order Perissodactyla in the study because there was notably less data available on the social organization and mating systems of the sixteen perissodactyl species in comparison to the artiodactyls. The initial search consisted of the scientific name (genus and species) and a keyword (‘social’, ‘herd’, or ‘group’ for social organization searches and ‘polygyny’,
‘monogamy’, ‘polyandry’, and ‘mating system’ for mating system searches). If no primary literature reporting social organization or mating system was found during the first searches, a final search using the scientific name only was conducted. In Web of Science, search results were refined by selecting for three research areas: “zoology”, “behavioral science”, and
“environmental science/ecology”, and by document type: “article”. Rather than relying on older datasets that gleaned information from a variety of primary and secondary sources, my dataset was built from primary literature only with very stringent criteria. Lab-based studies, studies conducted in outdoor enclosures smaller than 1,000-hectares that restricted individual movements, and studies that included manipulation of individuals, groups, or resources, were discarded.
Adult (i.e., sexually mature) male-female social organization was indexed by recording the number of adult males and/or adult females per social unit or group. As a result, there were seven possible social organization categories: (i) solitary adult (male or female), (ii) adult male- female pair (MF), (iii) multiple adult females and one adult male (FFM), (iv) one adult female
46 and multiple adult males (FMM), (v) multiple adult females and multiple adult males (FFMM),
(vi) multiple adult males only (MM), and (vii) multiple adult females only (FF). For the purposes of this analysis, I grouped these into solitary (solitary males or females), pair-living (adult male- female pairs), group-living (all others), and variable (includes presence of more than one of the categories i-vii described above). Solitary dispersing individuals were not included in the categorization of social organization. A species was categorized as exhibiting intraspecific variation in social organization if more than one social organization category was reported for that species. Intraspecific variation in social organization was recognized only when both sexes had more than one form of social organization.
Mating systems reported for each species were categorized into one of four categories: (i) monogamy, (ii) polyandry, (iii) promiscuity, or (iv) polygyny. Polygynous systems, in which males mate with several females, were further broken down into four more categories: (i) territorial defense, (ii) harem defense, (iii) single-female defense, or (iv) lekking systems.
Compared to social organization, mating systems are less commonly reported in the literature. I included mating system studies that detailed individual interactions and copulations in the field during the breeding season, genetic studies that assigned paternity to offspring, and studies that reported home range overlap of males and females during the breeding season. Thus, I pooled reports based on social interaction, home range overlap, and genetics. A species was categorized as exhibiting intraspecific variation in mating system if more than one mating system was reported for that species. Presence of intraspecific variation in social organization and mating system was recorded as occurring within one study population, between separate populations, or both within and between populations.
47 Ecology and Life History
Every species was categorized as either a seasonal or non-seasonal breeder based on author-defined seasonality categorizations. For seasonal breeders, social organization was recorded to occur during the breeding season, non-breeding season, or during both breeding and non-breeding seasons. The extent of sexual dimorphism was indexed by the ratio of male to female body mass, using data reported in Pérez-Barbería and Gordon (2000). Mean female body mass was also taken from Pérez-Barbería and Gordon (2000) and included as a predictor, since body size influences the strength of feeding competition and risk of predation, as well as available anti-predation strategies (such as grouping to mitigate and dilute predation risk, or remaining solitary and cryptic to avoid detection), and thus influences social organization and, possibly, mating systems (Van Schaik and Van Hooff 1983). For all populations, the habitat type was derived from the primary source and categorized based on the International Union for
Conservation of Nature (IUCN) classification scheme (IUCN 2018) as desert, forest, rocky areas, savannah, grassland, shrubland, wetlands, or artificial (e.g., agricultural land). To control for the influence of study effort on the reporting of intraspecific variation, the number of studies reporting social organization or mating systems and the number of populations studied was recorded for each species and accounted for in the phylogenetic analyses.
Phylogeny
I used the mammal supertree from Bininda-Emonds et al. (2007) to capture the evolutionary history of artiodactyls. Dedicated phylogenies for Artiodactyla are available through the 10ktrees project (Arnold et al. 2010); however, these trees are not ultrametric (i.e., all paths from the root of the tree equal in length) as required by phylogenetic comparative analyses, and would first have to be dated using known age constraints. As the mammal super- tree is commonly used in comparative analyses (e.g., Lukas and Clutton-Brock 2012) I saw no
48 issue with using it. The species names in the database had to be slightly amended to match the phylogeny. In all cases, a name mismatch could be resolved by finding a pseudonym for that species through www.iucn.org (IUCN 2018), or by using a sister species that was not included in the database. The latter happened once in which two closely-related taxa missing from the supertree (Moschus leucogaster and Moschus cupreus) were proxied by the same sister species
(Moschus chrysogaster). This does not pose a problem for the phylogenetic mixed-effects model, but for the cruder species-level ancestral state estimation, one of the two had to be deleted. Since they were categorized as having the same social organization, this made no difference in the results obtained.
Statistical Analysis
I conducted both a crude ancestral state estimation using species-level data, as well as a more rigorous phylogenetic mixed-effects model estimation using population-level data. The latter better incorporates the high-resolution nature of the dataset (e.g., data on several populations of the same species), and allowed me to incorporate various predictor and control variables. In addition to the predictors mentioned above, the models controlled for the influence of study effort, by including the number of studies covering social organization and mating system, respectively. To control for potential geographical biases in research on artiodactyls, or unmeasured ecological similarity influencing social organization or mating systems, the continent where each study was conducted was included as a random effect. All statistical analyses were done with the help of Dr. Adrian Jaeggi, assistant professor in the Department of
Anthropology at Emory University in Atlanta, Georgia, USA.
Ancestral state estimation of species-level traits was conducted using the ape package v.
5.2. (Paradis et al. 2004) in the R statistical program v. 3.5.1. (R Development Core Team 2015).
Ape uses maximum likelihood estimation for discrete traits, and restricted maximum likelihood
49 estimation for continuous traits. Phylogenetic mixed-effects models incorporate intraspecific variation by treating the individual, or in this case, the population, rather than the species, as the unit of analysis (de Villemereuil and Nakagawa 2014, Garamszegi 2014). Expected variation among species is captured by a variance-covariance matrix based on a phylogeny, and a species- level random effect captures the extent to which populations of the same species resemble each other. Predictors and controls are easily included as fixed effects, and additional random effects can be added. For this study I treated habitat and continent of origin as random effects.
Furthermore, I used multinomial distributions for modeling the likelihood of several mutually exclusive categorical traits (i.e., different social organizations or mating systems; Koster and
McElreath 2017) and for determining how the likelihood of each trait would be affected by other variables in the model.
The global intercept in a phylogenetic regression model represents the ancestral state, or in this case, the likelihood of different social organizations or mating systems being assigned to the root of the tree. Since the intercept estimate depends on other variables in the model, I standardized all predictors such that the intercept represented a non-seasonally breeding species of average female body size, with no sexual dimorphism, that lived in one habitat and was included in one study. Coefficients represent changes in the probability of different social organizations or mating systems in seasonal vs. non-seasonal breeders when changing sexual dimorphism or female body size by one standard deviation, or when adding one habitat type or one study. I highlighted any covariates that significantly influenced the likelihood of different social organizations or mating systems and my inferences about the ancestral state.
Highly parameterized models with non-Gaussian distributions are best estimated within a
Bayesian framework (McElreath 2018). I fit all models in Stan (Carpenter et al. 2017) through the RStan interface (Stan Development Team 2018) using the brms package v. 2.5.1. (Bürkner
50 2017). Bayesian estimation produces a posterior probability distribution for each parameter, and these distributions can be summarized in various ways. Here I report the mean and 95% confidence intervals (CI), as well as what proportion of the distribution lies above or below a certain value. I considered associations as “significant” if the 95% CI does not include zero. I plotted random samples drawn from the posterior (see Figure 2.3) in some instances, and the entire posterior distributions in others (see Figure 2.4).
Results
Occurrence of Intraspecific Variation in Social Organization
Of the 221 extant Artiodactyla species, I found field data on the social organization for
100 species (45%). Almost all species with social organization data showed intraspecific variation in social organization (82%), whereas five species (5%) were strictly solitary, only one was strictly pair-living (1%), and twelve species were strictly group-living (12%). I also found social organization data for 218 different populations. Eighty-five percent (187/218) of all populations showed variable social organization. Most species with variable social organization showed IVSO both within and between populations (61%), whereas 39% of variable species showed variable social organization within a particular population. This suggests that intraspecific variation in social organization was not just due to differences in social organization among different populations, but due to variable social organization at the population level.
Phylogenetic Reconstruction of Ancestral Social Organization State and Factors Influencing
IVSO
A species-level ancestral state estimation for discrete traits with no covariates showed that almost all probability (99.9%) for ancestral social organization was assigned to “variable” with <0.1% assigned to “solitary” and “group-living” respectively (Figure 2.1). For my analysis,
51 “pair-living” is included in the “group-living” category because only one artiodactyl species,
Kirk’s dik-dik (Madoqua kirkii), was classified as exclusively pair-living.
Figure 2.1 A simple ancestral state estimation using discrete traits that predicts a variable ancestral social organization state (99.9%) over a solitary or group-living state (<0.1%) of Artiodactyla
52 The phylogeny in Figure 2.1 was based on Bininda-Emonds et al. (2007). Only species with data on social organization were included in the reconstruction.
The phylogenetic mixed-effects model analyzing social organization at the population level had intercepts that reflected a non-seasonally breeding species of average body size and no sexual dimorphism, that lived in only one habitat, and was studied once. An ancestral population with these characteristics was predicted to have a variable social organization (i.e., exhibiting more than one form of social organization) with much higher probability (0.84, 95% CI = 0.51 –
1.00) than a non-variable form (i.e., solitary or group-living; Figure 2.2). The only variables found to significantly alter the expected probability of a given social organization were (i) the number of studies, which increased the probability of variable social organization, and (ii) female body mass, which predicted less variable social organization in larger species (Figure
2.3).
53 Figure 2.2 A graphical comparison of the probability of solitary, group-living, and variable social organization at the ancestral node of all Artiodactyla
Figure 2.2 shows the probability of solitary (0.12, 95% CI = 0.00 – 0.36), group-living
(0.04, 95% CI = 0.00 – 0.20), and variable (0.84, 95% CI = 0.51 – 1.00) social organization.
54 Figure 2.3 A chart showing the probability of an artiodactyl population exhibiting more than one form of social organization relative to female body mass; the solid line represents the predicted mean, whereas the thin lines show 100 random samples drawn from the posterior distribution to illustrate the degree of uncertainty
Examining the random intercept for variable social organization by habitat type (Figure
2.4), forest habitats had a lower probability of variable social organization, with 82% of the posterior distribution falling below the global average. Nevertheless, even in forest habitats the probability of variable social organization was high (0.79, 95% CI = 0.28 – 0.99). Seasonality in breeding and sexual dimorphism did not influence the probability for populations to show variable social organization or other forms of stable social organization (i.e., solitary or group- living). The probability of finding variable social organization for a species that occupies multiple habitats did not deviate from the global average.
