Peter M. Kappeler

Evolution of Primate Social Systems

We review evolutionary processes and mechanisms that gave rise to the diversity of primate social systems. We define social organization, social structure and mating system as distinct components of a social system. For each component, we summarize levels and patterns of variation among primates and discuss evolutionary determinants of this variation. We conclude that conclusive explanations for a solitary life and pair-living are still lacking. We then focus on interactions among the 3 components in order to identify main targets of selection and potential constraints for social evolution. Social organization and mating system are more closely linked to each other than either one is to social structure. Further, we conclude that it is important to seek a priori measures for the effects of presumed selective factors and that the genetic contribution to social systems is still poorly examined. Finally, we examine the role of primate socio-ecology in current evolutionary biology and conclude that primates are not prominently represented because the main questions asked in behavioral ecology are often irrelevant for primate behavior. For the future, we see a rapprochement of these areas as the role of disease and life-history theory are integrated more fully into primate socio-ecology.

Infanticide risk and the evolution of male–female association in primates

Year–round association between adult males and females is common in primates, even though internal gestation and lactation predispose males to mate–desertion in the majority of mammals. Because there is little a priori support for alternative explanations, we hypothesized that permanent male–female association in primates serves to reduce the risk of infanticide by strange males whenever females and infants are closely associated. For a phylogenetic test of this hypothesis, we reconstructed the evolution of male–female and female–infant association among primates. The results of Maddisons concentrated changes test confirmed the prediction that mother–infant association, as opposed to infant parking, and female–male association did not evolve independently. Changes in litter size and activity, in contrast, were not significantly associated with evolutionary changes in male–female association. Thus, we demonstrate a fundamental link between primate life history and social behaviour, explain the most basic type of variation in primate social organization, and propose an additional determinant of social organization that may also operate in other mammals.

Sexual selection in primates : new and comparative perspectives

List of contributors Foreword Robert L. Trivers Preface Part I. Introduction: 1. Sexual selection in primates: review and selective preview Peter M. Kappeler and Carel P. van Schaik 2. What is sexual selection? Tim H. Clutton-Brock 3. Sex roles, contests for the control of reproduction and sexual selection Patricia Adair Gowaty Part II. Sexual Signals: Substrates and Function: 4. Sexual selection and communication Charles T. Snowdon 5. Sexual selection and exaggerated sexual swellings of female primates Dietmar P. Zinner, Charles L. Nunn, Carel P. van Schaik and Peter M. Kappeler 6. Female multiple mating and genetic benefits in humans: investigations of design Steven W. Gangestad and Randy Thornhill Part III. Sexual Selection in Action: 7. Sexual selection, behaviour and sexually transmitted diseases Charles L. Nunn and Sonia M. Altizer 8. Mating conflict in primates: infanticide, sexual harassment and female sexuality Carel P. van Schaik, Gauri R. Pradhan and Maria A. van Noordwijk 9. Post-copulatory sexual selection in birds and primates Tim R. Birkhead and Peter M. Kappeler Part IV. Development and Consequences: 10. Development and sexual selection in primates Joanna M. Setchell and Phyllis C. Lee 11. Alternative male reproductive strategies: male bimaturism in orangutans Suci Atmoko Utami and Jan A. R. A. M. van Hooff 12. Sexual selection and the careers of primate males: paternity concentration, dominance acquisition tactics and transfer decisions Maria A. van Noordwijk and Carel P. van Schaik 13. Sexual selection, measures of sexual selection and sexual dimorphism in primates J. Michael Plavcan 14. Sex ratios in primate groups Joan B. Silk and Gillian R. Brown 15. Natural and sexual selection and the evolution of multi-level societies: insights from zebras with comparisons to primates Daniel I. Rubenstein and Mace Hack Index.

Lemur social systems and their ecological basis

Patterns of Range Use and Social Organization of Ayeayes (Daubentonia madagascariensis) on Nosy Mangabe E.J. Sterling. The Socioecology of Eulemur macaco I.C. Colquhoun. Home Range and Diet in Red Ruffed Lemurs (Varecia variegata rubra) on the Masoala Peninsula, Madagascar M.M. Rigamonti. Male Transfer in Captive Ruffed Lemurs, Varecia variegata variegata F.J. White, et al. A Review of Predation on Lemurs S.M. Goodman, et al. Adaptation and Phylogenetic Constraints in the Antipredator Behavior of Ringtailed and Ruffed Lemurs J.M. Macedonia. Territoriality in Lemur catta Groups During the Birth Season at Berenty, Madagascar A. Jollly, et al. A New Interpretation of the Social Organization and Mating System of the Ringtailed Lemur (Lemur catta) M.L. Sauther, R.W. Sussman. Feeding Behavior of Lemur catta Females in Relation to their Physiological State H.R. Rasamimanana, E. Rafidinarivo. 8 additional articles. Index.

