Infanticide and the evolution of pair bonds in nonhuman primates

Social relationships between adult males and females vary widely among mammals. In general, interactions between the sexes, particularly those of an affiliative nature, are associated with and, indeed, often limited to the period of copulation or female estrus.¹ Nevertheless, cohesive male-female bonds persist beyond estrus in some species, particularly nonhuman primates,² for reasons that remain largely obscure. Protection from male infanticide has been offered as a potential benefit to females of bonds with males in a variety of primates, including mountain gorillas and gibbons. Here I evaluate this hypothesis within a comparative framework that considers alternative costs and benefits of social relationships between the sexes.     

Females drive primate social evolution

Within and across species of primates, the number of males in primate groups is correlated with the number of females. This correlation may arise owing to ecological forces operating on females, with subsequent competition among males for access to groups of females. The temporal relationship between changes in male and female group membership remains unexplored in primates and other mammalian groups. We used a phylogenetic comparative method for detecting evolutionary lag to test whether evolutionary change in the number of males lags behind change in the number of females. We found that change in male membership in primate groups is positively correlated with divergence time in pairwise comparisons. This result is consistent with male numbers adjusting to female group size and highlights the importance of focusing on females when studying primate social evolution.     

Determinants of behavioral rhythmicity during artificial menstrual cycles in rhesus monkeys (Macaca mulatta)

Reproductive success in many mammals depends on synchrony between copulation and ovulation, which is insured by the phenomenon of heat in the female. Certain anthropoid primates including rhesus monkeys do not show heat but may copulate throughout the menstrual cycle, especially when pairs are isolated from conspecifics. In social groups, however, mating mostly occurs around midcycle. We wished to test the hypothesis that copulations are more closely linked to ovulation when males have simultaneous access to several females in different cycle phases. Artificial menstrual cycles were therefore induced by giving hormones to ovariectomized female rhesus monkeys observed in small social groups that each consisted of four females and one male. The cycles of two hormone-treated femlab in each group were either made to synchronize or be offset by 7-day increments so that the estradiol peak of one female occurred 7 days before, and 7 and 14 days after, the estradiol peak of the other. Radioimmunoassay of plasma samples (N = 224) confirmed the timing of the estradiol peaks. Results from eight unique male-female groups (4 males, 8 females, 16 male-female pairs, 718 tests) fully supported the hypothesis. Compared with synchronized cycles, the amplitudes of rhythmic changes in offset cycles were reduced for ejaculations made by males but greatly enhanced for ejaculations received by females. We propose that this socio-hormonal integration of behavior in the group is highly adaptive and enhances the reproductive success of both males and females.     

Demography and life history of Thomas langurs (Presbytis thomasi)

Life history data from wild primate populations are necessary to explain variation in primate social systems and explain differences between primates and other mammals. Here we report life history data from a 12.5-year study on wild Thomas langurs. Mean age at first reproduction was 5.4 years and the sex ratio at birth was even. The mean interbirth interval (IBI) after a surviving infant was 26.8 mo, after nonsurviving infants 17.7 mo, and combined 22.0 mo. Mean annual birth rate of adult females was 0.44, while reaching a peak at 6 years of age and showing no decrease with age. Mortality was highest during the first year of life (48.0% for males and 43.0% for females) and consistently higher for males than females. The oldest female observed during the study was estimated to be 20 years of age, whereas the oldest male disappeared at age 13 years, indicating that males die at a much earlier age than females. A Leslie matrix based on these estimates yielded a growth rate of 1.01, which is comparable to the nonsignificant increase in density indicated by our long-term field data. A comparison with life history data for sympatric frugivorous primates suggests that folivory might be associated with faster life history.     

Dominance,Coloration, and Social and Sexual Behavior in Male Drills <Emphasis Type="Italic">Mandrillus leucophaeus</Emphasis>

Sexual selection has driven the evolution and elaboration of a wide variety of displays and ornaments in male nonhuman primates, including capes, cheek flanges, and sexual coloration. Among the most sexually dimorphic of all primates is the drill (Mandrillus leucophaeus), the males of which can be 3 times the mass of females, possess large canines, and exhibit extremely bright sexual skin coloration. However, the function of male coloration in this species has never been examined. Here, we present data on male color (measured objectively using digital photography), dominance rank, measures of male-female association, and key sexual behaviors, of adult male drills (n = 17) living in four semi free-ranging enclosures at the Drill Rehabilitation and Breeding Center in Nigeria. We test the hypothesis that male coloration is a badge of status, indicating dominance rank, and the hypothesis that male coloration attracts females. We found that male coloration did indicate rank, and that high ranking, strongly colored males were more likely to associate with adult females, and more specifically with fully tumescent females. These males also engaged in more sexual activity. However, measures of male-female association and sexual behaviors were not related to male color once rank had been taken into consideration; i.e., for males of a given rank, females did not prefer those that were more colorful. We discuss the results in light of what is known about the wild drill social system, in which unfamiliar individuals may come together in “supergroups,” and in which quality indicators of competitive ability may be particularly important.     