55 Figure 2.4 Posterior distributions of the habitat level random intercepts (zero indicates the global average in the probability of variable social organization)
The phylogenetic mixed-effects model analyzing the number of social organizations showed that the predicted number of forms of social organization for the ancestor of all
Artiodactyla was 2.57 (95% CI = 1.93 – 3.37; Figure 2.5). For this analysis, no variable significantly influenced the number of social organizations at the ancestral state.
56 Figure 2.5 A diagram showing the number of social organizations per species in the artiodactyl phylogeny
The phylogeny in Figure 2.5 was based on Bininda-Emonds et al. (2007). Only species with data on social organization were included in the reconstruction. The mean number of social organizations at the ancestral state was 2.57 (95% CI = 1.93 - 3.37) and was significantly greater than one social organization.
57 Occurrence of Intraspecific Variation in Mating System
I found field data reporting the mating system for 16% (36/221 species) of artiodactyl species. Eleven species (31% of those with data) showed intraspecific variation in mating system, nineteen species (53%) showed some form of polygyny, five species were promiscuous
(14%), and one species was exclusively monogamous (3%). I also found data on the mating system of 52 different populations. Nineteen percent (10/52) of all populations with mating system data showed intraspecific variation in mating system. Species with variable mating systems showed intraspecific variation in mating system within a population (20% of variable species) as well as both within and between populations (50% of variable species).
Phylogenetic Reconstruction of Ancestral Mating System State and Factors Influencing IVMS
In contrast to social organization, a clear ancestral mating system state could not be resolved for Artiodactyla with polygyny (43.0%), promiscuity (24.3%), variable (20.9%), and monogamy (11.8%) all receiving some support (Figure 2.6). It is noteworthy that monogamy, the previously hypothesized ancestral mating system for Artiodactyla (Pérez‐Barbería et al. 2002), was the least strongly supported ancestral mating system in this analysis. The number of different mating systems in the last common ancestor (Figure 2.7) was estimated to be either one or two (1.33, 95% CI = 0.54 – 2.13). None of the covariates significantly altered the probability of a given mating system. The majority of the posterior probability mass supported a positive associated between polygyny and sexual dimorphism (78.1%) and between promiscuity and dimorphism (79.8%).
58 Figure 2.6 A diagram showing the probability of polygyny (43.0%), promiscuity (24.3%), variable (20.9%), or monogamy (11.8%) mating system at the ancestral node of all Artiodactyla
The phylogeny in Figure 2.6 was based on Bininda-Emonds et al. (2007). Only species with data on social organization were included in the reconstruction.
59
Figure 2.7 A diagram showing the number of mating systems per species in the artiodactyl phylogeny
The phylogeny in Figure 2.7 was also based on Bininda-Emonds et al. (2007). Only
species with data on social organization were included in the reconstruction. The number of
60 mating systems at the ancestral state was estimated to be either one or two (1.33, 95% CI = 0.54
– 2.13).
Discussion
Phylogenetic Reconstruction of Artiodactyla Social Organization and Mating System
The classical descriptive study on the social organization of antelope by Jarman (1974) greatly influenced the field of behavioral ecology (Wilson 1975, Krebs and Davies 1981,
Drickamer et al. 1996, Krebs and Davies 2009). This study suggested that ancestral artiodactyls were monogamous, pair-living species which utilized closed habitats (i.e., forests) and subsequently transitioned to more polygynous, group-living species exploiting open habitats.
While this hypothesis was statistically tested and confirmed by Pérez‐Barbería et al. (2002), my study could not confirm these results, nor those of other comparative studies which suggested a solitary social organization as ancestral for Artiodactyla (Lukas and Clutton-Brock 2013).
Instead, a variable form of social organization emerged as the ancestral state, and as the most common current form of social organization among extant artiodactyls. I was unable to resolve the ancestral mating system of Artiodactyla, but my analysis found the least support for monogamy as the ancestral state. This indicates that the assertion by Pérez‐Barbería et al. (2002), that monogamy was the most likely ancestral state for all Artiodactyla, may not be accurate.
Inconsistencies among comparative studies likely occur because studies have relied on different datasets (some with heavy reliance on secondary source data; see Lukas and Clutton-
Brock 2013), methods of analysis, and conceptual frameworks. Moreover, misleading definitions and failure to separately analyze social organization and mating system can lead to disparate, and even faulty conclusions. Whereas the evolutionary transitions suggested by Jarman (1974) were statistically tested and confirmed by Pérez‐Barbería et al. (2002), the latter study had to rely on
61 an unresolved phylogeny and statistical methods constrained to discrete data, excluding much available information, such as intraspecific variation, in addition to inconsistent definitions for the main components of a social system. For example, species living “groups of one male and one or two females” were categorized as monogamous, whereas everything else was considered polygynous (Pérez‐Barbería et al. 2002). My study used a better resolved phylogeny and improved comparative methods to determine evolutionary transitions in artiodactyl social organization and mating system.
Other comparative studies used datasets that have relied heavily on information from secondary sources to achieve maximum taxonomic breadth. Some commonly used secondary sources (e.g., Walker's Mammals of the World; Nowak 1999) assume the same social organization for all species in a particular genus, based on data available for only one species.
These types of generalizations about social behavior at the species level can lead to inaccurate conclusions when used in comparative studies. For example, Lukas and Clutton-Brock (2013) used a database, which was often based on secondary literature, that reported data on 90% of
Eulipotyphla (399/445), with >99% of species categorized as solitary. In contrast, Valomy et al.
(2015) found reliable data for only 16 species using the primary literature. Of these species, nine
(56%) were social, and the remaining seven species showed intraspecific variation in social organization (Valomy et al. 2015). These results, combined with my own, show that including intraspecific variation in comparative analyses is important and can provide new insights into the evolution of social systems.
My study focused on resolving the ancestral social organization and mating system at the basal node for artiodactyls in order to illustrate how including intraspecific variation in comparative analyses can change what was previously understood about the evolution of social systems. Now that the ancestral social organization state has been addressed, future research can
62 expand these analyses to look at the ancestral state for different families of artiodactyls.
Although my species-level analysis found a high probability for a variable social organization state at virtually all nodes, that analysis used categorical data and did not account for any of the predictor or control variables. A future analysis that focuses on a family-level reconstruction could reveal that some artiodactyl families are more likely to show intraspecific variation in social organization than others.
Ecological and Life History Predictors of IVSO and IVMS
There are four recognized processes that have the potential to lead to IVSO: (i) genetic variation, (ii) developmental plasticity, (iii) social flexibility, and (iv) extrinsic factors, or environmental disrupters (Schradin 2013). Environmental disrupters, such as the death of a dominant breeder, lead to non-adaptive changes in social organization. Such changes are not due to an individual’s adaptive response to environmental change (Schradin 2013). In my analysis, the high probability that the ancestral artiodactyl population showed more than two social organizations suggests that this variation is not simply due to an environmental disrupter.
Social flexibility is expected to evolve as an adaptation to unpredictable environments.
Thus, one should expect to see more variable social organization in populations that experience high variability and unpredictability in temperature and rainfall (Schradin 2013). I was not able to get population-specific rainfall and temperature data for this study, so I used the utilization of multiple habitat types as a proxy. My analysis did not show that populations which utilized more than one habitat had a higher probability of exhibiting intraspecific variation in social organization. I did find, however, that artiodactyls living in forested habitats had an 82% probability of having less variable social organization than the global average. This supports observations in the literature that species utilizing forest habitats (high coverage habitats) are typically small, solitary species, whereas species inhabiting open areas are more often larger-
63 bodied, group-living species (Jarman 1974). A less variable social organization may be more advantageous in habitats with a high percentage of cover, or low visibility, as it is easier for solitary, cryptic individuals to conceal themselves from predators than it is for groups of varying size.
My analysis found body size to be the most important life history predictor of IVSO.
Variability in social organization decreased significantly with increasing female body mass.
While surprising, this last finding is interesting because of its link to predation risk and anti- predator strategies, and how these might constrain available social organization. Large bodied artiodactyls are typically found in more open habitats (Jarman 1974), and larger species in these habitats that cannot avoid predation by being cryptic (i.e., having coloration or features that allow an animal to blend in with its natural surroundings) might be constrained to group together permanently. For example, group size in Alaskan moose (Alces alces gigas) is positively correlated with distance from cover (Molvar and Bowyer 1994). This suggests that grouping of individuals in open habitats is an anti-predation strategy and an adaptation to avoid predation risk.
None of the covariates (sexual dimorphism, seasonal breeding, habitat type) significantly altered the probability of a species exhibiting a given mating system. This is somewhat surprising, especially in the case of sexual dimorphism, which is generally thought to be associated with increased male intrasexual competition in polygynous or promiscuous mating systems (Clutton-Brock et al. 1977, Alexander et al. 1979). This lack of support for any of the hypothesized predictors of IVMS may be due to the paucity of field data on artiodactyl mating systems. Intraspecific variation in social organization (82% of species) was more common than intraspecific variation in mating system (31% of species) in artiodactyls. This may also be due to less intensive study of artiodactyl mating systems. It is relatively easy to count and sex
64 individuals in the field to report social organization. However, to classify mating systems, long- term study of populations during the breeding season and genetic paternity analyses are required.
Limitations
One limitation of this study stems from potential observer error in the primary literature from which the social organization and mating system data was collected. Misidentification of the sex of individuals or the composition of groups by primary researchers could have inaccurately represented the social organization of a population. Similarly, field observations on the social mating system could differ from the actual genetic mating system of a population. For example, based on an observation of male-female pairs during the breeding season a researcher might assume a monogamous mating system; however, a genetic study might reveal a single- female defense polygynous system.
Another limitation of this study is the use of categorical data. Fitting species into categories with precise definitions may not accurately represent the social systems of these species because most behaviors are known to exist along a continuum. Now that variability in social organization and mating systems has been shown to be relatively common in artiodactyls and perissodactyls, future research would benefit from the establishment of a categorial scale of variability. This would allow us to distinguish between species that exhibit both solitary and group-living (e.g., solitary males and females, and single male/multiple female groups in the same population) and species that show variability in group-living social organizations (e.g., single-male/multiple female groups, multiple male-multiple female groups, male-only and female-only groups in the same population). Using discrete categories and simple descriptions of mating systems (e.g., monogamy, polygyny, promiscuity, etc.) is valuable in order to capture the potential variability in mating systems a species or population exhibits. Once a baseline for variability has been established, other factors such as sex-specific variation in mating success can
65 also be considered to gain a full understanding of the mating system and the allocation of reproductive success within a population or group.
Need for Long-term Studies and Manipulative Field Studies
A clear understanding of a species’ social system requires information from long-term studies that track known individuals and monitor changes in social organization and mating systems. The definition of a long-term study depends on the life history of the study organism, but can generally be defined as studies with more than 10 consecutive years of data on the same population (Clutton-Brock and Sheldon 2010, Hayes and Schradin 2017). Festa-Bianchet et al.
(2017) identified only 24 such long-term studies on artiodactyls. The majority of these observed only one population per species. A geographic bias was evident, with all these long-term studies taking place in either North America or Europe (Festa-Bianchet et al. 2017). In long-lived species such as artiodactyls, long-term studies can inform us about how ecological conditions influence dispersal, philopatry, and other demographic factors (e.g., mortality, growth rates, etc.) that affect sociality. Long-term studies can also provide insights on how the social organization and mating system of a population can change over time in response to different environmental conditions.