Patterns of Sexual Dimorphism in Body Weight among Prosimian Primates

Many primatologists believe that there is no sexual dimorphism in body size in prosimian primates. Because this belief is based upon data that came from only a few species and were largely flawed in some aspect of sample quality, I re-examined the extent of sexual dimorphism in body weight, using weights of 791 adult prosimians from 34 taxa recorded over the last 17 years at the Duke University Primate Center. There was no significant sex difference in body weight in 17 species, but males were significantly larger in Nycticebus pygmaeus, Tarsius syrichta, Galago moholi, Galagoides demidovii, Otolemur crassicaudatus and Otolemur garnettii. Moreover, females were significantly larger in Microcebus murinus. Thus, the general lack of sexual dimorphism could be confirmed, notably for lemurs, but prosimians as a group show more variability in sexual size dimorphism than was previously thought. After including previously published data obtained in the wild from 8 additional species, I found significant heterogeneity in the degree of sexual dimorphism at the family level, but only the Indridae and Galagidae were significantly different from each other. Among the prosimian infraorders, the Lorisiformes were significantly more dimorphic than the Lemuriformes. Differences in dimorphism between higher taxonomic groups are discussed in the context of prosimian evolution, concluding that phylogenetic inertia cannot provide a causal explanation for the evolution of sexual dimorphism. The relative monomorphism of most prosimians may be related to allometric constraints and, especially in the Lemuriformes, to selective forces affecting male and female behavioral strategies.

Development and application of a phylogenomic toolkit: Resolving the evolutionary history of Madagascar’s lemurs

Lemurs and the other strepsirrhine primates are of great interest to the primate genomics community due to their phylogenetic placement as the sister lineage to all other primates. Previous attempts to resolve the phylogeny of lemurs employed limited mitochondrial or small nuclear data sets, with many relationships poorly supported or entirely unresolved. We used genomic resources to develop 11 novel markers from nine chromosomes, representing approximately 9 kb of nuclear sequence data. In combination with previously published nuclear and mitochondrial loci, this yields a data set of more than 16 kb and adds approximately 275 kb of DNA sequence to current databases. Our phylogenetic analyses confirm hypotheses of lemuriform monophyly and provide robust resolution of the phylogenetic relationships among the five lemuriform families. We verify that the genus Daubentonia is the sister lineage to all other lemurs. The Cheirogaleidae and Lepilemuridae are sister taxa and together form the sister lineage to the Indriidae; this clade is the sister lineage to the Lemuridae. Divergence time estimates indicate that lemurs are an ancient group, with their initial diversification occurring around the Cretaceous-Tertiary boundary. Given the power of this data set to resolve branches in a notoriously problematic area of primate phylogeny, we anticipate that our phylogenomic toolkit will be of value to other studies of primate phylogeny and diversification. Moreover, the methods applied will be broadly applicable to other taxonomic groups where phylogenetic relationships have been notoriously difficult to resolve.

Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)?

In contrast to most anthropoid primates, sifakas (Propithecus verreauxi), like many group-living lemurs, exhibit a number of features that deviate from predictions of sexual selection theory. Despite a promiscuous mating system, they lack sexual dimorphism, suggesting that physical combat plays only a minor role in intrasexual competition for receptive females. In this study, we investigated the hypothesis that socioendocrinological mechanisms contribute to suppression of reproductive function of subordinate males. For that purpose, 10 male sifakas from five social groups were observed for 669 focal animal hours for 4 months, including the mating season, in Western Madagascar. Concomitantly 315 fecal samples of these animals were collected and the concentration of immunoreactive testosterone was quantified hy enzymeimmunoassay procedures. Clear dominance relationships existed among coresident males. Testosterone levels of dominant males were significantly higher than those of subordinates during, as well as outside, the mating season. Additionally, the increase in testosterone levels prior to the mating season was more pronounced for dominant than for subordinate males. These findings are in accordance with the hypothesis of suppression of sexual function of subordinate males, probably providing dominant males with ani advantage in sperm competition. If reproductive success is mainly determined by this nonagonistic form of intrasexual competition, the results of this study contribute an important piece to the puzzle of lacking sexual dimorphism in P. verreauxi.