Primate socioecology at the crossroads: Past, present, and future

Attempts to explain differences in the size and structure of primate groups have argued that they are a consequence of variation in the intensity of feeding competition caused by contrasts in food distribution. However, although feeding competition can limit the size of female groups, many other factors affect the costs and the benefits of sociality to females and contribute to differences in group size. Moreover, interspecific differences in social relationships between females, in female philopatry, and in kinship between group members appear to be more closely associated with variation in life‐history parameters, reproductive strategies, and phylogeny than with contrasts in food distribution or feeding competition. The mismatch between predictions of socioecological theory and observed variation in primate social behavior has led to protracted arguments about the future of primate socioecology. We argue that future attempts to understand the diversity of primate societies need to be based on an approach that explores separate explanations for different components of social organization, combines ecological and phylogenetic information, and integrates research on primates with similar studies of other groups of mammals. © 2012 Wiley Periodicals, Inc.     

The hidden matrilineal structure of a solitary lemur: implications for primate social evolution

Kin selection affects many aspects of social behaviour, especially in gregarious animals in which relatives are permanently associated. In most group-living primates with complex social behaviour, females are philopatric and organized into matrilines. Models of primate social evolution assume that females in solitary primates are also organized into matrilines. We examined the genetic structure and the mating system of a population of Coquerel's dwarf lemur (Mirza coquereli), a solitary primate from Madagascar, to test this assumption. Our genetic and behavioural analyses revealed that this population of solitary individuals is indeed structured into matrilines, even though this pattern was not predicted by behavioural data. Specifically, females sharing a mitochondrial DNA haplotype were significantly clustered in space and the average genetic and geographical distances among them were negatively correlated. Not all females were philopatric, but there is no evidence for the successful settlement of dispersing females. Although not all adult males dispersed from their natal range, they were not significantly clustered in space and all of them roamed widely in search of oestrous females. As a result, paternity was widely spread among males and mixed paternities existed, indicating that scramble competition polygyny is the mating system of this species. Our data therefore revealed facultative dispersal in both sexes with a strong bias towards female philopatry in this primitive primate. We further conclude that complex kinship structures also exist in non-gregarious species, where their consequences for social behaviour are not obvious.     

Social organization of the Milne-Edward's potto

Nocturnal prosimian primates are often seen alone during their nocturnal activities, and are therefore categorized as "solitary". Recent research has shown that these animals actually possess social networks that differ among species. Here we present new information on one of the lesser studied prosimian primates, the potto, derived from fieldwork in Cameroon that employed radiotelemetry and behavioral observations. An analysis of association patterns and home-range overlaps between animals revealed that pottos associated more frequently with conspecifics than expected for a supposedly solitary primate. Certain males and females that were seen together regularly throughout the study, but were not observed to have contact with other pottos of the opposite sex, were labeled as "pairs". These pairs were found to have higher levels of association with each other than with other conspecifics. The only affiliative and sexual behaviors observed between members of the opposite sex occurred within the pairs of pottos. Although given the secretive nature of these primates, the possibility of extrapair copulations cannot be ruled out, their relatively small testis size indicates that sperm competition is not so important for this species.     

Sex differences in vocal communication among adult rhesus macaques

In female-bonded primate species, females invest more time in grooming than males, and the majority of this grooming occurs in intra- rather than intersexual interactions. These clear sex differences in sociability reflect females' need to forge and maintain complex networks of social relationships with other females in the group. Increasing evidence indicates that vocal signals can have a similar function to grooming in mediating social interactions and relationships, and sex differences in patterns of use of vocal communication comparable to those seen for grooming might therefore be expected to occur. In this study of free-ranging adult rhesus macaques, we tested for such patterns, focusing on the frequency of utterance of three types of vocalisations given during close-range social interactions: coos, grunts, and girneys. As predicted, we found that females gave such calls significantly more frequently than males and also directed more of these vocalisations towards other females than to males; males' rate of vocalising towards the two sexes was not significantly different. To our knowledge, these results provide the first evidence for a sex difference in the rate of production of social vocalisations among adult nonhuman primates. The finding that increased sociability is associated with increased reliance on vocal communication may have important implications for theories of language evolution.     