More field studies on multiple populations that include long-term monitoring of known individuals and populations, as well as recording of ecological variables (e.g., habitat breadth, rainfall, temperature, food availability, predator density, etc.) are essential to identify the mechanisms and factors influencing intraspecific variation in social organization and mating systems (Schradin et al. 2018). Since many artiodactyl species and populations are heavily influenced by human exploitation and sustainable hunting as a form of population control, field data on population densities and population structure are also needed (Festa-Bianchet et al.
2017). Thus, long-term studies are essential to understand and predict how populations will
66 respond to continued human exploitation, as well as changing environmental conditions due to recent global climate change.
Manipulative studies can also provide valuable insights into which of the four mechanisms mentioned previously could be leading to IVSO in a particular population. It is predicted that all three adaptive mechanisms (i.e., genetic variation, developmental plasticity, and social flexibility) that can lead to IVSO evolved in response to environmental variation
(Schradin 2013). Experimental manipulation is the best way to determine whether IVSO is caused by variation of a particular environmental factor. For example, a long-term study of striped mice (Rhabdomys pumilio) found that social organization was influenced by variation in population density during the breeding season (Schradin et al. 2010). A subsequent study confirmed that striped mice switch from group-living to solitary-living in response to an experimental reduction in population density during the breeding season (Schoepf and Schradin
2012). Thus, both long-term studies and manipulative studies help explain the cause of intraspecific variation in social organization in some populations.
Conservation Implications and Concluding Remarks
It is predicted that all three adaptive mechanisms that lead to IVSO evolved in response to environmental variation (Schradin 2013). Genetic variation is thought to evolve more commonly in predictable environments with environmental variation among populations.
Developmental plasticity is more likely to evolve in environments characterized by predictable environmental variation within a population (e.g., El Niño-Southern Oscillation (ENSO) events), and social flexibility is predicted to evolve as a response to unpredictable environments with recurring environmental variation (Schradin et al. 2018). Of the three adaptive mechanisms, social flexibility alone allows for adaptation to an environment that fluctuates unpredictably. It is important to know the limits of social flexibility in the face of recent global climate change
67 which might lead to changes in environmental conditions at a rate to which individuals can no longer adapt.
The results of my study reveal that the majority of artiodactyl species for which there is field data show intraspecific variation in social systems, and that the likely ancestral state for artiodactyls was variable social organization. This study provides novel insights into the evolution of mammalian social systems and illustrates the importance of including intraspecific variation in future comparative analyses. My dataset, with its inclusion of intraspecific variation, will allow other researchers to extract more detailed information about the social systems of these species, and to study the evolution of social systems from a new perspective. Field studies that include long-term monitoring of known individuals and recording of site-specific ecological variables for the remaining artiodactyl species are necessary to fully understand the evolution of artiodactyl social systems and its implications for conservation. The monitoring and reporting of these factors can inform conservation and species management efforts and help us understand how and whether a species can adapt to changing environments in the face of recent global climate change.
68 REFERENCES
Acebes, P., J. E. Malo, and J. Traba. 2013. Trade-offs between food availability and predation risk in desert environments: The case of polygynous monomorphic guanaco (Lama guanicoe). Journal of Arid Environments 97:136-142.
Adamczak, V. G., and R. I. M. Dunbar. 2008. Variation in the mating system of oribi and its ecological determinants. African Journal of Ecology 46:197-206.
Agnani, P., C. Kauffmann, L. D. Hayes, and C. Schradin. 2018. Intra‐specific variation in social organization of Strepsirrhines. American Journal of Primatology 80:e22758.
Agnarsson, I., and L. J. May-Collado. 2008. The phylogeny of Cetartiodactyla: The importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies. Molecular Phylogenetics and Evolution 48:964-985.
Alexander, R. D., J. L. Hoogland, R. D. Howard, K. M. Noonan, and P. W. Sherman. 1979. Sexual dimorphisms and breeding systems in pinnipeds, ungulates, primates, and humans. Evolutionary Biology and Human Social Behavior: An Anthropological Perspective. North Scituate, MA. Duxbury Press. 402-435. Allsopp, R. 1979. Roan antelope population in the Lambwe Valley, Kenya. Journal of Applied Ecology 16:109-115.
Alves, J., A. A. da Silva, A. M. V. M. Soares, and C. Fonseca. 2013. Sexual segregation in red deer: is social behaviour more important than habitat preferences? Animal Behaviour 85:501-509.
Andanje, S. A., and W. K. Ottichilo. 1999. Population status and feeding habits of the translocated subpopulation of Hunter's antelope or hirola (Beatragus hunteri, Sclater, 1889) in Tsavo East National Park, Kenya. African Journal of Ecology 37:38-48.
Anzenberger, G., and B. Falk. 2012. Monogamy and family life in callitrichid monkeys: deviations, social dynamics and captive management. International Zoo Yearbook 46:109-122.
Apio, A., M. Plath, R. Tiedemann, and T. Wronski. 2007. Age-dependent mating tactics in male bushbuck (Tragelaphus scriptus). Behaviour 144:585-610.
Apollonio, M., S. Focardi, S. Toso, and L. Nacci. 1998. Habitat selection and group formation pattern of fallow deer Dama dama in a submediterranean environment. Ecography 21:225-234.
69 Arcese, P., G. Jongejan, and A. R. E. Sinclair. 1995. Behavioral flexibility in a small African antelope - group size and composition of the oribi (Ourebia ourebi, Bovidae). Ethology 99:1-23.
Argunov, A. V., and V. M. Safronov. 2013. Demographic structure of Siberian roe deer (Capreolus pygargus Pall.) population in central Yakutia. Russian Journal of Ecology 44:402-407.
Arnold, C., L. J. Matthews, and C. L. Nunn. 2010. The 10kTrees website: a new online resource for primate phylogeny. Evolutionary Anthropology: Issues, News, and Reviews 19:114- 118.
Averbeck, C., M. Plath, T. Wronski, and A. Apio. 2012. Effect of human nuisance on the social organisation of large mammals: group sizes and compositions of seven ungulate species in Lake Mburo National Park and the adjacent Ankole Ranching Scheme. Wildlife Biology 18:180-193.
Bagchia, S., S. P. Goyal, and K. Shankar. 2008. Social organisation and population structure of ungulates in a dry tropical forest in western India (Mammalia, Artiodactyla). Mammalia 72:44-49.
Balmford, A., S. Albon, and S. Blakeman. 1992. Correlates of male mating success and female choice in a lek-breeding antelope. Behavioral Ecology 3:112-123.
Barrette, C. 1977. Some aspects of behavior of muntjacs in Wilpattu National Park. Mammalia 41:1-34.
Bartos, L., P. Sustr, P. Janovsky, and J. Bertagnoli. 2003. Sika deer (Cervus nippon) lekking in a free-ranging population in Northern Austria. Folia Zoologica 52:1-10.
Baskaran, N., V. Kannan, K. Thiyagesan, and A. A. Desai. 2011. Behavioural ecology of four- horned antelope (Tetracerus quadricornis de Blainville, 1816) in the tropical forests of southern India. Mammalian Biology 76:741-747.
Bercovitch, F. B., and P. S. M. Berry. 2010. Ecological determinants of herd size in the Thornicroft's giraffe of Zambia. African Journal of Ecology 48:962-971.
Bercovitch, F. B., and P. S. M. Berry. 2013. Herd composition, kinship and fissionfusion social dynamics among wild giraffe. African Journal of Ecology 51:206-216.
Bercovitch, F. B., and P. S. M. Berry. 2015. The composition and function of all-male herds of Thornicroft's giraffe, Giraffa camelopardalis thornicrofti, in Zambia. African Journal of Ecology 53:167-174.
Berry, P. S. M., and F. B. Bercovitch. 2015. Leadership of herd progressions in the Thornicroft's giraffe of Zambia. African Journal of Ecology 53:175-182.
Bininda-Emonds, O. R., M. Cardillo, K. E. Jones, R. D. MacPhee, R. M. Beck, R. Grenyer, S. A. Price, R. A. Vos, J. L. Gittleman, and A. Purvis. 2007. The delayed rise of present-day mammals. Nature 446:507. 70 Blomberg, S. P., T. Garland, and A. R. Ives. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717-745.
Bonenfant, C., J. M. Gaillard, F. Klein, and D. Maillard. 2004. Variation in harem size of red deer (Cervus elaphus L.): the effects of adult sex ratio and age-structure. Journal of Zoology 264:77-85.
Bothma, J. d. P., and C. Walker. 2013. Larger Carnivores of the African Savannas. Springer Science & Business Media.
Bowyer, R. T., J. L. Rachlow, K. M. Stewart, and V. Van Ballenberghe. 2011. Vocalizations by Alaskan moose: female incitation of male aggression. Behavioral Ecology and Sociobiology 65:2251-2260.
Boyles, R. M., E. Shultz, and J. de Leon. 2016. Bubalus mindorensis. The IUCN Red List of Threatened Species 2016.
Brashares, J. S., and P. Arcese. 2002. Role of forage, habitat and predation in the behavioural plasticity of a small African antelope. Journal of Animal Ecology 71:626-638.
Braza, F., C. S. Jose, A. Blom, V. Cases, and J. E. Garcia. 1990. Population parameters of fallow deer at Doñana National Park (SW Spain). Acta Theriologica 35:277-288.
Brotherton, P. N. M., and M. B. Manser. 1997. Female dispersion and the evolution of monogamy in the dik-dik. Animal Behaviour 54:1413-1424.
Brotherton, P. N. M., J. M. Pemberton, P. E. Komers, and G. Malarky. 1997. Genetic and behavioural evidence of monogamy in a mammal, Kirk's dik-dik (Madoqua kirkii). Proceedings of the Royal Society B-Biological Sciences 264:675-681.
Brotherton, P. N. M., and A. Rhodes. 1996. Monogamy without biparental care in a dwarf antelope. Proceedings of the Royal Society B-Biological Sciences 263:23-29.
Brugiere, D., B. Magassouba, A. Sylla, H. Diallo, and M. Sow. 2006. Population abundance of the common hippopotamus Hippopotamus amphibius in the Haut Niger National Park, Republic of Guinea. Mammalia 70:14-16.
Bürkner, P.-C. 2017. brms: An R package for Bayesian multilevel models using Stan. Journal of Statistical Software 80:1-28.
Buzzard, P. J., W. V. Bleisch, D. Xue, and H. Zhang. 2008. Evidence for lekking in chiru. Journal of Zoology 276:330-335.
Byers, J. A., and D. W. Kitchen. 1988. Mating system shift in a pronghorn poulation. Behavioral Ecology and Sociobiology 22:355-360.
Cameron, E. Z., W. L. Linklater, K. J. Stafford, and E. O. Minot. 2003. Social grouping and maternal behaviour in feral horses (Equus caballus): the influence of males on maternal protectiveness. Behavioral Ecology and Sociobiology 53:92-101.
71 Carpenter, B., A. Gelman, M. D. Hoffman, D. Lee, B. Goodrich, M. Betancourt, M. Brubaker, J. Guo, P. Li, and A. Riddell. 2017. Stan: A probabilistic programming language. Journal of Statistical Software 76.