Delimiting Species without Nuclear Monophyly in Madagascar's Mouse Lemurs

Background Speciation begins when populations become genetically separated through a substantial reduction in gene flow, and it is at this point that a genetically cohesive set of populations attain the sole property of species: the independent evolution of a population-level lineage. The comprehensive delimitation of species within biodiversity hotspots, regardless of their level of divergence, is important for understanding the factors that drive the diversification of biota and for identifying them as targets for conservation. However, delimiting recently diverged species is challenging due to insufficient time for the differential evolution of characters—including morphological differences, reproductive isolation, and gene tree monophyly—that are typically used as evidence for separately evolving lineages. Methodology In this study, we assembled multiple lines of evidence from the analysis of mtDNA and nDNA sequence data for the delimitation of a high diversity of cryptically diverged population-level mouse lemur lineages across the island of Madagascar. Our study uses a multi-faceted approach that applies phylogenetic, population genetic, and genealogical analysis for recognizing lineage diversity and presents the most thoroughly sampled species delimitation of mouse lemur ever performed. Conclusions The resolution of a large number of geographically defined clades in the mtDNA gene tree provides strong initial evidence for recognizing a high diversity of population-level lineages in mouse lemurs. We find additional support for lineage recognition in the striking concordance between mtDNA clades and patterns of nuclear population structure. Lineages identified using these two sources of evidence also exhibit patterns of population divergence according to genealogical exclusivity estimates. Mouse lemur lineage diversity is reflected in both a geographically fine-scaled pattern of population divergence within established and geographically widespread taxa, as well as newly resolved patterns of micro-endemism revealed through expanded field sampling into previously poorly and well-sampled regions.

Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus)

The aim of this study was to investigate reproductive strategies and their consequences in gray mouse lemurs (Microcebus murinus), small solitary nocturnal primates endemic to Madagascar. Previous reports of sexual dimorphism in favor of males and females, respectively, a high potential for sperm competition and pheromonal suppression of mating activity among captive males, led us to investigate mechanisms of intrasexual competition in a wild population. Based on 3 years of mark-recapture data, we demonstrate that sexual dimorphism in this species fluctuated annually as a result of independent changes in male and female body mass. Male body mass increased significantly prior to the short annual mating season. Because their testes increased by 100% in the same period and because their canines are not larger than those of females, we suggest that large male size may be advantageous in searching for estrous females and in enabling them to sustain periods of short-term torpor. In contrast to reports from captive colonies, we found no evidence for two morphologically distinct classes of males. Finally, we also show that most adult males are active throughout the cool dry season that precedes the mating season, whereas most adult females hibernate for several months. This is in contrast to other solitary hibernating mammals, where males typically emerge 1–2 weeks before females. Thus, this first extended field study of M.␣murinus clarified previous conflicting reports on sexual dimorphism and male reproductive strategies in this primitive primate by showing that their apparent deviation from predictions of sexual selection theory is brought about by specific environmental conditions which result in sex-specific life history tactics not previously described for mammals. A general conclusion is that sexual selection can operate more strongly on males without resulting in sexual dimorphism because of independent selection on the same traits in females.

Determinants of primate social organization : comparative evidence and new insights from Malagasy lemurs

The aim of this review is to summarize newly available information on lemur social systems, to contrast it with the social organization of other primates and to relate it to existing models of primate social evolution. Because of their evolutionary history, the primates of Madagascar constitute a natural experiment in social evolution. During millions of years of isolation, they converged with other primates only in the most fundamental way in the evolution of solitary, pair‐living and group‐living species, but deviate in several respects within these basic categories of social organization. Solitary lemurs remain poorly studied, but their social organization appears to be broadly similar to that of other solitary primates, even though the unexpected lack of sexual dimorphism may indicate that similar types of social organization can give rise to different mating systems. The determinants of a solitary lifestyle remain elusive. Pair‐living lemurs show striking convergences with other monogamous primates in several behavioural traits, but also deviate in that the majority of species are at least partly nocturnal and do not exhibit direct paternal care of dependent young. Group‐living lemurs have not evolved single‐male groups, male‐bonded and multi‐level societies, and polyandrous groups may also be lacking. Female philopatry is common, but female bonds are generally weakly developed and eviction of females from natal groups is not unusual. Group‐living lemurs also differ from anthropoids in that their groups have even adult sex ratios, smaller average size and may split up on a seasonal basis. Feeding competition, predation risk and reproductive competition can not fully explain these unusual aspects of lemur social organization. It has therefore been suggested that the social consequences of the risk of infanticide and of recent changes in activity may be ultimately responsible for these idiosyncracies of group‐living lemurs, an explanation largely supported by the available evidence. Thus, social factors and fundamental life‐history traits, in addition to ecological factors, contribute importantly to variation in social systems among lemurs, and possibly other primates. However, neither the diversity of lemur social systems, nor the evolutionary forces and mechanisms operating in these and other primates are yet fully understood.