The Social Systems of Gregarious Lemurs: Lack of Convergence with Anthropoids due to Evolutionary Disequilibrium?

The gregarious lemurs of Madagascar show a lack of convergence with anthropoid primates in several social, demographic, morphological and ecological features. They lack sexual dimorphism in canine and body size, and live in groups with equal adult sex ratios that can vary in composition from pairs to larger units. In most species, females dominate males, and have brief and often synchronized estruses. Finally, lemurs are often active during both day and night (i.e. cathemeral). Three hypotheses for this lack of convergence are discussed. The traditional explanation is that Madagascar's unique ecological pressures have forced females to exclude males from access to limiting resources, selecting for the other unique features as means to maintain female dominance over males. This idea is not logically consistent and is also poorly supported empirically. The second hypothesis claims that cathemerality imposes unique constraints on lemur social organization. The social behavior of cathemeral taxa is largely consistent with this idea. However, the social organization of the diurnal species is not. The third hypothesis claims that recent ecological changes, in particular the demise of large diurnal raptors, have produced a mismatch between current activity periods and adaptations to activity period. This idea is supported by a review of morphological adaptations to light conditions among lemurs, and, more generally, by a comparative analysis of cathemerality among tropical forest mammals. We conclude that the social systems of non-nocturnal lemurs are best considered as groups formed by species adapted to live in pairs. However, we cannot conclusively exclude the possibility that cathemeral activity is an old and stable activity pattern among lemurs. We indicate which data would decide the issue, and discuss the implications for views of social evolution of lemurs and other animals.     

Female macaques compete for ‘power’ and ‘commitment’ in their male partners

The formation of male-female social bonds and the resulting competition among females for male partners is a core element of human societies. While female competition for a male partner outside the mating context is well studied in humans, evidence from non-human primates is scarce, and its evolutionary roots remain to be explored. We studied two multi male – multi female groups of wild Assamese macaques (Macaca assamensis), a species where females gain benefits from selectively affiliating with particular males. Using a behavioral data set collected over several years, we tested whether females competed over access to male social partners, whether success in competition was driven by female dominance rank, and which male traits were most attractive for females. We found assortative bonding by dominance rank between females and males, which together with females initiating and maintaining contact suggests direct female competition over males. Two male traits independently predicted male attractiveness to females: (1) current dominance rank, a measure of 'power' or a male's ability to provide access to resources, and (2) prior male affiliation with immatures, a measure of a male's potential paternal proclivity or 'commitment' to infant care. Both traits have been consistently identified as drivers of female partner choice in humans. Our study adds to the evidence that female competition for valuable male partners is not unique to humans, suggesting deep evolutionary origins of women's mate choice tendencies for ‘power’ and ‘commitment’.     

Effects of the distribution of female primates on the number of males

The spatiotemporal distribution of females is thought to drive variation in mating systems, and hence plays a central role in understanding animal behavior, ecology and evolution. Previous research has focused on investigating the links between female spatiotemporal distribution and the number of males in haplorhine primates. However, important questions remain concerning the importance of spatial cohesion, the generality of the pattern across haplorhine and strepsirrhine primates, and the consistency of previous findings given phylogenetic uncertainty. To address these issues, we examined how the spatiotemporal distribution of females influences the number of males in primate groups using an expanded comparative dataset and recent advances in bayesian phylogenetic and statistical methods. Specifically, we investigated the effect of female distributional factors (female number, spatial cohesion, estrous synchrony, breeding season duration and breeding seasonality) on the number of males in primate groups. Using bayesian approaches to control for uncertainty in phylogeny and the model of trait evolution, we found that the number of females exerted a strong influence on the number of males in primate groups. In a multiple regression model that controlled for female number, we found support for temporal effects, particularly involving female estrous synchrony: the number of males increases when females are more synchronously receptive. Similarly, the number of males increases in species with shorter birth seasons, suggesting that greater breeding seasonality makes defense of females more difficult for male primates. When comparing primate suborders, we found only weak evidence for differences in traits between haplorhines and strepsirrhines, and including suborder in the statistical models did not affect our conclusions or give compelling evidence for different effects in haplorhines and strepsirrhines. Collectively, these results demonstrate that male monopolization is driven primarily by the number of females in groups, and secondarily by synchrony of female reproduction within groups.     