Clayton, L., and D. W. MacDonald. 1999. Social organization of the babirusa (Babyrousa babyrussa) and their use of salt licks in Sulawesi, Indonesia. Journal of Mammalogy 80:1147-1157.
Clutton-Brock, T., and B. C. Sheldon. 2010. Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends in Ecology & Evolution 25:562-573.
Clutton-Brock, T. H. 1989. Review lecture: mammalian mating systems. Proceedings of the Royal Society B-Biological Sciences 236:339-372.
Clutton-Brock, T. H., F. E. Guinness, and S. D. Albon. 1982. Red Deer: Behavior and Ecology of Two Sexes. University of Chicago press.
Clutton-Brock, T. H., P. H. Harvey, and B. Rudder. 1977. Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature 269:797.
Clutton-Brock, T. H., and D. Lukas. 2012. The evolution of social philopatry and dispersal in female mammals. Molecular Ecology 21:472-492.
Cooper, J. D., P. M. Waser, E. C. Hellgren, T. M. Gabor, and J. A. DeWoody. 2011. Is sexual monomorphism a predictor of polygynandry? Evidence from a social mammal, the collared peccary. Behavioral Ecology and Sociobiology 65:775-785.
Creel, S. 1995. Sociality, group size, and reproductive suppression among carnivores. Advances in the Study of Behaviour 24:203-257. d'Arc, N. R., M. H. Cassini, and B. L. Vila. 2000. Habitat use by vicunas Vicugna vicugna in the Laguna Blanca Reserve (Catamarca, Argentina). Journal of Arid Environments 46:107- 115.
Dalerum, F. 2007. Phylogenetic reconstruction of carnivore social organizations. Journal of Zoology 273:90-97.
Dalerum, F., S. Creel, and S. Hall. 2006. Behavioral and endocrine correlates of reproductive failure in social aggregations of captive wolverines (Gulo gulo). Journal of Zoology 269:527-536.
Dar, T. A., B. Habib, and J. A. Khan. 2012. Group size, habitat use and overlap analysis of four sympatric ungulate species in Shivalik Ecosystem, Uttarakhand, India. Mammalia 76:31- 41.
Dardaillon, M. 1988. Wild boar social groupings and their seasonal changes in the Camargue, southern France. Zeitschrift Fur Saugetierkunde-International Journal of Mammalian Biology 53:22-30.
72 de Villemereuil, P., and S. Nakagawa. 2014. General quantitative genetic methods for comparative biology. Pages 287-303 Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology. Springer.
Delgado-Acevedo, J., A. Zamorano, R. W. DeYoung, T. A. Campbell, D. G. Hewitt, and D. B. Long. 2010. Promiscuous mating in feral pigs (Sus scrofa) from Texas, USA. Wildlife Research 37:539-546.
Deutsch, J. C. 1994. Lekking by default - female habitat preferences and male strategies in Uganda kob. Journal of Animal Ecology 63:101-115.
Difiore, A., and D. Rendall. 1994. Evolution of social organization - a reappraisal for primates using phylogenetic methods. Proceedings of the National Academy of Sciences of the United States of America 91:9941-9945.
Drickamer, L. C., S. H. Vessey, and D. Meikle. 1996. Animal Behavior: Mechanims, Ecology, Evolution. 4th edition. Wm. C. Brown, Dubuque, Iowa.
Emlen, S. T., and L. W. Oring. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197:215-223.
Endo, A., and T. Doi. 2002. Multiple copulations and post-copulatory guarding in a free-living population of sika deer (Cervus nippon ). Ethology 108:739-747.
Fakhar-i-Abbas, T. P. Rooney, A. Mian, Z. I. Bhatti, and J. Haider. 2015. The distribution, population status, and wildlife product trade of Himalayan musk deer in Gilgit-Baltistan, Pakistan. Journal of Bioresource Management 2:38-47.
Fernández-Llario, P., J. Carranza, and S. H. De Trucios. 1996. Social organization of the wild boar (Sus scrofa) in Doñana National Park. Miscellània Zoològica 19:9-18.
Festa-Bianchet, M., M. Douhard, J.-M. Gaillard, and F. Pelletier. 2017. Successes and challenges of long-term field studies of marked ungulates. Journal of Mammalogy 98:612-620.
Fischer, F., and K. E. Linsenmair. 1999. The territorial system of the kob antelope (Kobus kob kob) in the Comoe National Park, Cote d'Ivoire. African Journal of Ecology 37:386-399.
Fischer, F., and K. E. Linsenmair. 2007. Changing social organization in an ungulate population subject to poaching and predation - the kob antelope (Kobus kob kob) in the Comoe National Park, Cote d'Ivoire. African Journal of Ecology 45:285-292.
Fischhoff, I. R., J. Dushoff, S. R. Sundaresan, J. E. Cordingley, and D. I. Rubenstein. 2009. Reproductive status influences group size and persistence of bonds in male plains zebra (Equus burchelli). Behavioral Ecology and Sociobiology 63:1035-1043.
Fischhoff, I. R., S. R. Sundaresan, J. Cordingley, H. M. Larkin, M.-J. Sellier, and D. I. Rubenstein. 2007. Social relationships and reproductive state influence leadership roles in movements of plains zebra, Equus burchellii. Animal Behaviour 73:825-831.
73 Garamszegi, L. Z. 2014. Uncertainties due to within-species variation in comparative studies: measurement errors and statistical weights. Pages 157-199 Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology. Springer.
Garay, G., I. M. Ortega, and O. Guineo. 2016. Social ecology of the huemul at Torres Del Paine National Park, Chile. Anales del Instituto de la Patagonia 44:25-38.
Garnier, J. N., M. W. Bruford, and B. Goossens. 2001. Mating system and reproductive skew in the black rhinoceros. Molecular Ecology 10:2031-2041.
Ghiglieri, M. P., T. M. Butynski, T. T. Struhsaker, L. Leland, S. J. Wallis, and P. Waser. 1982. Bush pig (Potamochoerus porcus) polychromatism and ecology in Kibale Forest, Uganda. African Journal of Ecology 20:231-236.
Gittleman, J. L. 1989. Carnivore group living: comparative trends. Pages 183-207 Carnivore Behavior, Ecology, and Evolution. Springer.
Habibi, K. 1997. Group dynamics of the Nubian ibex (Capra ibex nubiana) in the Tuwayiq Canyons, Saudi Arabia. Journal of Zoology 241:791-801.
Hameed, W., A. Fakhar i, and A. Mian. 2009. Population features of barking deer (Muntiacus muntjak) in Margalla Hills National Park, Pakistan. Pakistan Journal of Zoology 41:137- 142.
Hamilton, W. D. 1971. Geometry for the selfish herd. Journal of theoretical Biology 31:295-311.
Hampton, J., J. R. Pluske, and P. B. S. Spencer. 2004. A preliminary genetic study of the social biology of feral pigs in south-western Australia and the implications for management. Wildlife Research 31:375-381.
Harmon, L. J., and J. B. Losos. 2005. The effect of intraspecific sample size on type I and type II error rates in comparative studies. Evolution 59:2705-2710.
Hayes, L. D. 2000. To nest communally or not to nest communally: a review of rodent communal nesting and nursing. Animal Behaviour 59:677-688.
Hayes, L. D., and C. Schradin. 2017. Long-term field studies of mammals: what the short-term study cannot tell us. Journal of Mammalogy 98:600-602.
Hirth, D. H. 1997. Lek breeding in a Texas population of fallow deer (Dama dama). American Midland Naturalist 138:276-289.
Holden, J., A. Yanuar, and D. J. Martyr. 2003. The Asian Tapir in Kerinci Seblat National Park, Sumatra: evidence collected through photo-trapping. Oryx 37:34-40.
Ishihara, S., R. M. Boyles, H. Matsubayashi, A. N. del Barrio, M. R. Cebrian, A. Ishida, R. M. Lapitan, E. P. Atabay, L. C. Cruz, and Y. Kanai. 2015. Long-term community-based monitoring of tamaraw Bubalus mindorensis on Mindoro Island, Philippines. Oryx 49:352-359.
74 Ishihara, S., A. Ishida, A. N. Del Barrio, R. M. Lapitan, E. Atabay, R. M. Boyles, R. L. Salac, J. L. de Leon, M. M. Eduarte, L. C. Cruz, and Y. Kanai. 2007. Field survey on Tamaraw (Bubalus mindorensis) - Present population size and herd behavior in wild. Italian Journal of Animal Science 6:1249-1251.
Isvaran, K. 2007. Intraspecific variation in group size in the blackbuck antelope: the roles of habitat structure and forage at different spatial scales. Oecologia 154:435-444.
Isvaran, K., and Y. Jhala. 2000. Variation in lekking costs in blackbuck (Antilope cervicapra): Relationship to lek-territory location and female mating patterns. Behaviour 137:547- 563.
IUCN. 2018. The IUCN Red List of Threatened Species.
Jackson, T. 1999. The social organization and breeding system of Brants' whistling rat (Parotomys brantsii). Journal of Zoology 247:323-331.
Jaeggi, A. V., K. J. Boose, F. J. White, and M. Gurven. 2016. Obstacles and catalysts of cooperation in humans, bonobos, and chimpanzees: behavioural reaction norms can help explain variation in sex roles, inequality, war and peace. Behaviour 153:1015-1051.
Jarman, P. 1974. The social organisation of antelope in relation to their ecology. Behaviour 48:215-267.
Jarvis, J., and N. Bennett. 1993. Eusociality has evolved independently in two genera of bathyergid mole-rats—but occurs in no other subterranean mammal. Behavioral Ecology and Sociobiology 33:253-260.
Jedrzejewski, W., H. Spaedtke, J. F. Kamler, B. Jedrzejewska, and U. Stenkewitz. 2006. Group size dynamics of red deer in Bialowieza Primeval Forest, Poland. Journal of Wildlife Management 70:1054-1059.
Kamilar, J. M., and N. Cooper. 2013. Phylogenetic signal in primate behaviour, ecology and life history. Proceedings of the Royal Society B-Biological Sciences 368:20120341.
Kamler, J. F., W. B. Ballard, P. R. Lemons, and K. Mote. 2004. Variation in mating system and group structure in two populations of swift foxes, Vulpes velox. Animal Behaviour 68:83- 88.
Kampmann, S., B. A. Hampson, and C. C. Pollitt. 2013. Population dynamics of feral horses (Equus caballus) following above-average rainfall in a semi-arid environment of Australia. Australian Veterinary Journal 91:482-487.
Kappeler, P. M. 2014. Lemur behaviour informs the evolution of social monogamy. Trends in Ecology & Evolution 29:591-593.
Kappeler, P. M. 2018 in press. A framework for studying social complexity. Behavioral Ecology and Sociobiology.
75 Kappeler, P. M., and C. Fichtel. 2016. The evolution of Eulemur social organization. International Journal of Primatology 37:10-28.
Kappeler, P. M., and C. P. van Schaik. 2002. Evolution of primate social systems. International Journal of Primatology 23:707-740.
Karstad, E. L., and R. J. Hudson. 1986. Social organization and communication of riverine hippopotami in southwestern Kenya. Mammalia 50:153-164.
Kie, J. G., and R. T. Bowyer. 1999. Sexual segregation in white-tailed deer: Density-dependent changes in use of space, habitat selection, and dietary niche. Journal of Mammalogy 80:1004-1020.
Kishimoto, R., and T. Kawamichi. 1996. Territoriality and monogamous pairs in a solitary ungulate, the Japanese serow, Capricornis crispus. Animal Behaviour 52:673-682.
Klingel, H. 1998. Observations on social organization and behaviour of African and Asiatic Wild Asses (Equus africanus and Equus hemionus; Reprinted from Z Tierpsychol, vol 44, pg 323-331, 1977). Applied Animal Behaviour Science 60:103-113.
Koenig, A., C. J. Scarry, B. C. Wheeler, and C. Borries. 2013. Variation in grouping patterns, mating systems and social structure: what socio-ecological models attempt to explain. Proceedings of the Royal Society B-Biological Sciences 368:20120348.
Koenig, W. D., and J. L. Dickinson. 2016. Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution, and Behavior. Cambridge University Press.
Koster, J., and R. McElreath. 2017. Multinomial analysis of behavior: statistical methods. Behavioral Ecology and Sociobiology 71:138.
Krause, J., and G. D. Ruxton. 2002. Living in Groups. Oxford University Press.
Krebs, J. R., and N. B. Davies. 1981. An Introduction to Behavioural Ecology. Blackwell Scientific, Oxford.
Krebs, J. R., and N. B. Davies. 2009. Behavioural Ecology: An Evolutionary Approach. John Wiley & Sons.
Kucera, T. E. 1978. Social behavior and breeding system of desert mule deer. Journal of Mammalogy 59:463-476.
Kuehn, D. W. 1986. Population and social characteristics of the tamarao (Bubalus mindorensis). Biotropica 18:263-266.
Langbein, J., and S. J. Thirgood. 1989. Variation in mating systems of fallow deer (Dama dama) in relation to ecology. Ethology 83:195-214.
Laurie, A. 1982. Behavioral ecology of the greater one-horned rhinoceros (Rhinoceros unicornis). Journal of Zoology 196:307-341.
76 Lloyd, P. H., and O. A. E. Rasa. 1989. Status, reproductive success and fitness in cape mountain zebra (Equus zebra zebra). Behavioral Ecology and Sociobiology 25:411-420.
Loe, L. E., R. J. Irvine, C. Bonenfant, A. Stien, R. Langvatn, S. D. Albon, A. Mysterud, and N. C. Stenseth. 2006. Testing five hypotheses of sexual segregation in an arctic ungulate. Journal of Animal Ecology 75:485-496.
Lott, D. F. 1984. Intraspecific variation in the social systems of wild vertebrates. Behaviour 88:266-325.
Lott, D. F. 1991. Intraspecific Variation in the Social Systems of Wild Vertebrates. Cambridge University Press.
Lovari, S., and R. Cosentino. 1986. Seasonal habitat and group size of teh abruzzo chamois (Rupicapra pyrenaica ornata). Bollettino Di Zoologia 53:73-78.
Lukas, D., and T. Clutton-Brock. 2012. Cooperative breeding and monogamy in mammalian societies. Proceedings of the Royal Society B-Biological Sciences 279:2151-2156.
Lukas, D., and T. Clutton-Brock. 2017. Climate and the distribution of cooperative breeding in mammals. Royal Society Open Science 4:160897.
Lukas, D., and T. H. Clutton-Brock. 2013. The evolution of social monogamy in mammals. Science 341:526-530.
Luzhang, R., Z. Lixun, L. Naifa, H. Zuhao, M. Muli, and X. Kerong. 2005. Distribution and population status of the wild bactrian camel (Camelus bactrianus ferus) in Gansu Province, China. Journal of Camel Practice and Research 12:59-63.
Mabry, K. E., E. L. Shelley, K. E. Davis, D. T. Blumstein, and D. H. Van Vuren. 2013. Social mating system and sex-biased dispersal in mammals and birds: A phylogenetic analysis. Plos One 8:e57980.
Maher, C. R. 1991. Activity budgets and mating system of male pronghorn antelope at Sheldon National Wildlife Refuge, Nevada. Journal of Mammalogy 72:739-744.
Maher, C. R., and J. R. Burger. 2011. Intraspecific variation in space use, group size, and mating systems of caviomorph rodents. Journal of Mammalogy 92:54-64.
Mainguy, J., S. D. Cote, E. Cardinal, and M. Houle. 2008. Mating tactics and mate choice in relation to age and social rank in male mountain goats. Journal of Mammalogy 89:626- 635.
Maselli, V., D. Rippa, G. Russo, R. Ligrone, O. Soppelsa, B. D'Aniello, P. Raia, and D. Fulgione. 2014. Wild boars' social structure in the Mediterranean habitat. Italian Journal of Zoology 81:610-617.
Matsubayashi, H., E. Bosi, and S. Kohshima. 2006. Social system of the lesser mouse-deer (Tragulus javanicus). Mammal Study 31:111-114.
77 McCollum, K. R., A. L. Conway, M.-B. Lee, and J. P. Carroll. 2017. Occupancy and demographics of red river hog Potamochoerus porcus on Tiwai Island, Sierra Leone. African Journal of Ecology 55:47-55.
McElreath, R. 2018. Statistical Rethinking: A Bayesian Course with Examples in R and Stan. CRC Press.
Meredith, R. W., J. E. Janecka, J. Gatesy, O. A. Ryder, C. A. Fisher, E. C. Teeling, A. Goodbla, E. Eizirik, T. L. Simão, and T. Stadler. 2011. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science:1211028.
Milner, J. M., E. B. Nilsen, and H. P. Andreassen. 2007. Demographic side effects of selective hunting in ungulates and carnivores. Conservation Biology 21:36-47.
Moehlman, P. D. 1998. Feral asses (Equus africanus): intraspecific variation in social organization in arid and mesic habitats. Applied Animal Behaviour Science 60:171-195.
Molvar, E. M., and R. T. Bowyer. 1994. Costs and benefits of group living in a recently social ungulate - the Alaskan moose. Journal of Mammalogy 75:621-630.
Mooring, M. S., D. D. Reisig, E. R. Osborne, A. L. Kanallakan, B. M. Hall, E. W. Schaad, D. S. Wiseman, and R. R. Huber. 2005. Sexual segregation in bison: a test of multiple hypotheses. Behaviour 142:897-927.
Mukinya, J. G. 1973. Density, distribution, population structure and social organization of the black rhinoceros in Masai Mara Game Reserve. African Journal of Ecology 11:385-400.
Murray, M. G. 1982. The rut of impala - aspects of seasonal mating under tropical conditions. Zeitschrift Fur Tierpsychologie-Journal of Comparative Ethology 59:319-337.
Nakashima, Y., E. Inoue, and E.-F. Akomo-Okoue. 2013. Population density and habitat preferences of forest duikers in Moukalaba-Doudou National Park, Gabon. African Zoology 48:395-399.
Nikaido, M., A. P. Rooney, and N. Okada. 1999. Phylogenetic relationships among cetartiodactyls based on insertions of short and long interpersed elements: hippopotamuses are the closest extant relatives of whales. Proceedings of the National Academy of Sciences 96:10261-10266.
Novellie, P. A., J. Manson, and R. C. Bigalke. 1984. Behavioral ecology and communication in the cape grysbok. South African Journal of Zoology 19:22-30.
Nowak, R. M. 1999. Walker's Mammals of the World. JHU Press.
O'leary, M. A., J. I. Bloch, J. J. Flynn, T. J. Gaudin, A. Giallombardo, N. P. Giannini, S. L. Goldberg, B. P. Kraatz, Z.-X. Luo, and J. Meng. 2013. The placental mammal ancestor and the post–K-Pg radiation of placentals. Science 339:662-667.
78 Opie, C., Q. D. Atkinson, R. I. Dunbar, and S. Shultz. 2013. Male infanticide leads to social monogamy in primates. Proceedings of the National Academy of Sciences 110:13328- 13332.
Ortega, I. M., and W. L. Franklin. 1995. Social organization, distribution and movements of a migratory guanaco. Revista Chilena de Historia Natural 68:489-500.
Ostrowski, S., H. Rahmani, J. M. Ali, R. Ali, and P. Zahler. 2016. Musk deer Moschus cupreus persist in the eastern forests of Afghanistan. Oryx 50:323-328.
Owen-Smith, N. 1984. Spatial and temporal components of teh systems of kudu bulls and red deer stags. Animal Behaviour 32:321-332.
Paradis, E., J. Claude, and K. Strimmer. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290.
Patry, M., K. Leus, and A. A. Macdonald. 1995. Group structure and behaviour of babirusa (Babyrousa babyrussa) in Northern Sulawesi. Australian Journal of Zoology 43:643-655.
Penzhorn, B. 1984. A long‐term study of social organisation and behaviour of Cape Mountain Zebras Equus zebra zebra. Ethology 64:97-146.
Penzhorn, B. L. 1982. Habitat selection by cape mountain zebras in the Mountain Zebra National Park. South African Journal of Wildlife Research 12:48-54.
Penzhorn, B. L., and P. A. Novellie. 1991. Some behavioral traits of cape mountain zebras (Equus zebra zebra) and their implications for the management of a small conservation area. Applied Animal Behaviour Science 29:293-299.
Pérez-Barbería, F. J., and I. J. Gordon. 2000. Differences in body mass and oral morphology between the sexes in the Artiodactyla: evolutionary relationships with sexual segregation. Evolutionary Ecology Research 2:667-684.
Perez-Gonzalez, J., and J. Carranza. 2011. Female aggregation interacts with population structure to influence the degree of polygyny in red deer. Animal Behaviour 82:957-970.
Perez-Irineo, G., and A. Santos-Moreno. 2016. Abundance, herd size, activity pattern and occupancy of ungulates in Southeastern Mexico. Animal Biology 66:97-109.
Pérez‐Barbería, F. J., I. Gordon, and M. Pagel. 2002. The origins of sexual dimorphism in body size in ungulates. Evolution 56:1276-1285.
Perrin, M., and C. Taolo. 1998. Home range, activity pattern and social structure of anintroduced herd of roan antelope in KwaZulu-Natal, South Africa. South African Journal of Wildlife Research 28:27-32.
Piersma, T., and J. Drent. 2003. Phenotypic flexibility and the evolution of organismal design. Trends in Ecology & Evolution 18:228-233.
79 Poteaux, C., E. Baubet, G. Kaminski, S. Brandt, F. S. Dobson, and C. Baudoin. 2009. Socio- genetic structure and mating system of a wild boar population. Journal of Zoology 278:116-125.
Povilitis, A. J. 1983. Social organization and mating strategy of the huemul (Hippocamelus bisulcus). Journal of Mammalogy 64:156-158.
Povilitis, A. J. 1985. Social behavior of the huemul (Hippocamelus bisulcus) during the breeding season. Zeitschrift Fur Tierpsychologie-Journal of Comparative Ethology 68:261-286.
Probert, J., B. Evans, S. Andanje, R. Kock, and R. Amin. 2015. Population and habitat assessment of the Critically Endangered hirola Beatragus hunteri in Tsavo East National Park, Kenya. Oryx 49:514-520.