Postcanine tooth size in female primates

The results of many allometric studies of postcanine tooth size in mammals have not corresponded to expectations of tooth size based on energy requirements and dental function. The purpose of this study is to investigate the relationship between postcanine occlusal surface area, body size, and the metabolic demands of pregnancy and lactation in female primates. Tooth and body sizes from 38 primate species were taken from the literature to test two hypotheses: 1) females should have relatively larger teeth than males in order to masticate additional food for the energetic costs of reproduction; 2) taxa with the largest neonatal size (a measure of average metabolic costs of pregnancy and lactation) should have females with a greater degree of relative dental enlargement. The results show that relatively large female teeth are not found consistently in primate species. Females have less occlusal surface area than expected on the basis of the male tooth and body size regression in 21% of the species, and there is no correlation between relative female tooth size and relative newborn size across higher primate taxa. The degree of female dental enlargement is most closely related to degree of sexual dimorphism in body weight. The correlation between degree of body weight dimorphism and relatively larger postcanine teeth in females than in males is 0.87 in the 38 species. Species that are monomorphic in weight tend to be monomorphic in tooth size even though females apparently require more food than males.(ABSTRACT TRUNCATED AT 250 WORDS)     

Male × female interaction for a pre-copulatory trait, but not a post-copulatory trait, among cosmopolitan populations of Drosophila melanogaster

Sexual coevolution occurs when changes in the phenotype of one sex select for changes in the other sex. We can identify the "footprint" of this coevolution by mating males and females from different populations and testing for a male-female genotype interaction for a trait associated with male (or female) performance. Here we mated male Drosophila melanogaster from five different continents with females from their own and different continents to test for a male-female interaction for mating speed, a pre-copulatory trait, and female reproductive investment, a post-copulatory trait. We found a strong male-female interaction for mating speed, consistent with previous studies using different populations, suggesting that the potential for sexual coevolution for this trait is present in this species. In contrast, we did not detect a male-female interaction for female reproductive investment. Although a male-female interaction for mating speed is compatible with the hypothesis of ongoing sexual coevolution, the nature of our experimental design is unable to exclude alternate explanations. Thus, the evolutionary mechanisms promoting male-female genotype interactions for pre-copulatory mating traits in D. melanogaster warrant further investigation.     

Paternity Recognition in Multi-male Primate Groups

A traditional view of multi-male primate groups has held thatmales provide relatively little direct care to infants, possiblyas a result of low confidence of paternity associated with arelatively promiscuous breeding system. In the last five yearsthis view has changed as a result of a careful documentationof intimate male-infant affiliations in certain species, especiallythe savanna-dwelling baboons (Papio spp.). The occurrence ofthese affiliations raises the question as to whether males carefor their own offspring preferentially and, if so, on what basismale confidence of paternity is mediated. Recent field studiesof baboons suggest that male-infant relationships are mediatedthrough affiliations between the males and the infants' mothers,but the degree to which these male-female affiliations are basedon prior mating experience (hence, paternity) has not been established. Comparative studies of male-infant relations in primates havegiven little attention to the variation in the intensity andform of male care patterns within the set of species that havea multi-male social organization. Among multi-male species,male care of young is reported most often in baboons and barbarymacaques (Macaca sylvanus) and least often in other macaques,chimpanzees (Pan troglodytes), and vervet monkeys (Cercopithecus).This interspecific variation may result both from differencesin the importance of male care to infant survival and from differencesin male confidence of paternity, which in turn may relate toseasonal breeding patterns and, in particular, to the presenceor absence of conspicuous signs of ovulation in females.     