R Development Core Team. 2015. R: A language and environment for statistical computing.
Roberts, S. C., and R. I. M. Dunbar. 2000. Female territoriality and the function of scent-marking in a monogamous antelope (Oreotragus oreotragus). Behavioral Ecology and Sociobiology 47:417-423.
Rowe-Rowe, D. T., P. S. Everett, and M. R. Perrin. 1992. Group sizes of oribis in different habitats. South African Journal of Zoology 27:140-143.
Rubenstein, D. R., and P. Abbot. 2017. Comparative Social Evolution. Cambridge University Press.
Ruckstuhl, K. E., and P. Neuhaus. 2002. Sexual segregation in ungulates: a comparative test of three hypotheses. Biological Reviews 77:77-96.
Ruckstuhl, K. E., and P. Neuhaus. 2009. Activity budgets and sociality in a monomorphic ungulate: the African oryx (Oryx gazella). Canadian Journal of Zoology-Revue Canadienne de Zoologie 87:165-174.
Salter, R. E., and R. J. Hudson. 1982. Social organizaiton of feral horses in western Canada. Applied Animal Ethology 8:207-223.
Sandel, A. A., J. A. Miller, J. C. Mitani, C. L. Nunn, S. K. Patterson, and L. Z. Garamszegi. 2016. Assessing sources of error in comparative analyses of primate behavior: intraspecific variation in group size and the social brain hypothesis. Journal of Human Evolution 94:126-133.
Schaller, G. B., J. R. Ren, and M. J. Qiu. 1991. Observations of the tibetan antelope (Pantholops hodgsoni). Applied Animal Behaviour Science 29:361-378.
Schoepf, I., and C. Schradin. 2012. Better off alone! Reproductive competition and ecological constraints determine sociality in the African striped mouse (Rhabdomys pumilio). Journal of Animal Ecology 81:649-656.
80 Schradin, C. 2013. Intraspecific variation in social organization by genetic variation, developmental plasticity, social flexibility or entirely extrinsic factors. Philosophical Transactions of the Royal Society B-Biological Sciences 368:20120346.
Schradin, C., L. D. Hayes, N. Pillay, and C. Bertelsmeier. 2018. The evolution of intraspecific variation in social organization. Ethology 124:527-536.
Schradin, C., B. König, and N. Pillay. 2010. Reproductive competition favours solitary living while ecological constraints impose group‐living in African striped mice. Journal of Animal Ecology 79:515-521.
Schradin, C., A. K. Lindholm, J. Johannesen, I. Schoepf, C.-H. Yuen, B. Koenig, and N. Pillay. 2012. Social flexibility and social evolution in mammals: a case study of the African striped mouse (Rhabdomys pumilio). Molecular Ecology 21:541-553.
Schradin, C., and N. Pillay. 2005. Intraspecific variation in the spatial and social organization of the African striped mouse. Journal of Mammalogy 86:99-107.
Seidensticker, J. 1976. Ungulate populations in Chitawan valley, Nepal. Biological Conservation 10:183-210.
Shultz, S., C. Opie, and Q. D. Atkinson. 2011. Stepwise evolution of stable sociality in primates. Nature 479:219-U296.
Silk, J. B. 2007. The adaptive value of sociality in mammalian groups. Philosophical Transactions of the Royal Society B-Biological Sciences 362:539-559.
Silva, R. B., E. M. Vieira, and P. Izar. 2008. Social monogamy and biparental care of the neotropical southern bamboo rat (Kannabateomys amblyonyx). Journal of Mammalogy 89:1464-1472.
Simpson, H. I., S. A. Rands, and C. J. Nicol. 2012. Social structure, vigilance and behaviour of plains zebra (Equus burchellii): a 5-year case study of individuals living on a managed wildlife reserve. Acta Theriologica 57:111-120.
Smith, R. K., A. Marais, P. Chadwick, P. H. Lloyd, and R. A. Hill. 2008. Monitoring and management of the endangered Cape mountain zebra Equus zebra zebra in the Western Cape, South Africa. African Journal of Ecology 46:207-213.
Solomon, N. G., and J. A. French. 1997. Cooperative Breeding in Mammals. Cambridge University Press.
Somers, M. J., O. A. E. Rasa, and B. L. Penzhorn. 1995. Group structure and social behavior of warthogs Phacochoerus aethiopicus. Acta Theriologica 40:257-281.
Stallings, J. R., M. C. M. Kierulff, and L. F. B. Silva. 1994. Use of space, and activity patterns of Brazilian bamboo rats (Kannabateomys amblyonyx) in exotic habitat. Journal of Tropical Ecology 10:431-438.
Stan Development Team. 2018. RStan: the R interface to Stan. R package version. 81 Strier, K. B., P. C. Lee, and A. R. Ives. 2014. Behavioral flexibility and the evolution of primate social states. Plos One 9:e114099.
Sun, L., and N. Dai. 1995. Male and female association and mating system in the Chinese water deer (Hydropotes inermis). Mammalia 59:171-178.
Svendsen, G., and P. Bosch. 1993. On the behavior of vicunas (Vigugna vicugna Molina, 1782): difference due to sex, season and proximity to neighbors. Zeitschrift für Säugetierkunde 58:337-343.
Tatman, S. C., B. Stevens‐Wood, and V. B. Smith. 2000. Ranging behaviour and habitat usage in black rhinoceros, Diceros bicornis, in a Kenyan sanctuary. African Journal of Ecology 38:163-172.
Taylor, W. A., J. D. Skinner, and R. C. Krecek. 2006a. The activity budgets and activity patterns of sympatric grey rhebok and mountain reedbuck in a highveld grassland area of South Africa. African Journal of Ecology 44:431-437.
Taylor, W. A., J. D. Skinner, M. C. Williams, and R. C. Krecek. 2006b. Population dynamics of two sympatric antelope species, grey rhebok (Pelea capreolus) and mountain reedbuck (Redunca fulvorufula), in a highveld grassland region of South Africa. Journal of Zoology 268:369-379.
Tewari, R., and G. S. Rawat. 2013. Factors influencing seasonal changes in the herd size and composition of swamp deer in Jhilmil Jheel Conservation Reserve, Haridwar, Uttarakhand, India. International Journal of Pharmacy & Life Sciences 4:2870-2875.
Thierry, B. 2013. Identifying constraints in the evolution of primate societies. Philosophical Transactions of the Royal Society of London B: Biological Sciences 368:20120342.
Thirgood, S., J. Langbein, and R. J. Putman. 1999. Intraspecific variation in ungulate mating strategies: The case of the flexible fallow deer. Advances in the Study of Behavior 28:333-361.
Tilson, R. L. 1980. Klipspringer (Oreotragus oreotragus) social structure and predator avoidance in a desert canyon. Madoqua 11:303-314.
Torres, M. E., S. Puig, A. Novillo, and R. Ovejero. 2015. Vigilance behaviour of the year-round territorial vicuna (Vicugna vicugna) outside the breeding season: Influence of group size, social factors and distance to a water source. Behavioural Processes 113:163-171.
Torres, M. M., and S. Puig. 2012. Habitat use and selection by the vicuna (Vicugna vicugna, Camelidae) during summer and winter in the High Andean Puna of Argentina. Small Ruminant Research 104:17-27.
Travis, S. E., C. Slobodchikoff, and P. Keim. 1995. Ecological and demographic effects on intraspecific variation in the social system of prairie dogs. Ecology 76:1794-1803.
Valomy, M., L. D. Hayes, and C. Schradin. 2015. Social organization in Eulipotyphla: evidence for a social shrew. Biology Letters 11. 82 Van Schaik, C. P. 1983. Why are diurnal primates living in groups? Behaviour 87:120-144. van Schaik, C. P. 1989. The ecology of social relationships amongst female primates. Comparative socioecology. Blackwell, Oxford.
Van Schaik, C. P., and J. Van Hooff. 1983. On the ultimate causes of primate social systems. Behaviour 85:91-117.
Vanpé, C., P. Kjellander, J. M. Gaillard, J. F. Cosson, M. Galan, and A. J. M. Hewison. 2009. Multiple paternity occurs with low frequency in the territorial roe deer, Capreolus capreolus. Biological Journal of the Linnean Society 97:128-139.
Vanpé, C., P. Kjellander, M. Galan, J. F. Cosson, S. Aulagnier, O. Liberg, and A. M. Hewison. 2007. Mating system, sexual dimorphism, and the opportunity for sexual selection in a territorial ungulate. Behavioral Ecology 19:309-316.
Vaughan, T. A., J. M. Ryan, and N. J. Czaplewski. 2015. Mammalogy. 6th edition. Jones & Bartlett Publishers.
Vila, B. L., and V. G. Roig. 1992. Diurnal movements, family groups and alertness of vicuna (Vicugna vicugna) during the late dry season in the Laguna Blanca Reserve (Catamarca, Argentina). Small Ruminant Research 7:289-297.
Weinberg, P. I., R. Valdez, and A. K. Fedosenko. 1997. Status of the Heptner's markhor (Capra falconeri heptneri) in Turkmenistan. Journal of Mammalogy 78:826-829.
White, A. M. 2010. A pigheaded compromise: do competition and predation explain variation in warthog group size? Behavioral Ecology 21:485-492.
White, A. M., and E. Z. Cameron. 2011. Evidence of helping behavior in a free-ranging population of communally breeding warthogs. Journal of Ethology 29:419-425.
White, A. M., E. Z. Cameron, and M. M. Peacock. 2010. Grouping patterns in warthogs, Phacochoerus africanus: is communal care of young enough to explain sociality? Behaviour 147:1-18.
White, P. J., C. N. Gower, T. L. Davis, J. W. Sheldon, and J. R. White. 2012. Group dynamics of Yellowstone pronghorn. Journal of Mammalogy 93:1129-1138.
Willisch, C. S., and P. Neuhaus. 2009. Alternative mating tactics and their impact on survival in adult male alpine ibex (Capra ibex ibex). Journal of Mammalogy 90:1421-1430.
Wilson, D. E., and D. M. Reeder. 2005. Mammal Species of the World: A Taxonomic and Geographic Reference. JHU Press.
Wilson, E. O. 1975. Sociobiology: The New Synthesis. Harvard University Press, Cambridge, Massachusetts.
Yamagiwa, J., J. Kahekwa, and A. K. Basabose. 2003. Intra-specific variation in social organization of gorillas: implications for their social evolution. Primates 44:359-369. 83 Zisadza, P., E. Gandiwa, H. van der Westhuizen, E. van der Westhuizen, and V. Bodzo. 2010. Abundance, distribution and population trends of hippopotamus in Gonarezhou National Park, Zimbabwe. South African Journal of Wildlife Research 40:149-157.