Derived vocalizations of geladas (Theropithecus gelada) and the evolution of vocal complexity in primates

Primates are intensely social and exhibit extreme variation in social structure, making them particularly well suited for uncovering evolutionary connections between sociality and vocal complexity. Although comparative studies find a correlation between social and vocal complexity, the function of large vocal repertoires in more complex societies remains unclear. We compared the vocal complexity found in primates to both mammals in general and human language in particular and found that non-human primates are not unusual in the complexity of their vocal repertoires. To better understand the function of vocal complexity within primates, we compared two closely related primates (chacma baboons and geladas) that differ in their ecology and social structures. A key difference is that gelada males form long-term bonds with the 2-12 females in their harem-like reproductive unit, while chacma males primarily form temporary consortships with females. We identified homologous and non-homologous calls and related the use of the derived non-homologous calls to specific social situations. We found that the socially complex (but ecologically simple) geladas have larger vocal repertoires. Derived vocalizations of geladas were primarily used by leader males in affiliative interactions with 'their' females. The derived calls were frequently used following fights within the unit suggesting that maintaining cross-sex bonds within a reproductive unit contributed to this instance of evolved vocal complexity. Thus, our comparison highlights the utility of using closely related species to better understand the function of vocal complexity.     

Canine size, shape, and bending strength in primates and carnivores

Anthropoid primates are well known for their highly sexually dimorphic canine teeth, with males possessing canines that are up to 400% taller than those of females. Primate canine dimorphism has been extensively documented, with a consensus that large male primate canines serve as weapons for intrasexual competition, and some evidence that large female canines in some species may likewise function as weapons. However, apart from speculation that very tall male canines may be relatively weak and that seed predators have strong canines, the functional significance of primate canine shape has not been explored. Because carnivore canine shape and size are associated with killing style, this group provides a useful comparative baseline for primates. We evaluate primate maxillary canine tooth size, shape and relative bending strength against body size, skull size, and behavioral and demographic measures of male competition and sexual selection, and compare them to those of carnivores. We demonstrate that, relative to skull length and body mass, primate male canines are on average as large as or larger than those of similar sized carnivores. The range of primate female canine sizes embraces that of carnivores. Male and female primate canines are generally as strong as or stronger than those of carnivores. Although we find that seed-eating primates have relatively strong canines, we find no clear relationship between male primate canine strength and demographic or behavioral estimates of male competition or sexual selection, in spite of a strong relationship between these measures and canine crown height. This suggests either that most primate canines are selected to be very strong regardless of variation in behavior, or that primate canine shape is inherently strong enough to accommodate changes in crown height without compromising canine function.     

Nepotistic cooperation in non-human primate groups

Darwin was struck by the many similarities between humans and other primates and believed that these similarities were the product of common ancestry. He would be even more impressed by the similarities if he had known what we have learned about primates over the last 50 years. Genetic kinship has emerged as the primary organizing force in the evolution of primate social organization and the patterning of social behaviour in non-human primate groups. There are pronounced nepotistic biases across the primate order, from tiny grey mouse lemurs (Microcebus murinus) that forage alone at night but cluster with relatives to sleep during the day, to cooperatively breeding marmosets that rely on closely related helpers to rear their young, rhesus macaque (Macaca mulatta) females who acquire their mother''s rank and form strict matrilineal dominance hierarchies, male howler monkeys that help their sons maintain access to groups of females and male chimpanzees (Pan troglodytes) that form lasting relationships with their brothers. As more evidence of nepotism has accumulated, important questions about the evolutionary processes underlying these kin biases have been raised. Although kin selection predicts that altruism will be biased in favour of relatives, it is difficult to assess whether primates actually conform to predictions derived from Hamilton''s rule: br > c. In addition, other mechanisms, including contingent reciprocity and mutualism, could contribute to the nepotistic biases observed in non-human primate groups. There are good reasons to suspect that these processes may complement the effects of kin selection and amplify the extent of nepotistic biases in behaviour.     

Neocortex size predicts deception rate in primates

Human brain organization is built upon a more ancient adaptation, the large brain of simian primates: on average, monkeys and apes have brains twice as large as expected for mammals of their size, principally as a result of neocortical enlargement. Testing the adaptive benefit of this evolutionary specialization depends on finding an association between brain size and function in primates. However, most cognitive capacities have been assessed in only a restricted range of species under laboratory conditions. Deception of conspecifics in social circumstances is an exception, because a corpus of field data is available that encompasses all major lines of the primate radiation. We show that the use of deception within the primates is well predicted by the neocortical volume, when observer effort is controlled for; by contrast, neither the size of the rest of the brain nor the group size exert significant effects. These findings are consistent with the hypothesis that neocortical expansion has been driven by social challenges among the primates. Complex social manipulations such as deception are thought to be based upon rapid learning and extensive social knowledge; thus, learning in social contexts may be constrained by neocortical size.