84
APPENDIX A
SOCIAL ORGANIZATION DATA
85 Artiodactyla Social Organization Data
Genus species M F MF FFM FMM FFMM FF MM # SO # Studies # Populations Social State IVSO Antilocapra americana 2 2 1 1 4 6 6 Variable both
Aepyceros melampus 4 5 1 4 6 5 11 9 Variable both
Alcelaphus buselaphus 1 1 1 1 1 5 4 4 Variable both
Ammotragus lervia 2 1 1 1 1 4 4 6 6 6 Variable both
Antidorcas marsupialis 8 1 1 4 2 3 5 6 9 9 Variable both
Antilope cervicapra 2 3 2 3 3 6 Variable both
Beatragus hunteri 2 2 2 1 1 5 2 1 Variable wp
Bison bison 2 1 4 4 4 11 8 Variable both
Bison bonasus 3 1 4 3 4 2 Variable both
Bubalus bubalis 3 2 1 3 4 3 2 Variable both
Bubalus depressicornis 1 1 1 2 1 1 Variable wp
Bubalus mindorensis 3 3 3 1 3 4 3 1 Variable wp
Budorcas taxicolor 1 1 1 1 1 1 5 2 1 Variable wp
Capra falconeri 1 1 3 3 Group-living none
Capra ibex 2 2 1 1 1 4 2 6 7 5 Variable both
Capra nubiana 1 1 1 1 1 3 3 6 3 3 Variable both
Capra sibirica 6 6 2 6 5 Group-living wp
Capricornis crispus 3 3 3 2 3 3 Variable wp
Cephalophus silvicultor 1 1 1 1 1 Solitary none
Connochaetes gnou 9 9 9 3 5 11 Variable wp
Connochaetes taurinus 1 1 2 5 5 Variable wp
Damaliscus lunatus 1 1 1 2 3 3 5 3 3 Variable both
Damaliscus pygargus 1 1 1 3 3 3 Variable wp
Dorcatragus megalotis 2 1 2 3 1 4 4 1 Variable wp
Gazella bennettii 3 1 3 4 4 3 5 Variable both
Gazella dorcas 2 1 1 2 2 4 2 2 Variable both
Gazella gazella 3 3 1 2 4 4 5 3 3 Variable both
Gazella subgutturosa 4 4 1 1 5 5 5 8 6 Variable both
Hemitragus jayakari 1 1 1 2 1 1 Variable wp
Hemitragus jemlahicus 1 1 2 2 1 Group-living wp
Hippotragus equinus 2 1 4 4 Group-living none
Kobus ellipsiprymnus 3 1 3 4 4 4 5 Variable both
Kobus kob 4 4 2 1 5 2 5 5 2 Variable both
Kobus leche 1 1 2 2 2 Group-living wp
Kobus vardonii 5 4 2 3 3 3 5 4 5 Variable both
Litocranius walleri 2 1 1 2 1 4 2 1 Variable wp
86 Genus species M F MF FFM FMM FFMM FF MM # SO # Studies # Populations Social State IVSO Madoqua kirkii 4 1 4 3 Pair-living none
Naemorhedus goral 2 2 1 2 1 1 5 4 4 Variable both
Nanger granti 3 1 1 2 1 3 3 6 4 4 Variable both
Oreamnos americanus 2 1 2 3 2 Group-living wp
Oreotragus oreotragus 2 2 4 1 3 4 3 Variable both
Oryx beisa 2 2 2 2 1 ? 5 2 3 Variable both
Oryx gazella 1 1 2 3 3 Variable wp
Ourebia ourebi 7 3 7 7 7 5 5 7 8 Variable both
Ovibos moschatus 2 1 2 3 4 4 Variable both
Ovis ammon 1 3 3 3 8 6 Variable both
Ovis canadensis 3 1 5 5 3 5 4 Variable both
Ovis dalli 1 1 2 1 1 Variable wp
Pantholops hodgsonii 2 1 1 3 2 4 4 3 Variable both
Pelea capreolus 1 1 2 4 1 1 5 4 3 Variable both
Procapra picticaudata 3 2 2 4 2 Group-living both
Procapra przewalskii 6 3 8 8 3 7 4 Variable wp
Pseudois nayaur 1 1 2 4 4 Group-living wp
Pseudois schaeferi 1 1 2 1 1 Group-living wp
Raphicerus melanotis 1 1 1 2 1 1 Solitary wp
Redunca arundinum 1 1 1 1 1 1 5 2 2 Variable wp
Redunca fulvorufula 4 3 2 2 4 4 5 8 Variable both
Redunca redunca 1 1 1 2 4 3 Variable wp
Rupicapra pyrenaica 1 3 3 3 5 4 Variable both
Rupicapra rupicapra 2 2 4 2 5 5 Variable both
Saiga tatarica 1 1 2 1 1 Group-living wp
Sylvicapra grimmia 2 2 1 1 3 2 2 Variable both
Syncerus caffer 4 1 1 1 1 3 5 7 6 Variable both
Tetracerus quadricornis 1 1 1 2 1 1 Solitary wp
Tragelaphus buxtoni 2 1 1 1 3 5 3 Variable both
Tragelaphus eurycerus 2 1 2 1 3 3 2 Variable both
Tragelaphus imberbis 1 1 1 3 1 1 Variable wp
Tragelaphus scriptus 4 4 2 2 4 3 5 6 4 Variable both
Tragelaphus spekii 1 1 2 1 1 Variable wp
Tragelaphus strepsiceros 3 1 2 2 4 4 5 6 4 Variable both
Camelus bactrianus 1 1 1 1 4 2 2 Variable wp
Lama glama 3 3 1 3 4 3 3 Variable both
Vicugna vicugna 3 6 6 3 9 5 Variable both
87 Genus species M F MF FFM FMM FFMM FF MM # SO # Studies # Populations Social State IVSO Alces alces 2 2 1 1 3 2 5 6 3 Variable both
Axis axis 1 2 2 3 8 7 Variable both
Axis porcinus 2 2 1 1 1 4 2 2 Variable both
Blastocerus dichotomus 2 2 1 1 3 2 2 Variable both
Capreolus capreolus 3 2 1 1 3 7 6 Variable both
Capreolus pygargus 1 1 1 1 1 4 1 1 Variable wp
Cervus elaphus 1 1 2 1 4 4 5 12 10 Variable both
Cervus nippon 1 1 3 3 3 6 5 Variable both
Dama dama 2 2 2 1 3 4 5 6 6 Variable both
Hippocamelus antisensis 1 1 2 1 3 2 2 Variable both
Hippocamelus bisulcus 3 3 3 1 3 6 5 Variable both
Muntiacus muntjak 4 4 3 2 4 4 Variable wp
Odocoileus hemionus 1 1 3 2 4 6 5 Variable both
Odocoileus virginianus 5 5 1 4 5 4 11 11 Variable both
Ozotoceros bezoarticus 3 3 3 3 3 4 4 Variable wp
Rangifer tarandus 1 1 3 3 4 4 4 Variable both
Rucervus duvaucelii 1 1 2 2 2 Group-living wp
Rusa unicolor 1 1 1 1 1 4 4 4 Variable wp
Giraffa camelopardalis 8 6 2 5 3 4 16 11 Variable both
Hippopotamus amphibius 1 1 1 3 10 7 Variable both
Moschus cupreus 1 1 1 1 1 Solitary none
Moschus leucogaster 1 1 1 1 1 Solitary none
Babyrousa babyrussa 2 2 2 1 2 1 5 2 1 Variable wp
Phacochoerus aethiopicus 1 1 1 1 3 1 1 Variable wp
Phacochoerus africanus 2 2 1 4 2 Solitary none
Potamochoerus porcus 1 1 1 1 3 2 2 Variable wp
Sus scrofa 5 5 2 6 2 5 8 7 Variable both
88 Perissodactyla Social Organization Data
Genus species M F MF FFM FFMM FF MM # SO # Studies # Populations Social State IVSO Equus asinus 7 2 4 6 4 6 7 6 7 8 Variable both
Equus burchellii 3 1 1 2 4 4 3 Variable both
Equus caballus 3 5 4 1 3 5 6 4 Variable both
Equus hemionus 3 5 1 3 4 2 8 Variable both
Equus kiang 1 1 1 3 4 4 Variable wp
Equus zebra 5 1 6 3 Group-living none
Diceros bicornis 2 2 1 1 3 4 4 Variable both
Rhinoceros unicornis 1 1 1 1 1 4 2 1 Variable wp
Tapirus bairdii 1 1 1 1 1 Solitary none
Tapirus indicus 1 1 1 2 1 1 Variable wp
89
APPENDIX B
MATING SYSTEM DATA
90 Artiodactyla Mating System Data
Single- Genus Territorial Harem Lekking female # Mating species Defense Defense System Defense Promiscuity Monogamy MS # Studies # Populations System IVSM Antilocapra 1 1 2 3 2 Variable bp americana Aepyceros Territorial 1 1 1 1 none melampus Defense Ammotragus 1 1 1 1 Promiscuity none lervia Antidorcas Territorial 2 1 2 2 none marsupialis Defense Antilope Lekking 2 1 1 2 none cervicapra System Bison bison 4 1 2 4 3 Variable both Single- Capra ibex 1 1 1 1 female none Defense Capricornis 2 2 2 2 2 Variable wp crispus Connochaetes Territorial 1 1 1 1 none taurinus Defense Damaliscus Territorial 1 1 1 1 none lunatus Defense Kobus 2 2 2 4 2 Variable bp kob Kobus 2 2 2 2 1 Variable both leche Madoqua 1 4 2 3 2 Variable both kirkii Oreamnos 1 1 1 1 Promiscuity none americanus Oreotragus 3 1 2 2 Monogamy none oreotragus Ourebia 2 1 2 2 2 Variable both ourebi Pantholops Lekking 1 1 1 1 none hodgsonii System Pelea Harem 2 1 1 1 none capreolus Defense Rupicapra Harem 1 1 1 1 none pyrenaica Defense Rupicapra Territorial 2 1 2 1 none rupicapra Defense Tragelaphus Territorial 1 1 1 1 none scriptus Defense Tragelaphus Single- strepsicero 1 1 1 2 female none s Defense Vicugna Harem 1 1 1 1 none vicugna Defense Harem Alces alces 1 1 2 1 none Defense Capreolus 1 1 1 1 Promiscuity none capreolus Cervus Harem 3 1 4 3 none elaphus Defense Cervus 1 1 2 2 2 Variable both nippon Dama 3 1 2 3 3 Variable wp dama
91 Single- Territorial Harem Lekking female # # # Mating Genus species Defense Defense System Defense Promiscuity Monogamy MS Studies Populations System IVSM Single- Hydropotes 1 1 1 1 female none inermis Defense Muntiacus Territorial 1 1 1 1 none munjak Defense Single- Odocoileus 1 1 1 1 female none hemionus Defense Single- Odocoileus 3 1 1 3 female none virginianus Defense Phacochoerus 1 1 1 1 Promiscuity none aethiopicus Sus srofa 2 2 2 4 4 Variable bp Pecari 1 1 1 1 Promiscuity none tajacu Tragulus 1 1 2 1 1 Variable wp javanicus
Perissodactyla Mating System Data
Territorial Harem Genus species Defense Defense # MS # Studies # Populations Mating System IVSM Equus asinus 1 2 2 2 3 Variable bp Equus burchellii 1 1 2 1 Harem Defense none Equus caballus 3 1 3 3 Harem Defense none Equus zebra 5 1 5 2 Harem Defense none Diceros bicornis 1 1 1 1 Territorial Defense none
92
APPENDIX C
ECOLOGICAL AND LIFE HISTORY DATA
93 Artiodactyla Ecological and Life History Data
Male Female Breeding Sexual BM BM M:F # Genus species Seasonality Dimorphism Continent (kg) (kg) BM Habitats Antilocapra North Seasonal Dimorphic 56.2 49.8 1.128 2 americana America Aepyceros melampus Seasonal Dimorphic Africa 56.9 43.8 1.299 2
Alcelaphus buselaphus Monomorphic Africa 152.1 144.6 1.051 2 Ammotragus lervia Seasonal Monomorphic Africa 111.8 51.6 2.166 3 Antidorcas Seasonal Monomorphic Africa 40.7 35.5 1.146 4 marsupialis Antilope cervicapra Non-seasonal Dimorphic Asia 40.2 34.4 1.168 4 Beatragus hunteri Seasonal Monomorphic Africa 91 86 1.0581 2 North Seasonal Dimorphic 795.3 452.8 1.756 2 Bison bison America Bison bonasus Seasonal Dimorphic Europe; Asia 718 423 1.697 2 Asia; Seasonal Dimorphic 1200 800 1.500 3 Bubalus bubalis Australia Bubalus Non-seasonal Monomorphic Asia 156 145 1.0758 1 depressicornis
Bubalus mindorensis Asia 1 Budorcas taxicolor Seasonal Dimorphic Asia 282.7 160 1.766 1 Capra falconeri Seasonal Monomorphic Europe; Asia 92.7 36.3 2.553 1 Capra ibex Seasonal Monomorphic Europe; Asia 80.5 48.9 1.646 3
Capra nubiana Seasonal Africa 62.5 26.5 2.358 2
Capra sibirica Seasonal Europe; Asia 4
Capricornis crispus Seasonal Monomorphic Africa 30 3 Cephalophus Non-seasonal Monomorphic Africa 52.5 72 0.729 1 silvicultor Connochaetes gnou Seasonal Dimorphic Africa 166.7 135 1.234 1 Connochaetes taurinus Seasonal Dimorphic Africa 235.3 184.9 1.272 1 Damaliscus lunatus Seasonal Dimorphic Africa 137 120.1 1.140 2
Damaliscus pygargus Seasonal Africa 72.5 62.5 1.160 1 Dorcatragus megalotis Seasonal Dimorphic Africa 10 10.7 0.934 1
Gazella bennettii Seasonal Europe; Asia 2 Gazella dorcas Seasonal Monomorphic Africa 16.3 13.3 1.225 2 Gazella gazella Seasonal Monomorphic Europe; Asia 23.3 20.8 1.120 2 Gazella subgutturosa Seasonal Monomorphic Europe; Asia 27.3 23 1.186 2 Hemitragus jayakari Non-seasonal Monomorphic Europe; Asia 26.5 17 1.558 1 Hemitragus Seasonal Dimorphic Asia 103.3 56 1.844 2 jemlahicus Hippotragus equinus Non-seasonal Monomorphic Africa 274.4 256.4 1.070 2
94 Male Female Breeding Sexual BM BM M:F # Genus species Seasonality Dimorphism Continent (kg) (kg) BM Habitats Kobus ellipsiprymnus Non-seasonal Dimorphic Africa 236.8 187.3 1.264 4 Kobus kob Non-seasonal Dimorphic Africa 97.5 61.9 1.575 2 Kobus leche Seasonal Dimorphic Africa 104.3 78.7 1.325 1 Kobus vardonii Seasonal Dimorphic Africa 76 63.5 1.196 2 Litocranius walleri Non-seasonal Monomorphic Africa 35 34.3 1.020 1 Madoqua kirkii Seasonal Monomorphic Africa 4.6 5.1 0.901 3 Naemorhedus goral Seasonal Monomorphic Asia 32 29.9 1.070 1 Nanger granti Non-seasonal Dimorphic Africa 72.1 46 1.567 2 North Seasonal Monomorphic 95.9 61 1.572 2 Oreamnos americanus America Oreotragus oreotragus Non-seasonal Monomorphic Africa 11.3 13 0.869 2
Oryx beisa Non-seasonal Africa 2 Oryx gazella Non-seasonal Monomorphic Africa 178 166.4 1.069 1 Ourebia ourebi Non-seasonal Monomorphic Africa 14.1 15.1 0.933 2 North Seasonal Dimorphic 356 247.3 1.439 2 Ovibos moschatus America Ovis ammon Seasonal Monomorphic Europe; Asia 120.7 63.2 1.909 3 North Seasonal Monomorphic 83.4 58.7 1.420 2 Ovis canadensis America North Seasonal Monomorphic 80.4 53.3 1.508 1 Ovis dalli America Pantholops hodgsonii Seasonal Dimorphic Asia 42.3 25.8 1.639 1 Pelea capreolus Seasonal Monomorphic Africa 24 25 0.96 1
Procapra picticaudata Seasonal Asia 2
Procapra przewalskii Seasonal Asia 2 Pseudois nayaur Seasonal Monomorphic Europe; Asia 60 39.5 1.518 1
Pseudois schaeferi Seasonal Asia 1 Raphicerus melanotis Seasonal Monomorphic Africa 10.7 10.5 1.019 1 Redunca arundinum Non-seasonal Dimorphic Africa 58.3 43.2 1.349 2 Redunca fulvorufula Seasonal Monomorphic Africa 30.1 28.5 1.0561 4 Redunca redunca Non-seasonal Dimorphic Africa 51.6 40.3 1.280 2
Rupicapra pyrenaica Seasonal Europe; Asia 3 Rupicapra rupicapra Seasonal Dimorphic Europe; Asia 40.3 31.7 1.271 3 Saiga tatarica Seasonal Dimorphic Europe; Asia 42.5 32.3 1.315 1 Sylvicapra grimmia Non-seasonal Monomorphic Africa 18.3 19.6 0.933 3 Syncerus caffer Non-seasonal Dimorphic Africa 642.9 467.5 1.375 3 Tetracerus Seasonal Monomorphic Asia 18 17 1.058 1 quadricornis
95 # Breeding Dimorphis Male BM Female BM M:F Habitat Genus species Seasonality m Continent (kg) (kg) BM s Tragelaphus Seasonal Dimorphic Africa 232 166.7 1.391 2 buxtoni Tragelaphus Seasonal Africa 322.5 222.5 1.449 1 eurycerus Tragelaphus Dimorphic Africa 95.6 62.1 1.539 1 imberbis Tragelaphus Non-seasonal Dimorphic Africa 49.7 31.1 1.598 3 scriptus Tragelaphus spekii Non-seasonal Dimorphic Africa 102.3 60.2 1.699 1 Tragelaphus Seasonal Dimorphic Africa 240.8 159.2 1.512 2 strepsiceros
Camelus bactrianus Seasonal Europe; Asia 1 Monomorp Seasonal South America 109.5 99 1.106 2 Lama glama hic Monomorp Seasonal South America 40.5 37.5 1.08 3 Vicugna vicugna hic Europe; Asia; Seasonal Dimorphic 510.2 358.8 1.421 2 Alces alces North America
Axis axis Dimorphic Asia 80.7 48.7 1.657 2 Axis porcinus Seasonal Dimorphic Asia 44.1 30.6 1.441 3 Blastocerus Seasonal Dimorphic South America 140 120 1.166 2 dichotomus Capreolus Monomorp Seasonal Europe; Asia 24.2 23.4 1.0341 3 capreolus hic Capreolus Europe; Asia 1 pygargus Cervus elaphus Seasonal Dimorphic Europe; Asia 185.1 140.2 1.320 2 Cervus nippon Seasonal Dimorphic Europe; Asia 56.5 37.4 1.510 3 Dama dama Seasonal Dimorphic Europe; Asia 68 44.6 1.524 5 Hippocamelus Seasonal South America 1 antisensis Hippocamelus Seasonal Dimorphic South America 65 55 1.181 2 bisulcus
Hydropotes inermis Europe; Asia 1 Muntiacus muntjak Non-seasonal Dimorphic Asia 20.9 15.1 1.384 1 Odocoileus Seasonal Dimorphic North America 70.3 46.9 1.498 2 hemionus Odocoileus North America; South Seasonal Dimorphic 57.6 47.1 1.222 4 virginianus America Ozotoceros Seasonal South America 2 bezoarticus North America; Europe; Seasonal Dimorphic 145 85.8 1.689 3 Rangifer tarandus Asia Rucervus Seasonal Dimorphic Asia 223.1 142 1.571 1 duvaucelii Rusa unicolor Non-seasonal Dimorphic Asia 206.3 131.8 1.565 2
96
# Breeding Dimorphi Male BM Female BM M:F Habitat Genus species Seasonality sm Continent (kg) (kg) BM s Giraffa Non-seasonal Dimorphic Africa 1190.2 814.3 1.461 5 camelopardalis Hippopotamus Non-seasonal Dimorphic Africa 1 amphibius
Moschus cupreus Europe; Asia 1 Moschus Seasonal Asia 1 leucogaster Babyrousa Non-seasonal Asia 1 babyrussa Phacochoerus Seasonal Dimorphic Africa 1 aethiopicus Phacochoerus Seasonal Africa 2 africanus Potamochoerus Seasonal Africa 1 porcus
Sus scrofa Seasonal Dimorphic Europe; Asia 4 Monomorp South America; North Non-seasonal 1 Pecari tajacu hic America Monomorp Non-seasonal Asia 1.3 1.5 0.866 1 Tragulus javanicus hic Blank cells indicate unavailable data
97
APPENDIX D
PHYLOGENETIC MODELS
98 Phylogenetic Mixed-Effect Models
These models are used to test for associations between social organization/mating system and the predictors, estimate ancestral states, and partition variance in social organization/mating system into phylogenetic, within and between species effects (wherein the phylogenetic effect is a measure of phylogenetic constraints or inertia, the within species effect is a measure of IVSO/IVMS, and the between species effect accounts for any variation in species typical social organization/mating system that is not accounted for by the predictors).
Model 1a: SO (categorical) ~ sexual dimorphism + female body size + no.habitats + SeasonBreed + no.studies + (1|phylo) + (1|Genus_species) + (1|Continent) + (1|Habitat)
Model 1b: SO (numerical) ~ sexual dimorphism + female body size + no.habitats + SeasonBreed + no.studies + (1|phylo) + (1|Genus_species) + (1|Continent) + (1|Habitat)
Model 2a: MS (categorial) ~ sexual dimorphism + female body size + no.habitats + SeasonBreed + no.studies + (1|phylo) + (1|Genus_species) + (1|Continent) + (1|Habitat)
Model 2b: MS (numerical) ~ sexual dimorphism + female body size + no.habitats + SeasonBreed + no.studies + (1|phylo) + (1|Genus_species) + (1|Continent) + (1|Habitat)
99
VITA
Monica Miles was born in Springfield, TN, to the parents of David and Colleen Miles.
She is the third of four children with two older brothers and one younger brother. She attended
Springfield High School in Springfield, TN. After graduation, she attended The University of
Tennessee at Chattanooga as a first-generation college student, where she became interested in organismal biology and animal behavior. She completed her Bachelor of Science in May 2016 with a major in Biology and a minor in Chemistry. Upon graduation, she entered UTC’s
Environmental Science master’s program. Monica graduated with a Master of Science in
Environmental Science in December 2018.
100