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.     

Violent coalitionary attack by female mandrills against an injured alpha male

Female contact aggression against males is relatively rare in species in which the adult males are larger than the females, but it has the potential to influence group structure, male group membership, tenure, and dominance rank. We report an incident in which female mandrills living in a semi-free-ranging group in Franceville, Gabon, attacked a male that was apparently incapacitated after a fight with another male and was unable to escape. The attack involved the alpha male and did not occur in a sexual or infanticidal context. Other adult and adolescent males observed the attack, but when one adult male attempted to participate he was chased away by the females. This observation adds to reports of female coalitions excluding unwanted males from primate groups, or even killing them. The fact that this can also occur in mandrills suggests that females have a degree of control over male group membership, despite the large degree of sexual dimorphism in this species, and highlights the importance of coalitions in primate social organization.     

Neocortex evolution in primates: the "social brain" is for females

According to the social intelligence hypothesis, relative neocortex size should be directly related to the degree of social complexity. This hypothesis has found support in a number of comparative studies of group size. The relationship between neocortex and sociality is thought to exist either because relative neocortex size limits group size or because a larger group size selects for a larger neocortex. However, research on primate social evolution has indicated that male and female group sizes evolve in relation to different demands. While females mostly group according to conditions set by the environment, males instead simply go where the females are. Thus, any hypothesis relating to primate social evolution has to analyse its relationship with male and female group sizes separately. Since sex-specific neocortex sizes in primates are unavailable in sufficient quantity, I here instead present results from phylogenetic comparative analyses of unsexed relative neocortex sizes and female and male group sizes. These analyses show that while relative neocortex size is positively correlated with female group size, it is negatively, or not at all correlated with male group size. This indicates that the social intelligence hypothesis only applies to female sociality.     

Number of males in primate groups: Comparative tests of competing hypotheses

Primate social groups frequently contain multiple males. Male group size has been hypothesized to result from male mating competition, but the selective factors responsible for the evolution of multimale groups are unclear. Short breeding seasons create situations that are not conducive for single males to monopolize mating access to females, and may therefore favor the formation of large male groups. Alternatively, since the costs of mate defense increase with the spatial clumping of females, female group size may be a primary determinant of the number of males in a primate group. We used comparative methods designed to control for the potentially confounding effects of hidden third variables associated with phylogeny to test the breeding season and female group size hypotheses for the evolution of multimale groups. Our results revealed no association between breeding season duration and the number of males in groups. In contrast, we provide support for the female group size hypothesis by demonstrating a strong pattern of correlated evolution between female and male group size. © 1996 Wiley-Liss, Inc.     

Male Competition,Mating Success and Female Choice in a Seasonally Breeding Primate (Erythrocebus patas)

Mammals with restricted breeding seasons often show brief but intense bouts of male competition for mates and male reproductive success has been attributed to male competitive abilities, with the most aggressively successful males able to control access to fertile females, or with females choosing to mate with such males. We studied male competition, mating behaviour and female mate selection in patas monkeys, a primate with a restricted breeding period. We observed two habituated patas groups in Laikipia District, Kenya, during Jun.-Aug. 1983. During the study, one group had a single resident male while the other group had multiple adult males. Within the multimale group, experienced adult males were no more successful than the subadult male. The sole resident male had a significantly higher rate of fights won (p < 0.02) although he did not differ from the multimale group males in rate of aggression or initiation of fights. We found no significant differences in either mating success or female preference based on males' experience or residency. The rates at which males copulated with and were solicited by females were not significantly correlated. We found no evidence of stable dominance ranks among males in the multimale group and aggressive success was not significantly correlated with copulation rate for males in the multimale group. Subadult males were responsible for the majority of copulations observed during the final third of the breeding season. Our observations of this patas population showed a fluid number of males in groups, with the same groups able to shift rapidly from single to multimale structure. This fluidity may result from the large fluctuations in numbers of breeding-age males and females observed over 4 yr of studying this population.     

Network cohesion,group size and neocortex size in female-bonded Old World primates

Most primates are intensely social and spend a large amount of time servicing social relationships. In this study, we use social network analysis to examine the relationship between primate group size, total brain size, neocortex ratio and several social network metrics concerned with network cohesion. Using female grooming networks from a number of Old World monkey species, we found that neocortex size was a better predictor of network characteristics than endocranial volumes. We further found that when we controlled for group size, neocortex ratio was negatively correlated with network density, connectivity, relative clan size and proportional clan membership, while there was no effect of neocortex ratio on change in connectivity following the removal of the most central female in the network. Thus, in species with larger neocortex ratios, females generally live in more fragmented networks, belong to smaller grooming clans and are members of relatively fewer clans despite living in a closely bonded group. However, even though groups are more fragmented to begin with among species with larger neocortices, the removal of the most central individual does cause groups to fall apart, suggesting that social complexity may ultimately involve the management of highly fragmented social groups while at the same time maintaining overall social cohesion. These results emphasize a need for more detailed brain data on a wider sample of primate species.     

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.     

Dominance and reproductive success among nonhuman animals: A cross-species comparison

This paper updates and extends Dewsbury's (1982) review of the literature on dominance and reproductive success (RS). The findings from approximately 700 studies are included, over two thirds of which were unavailable to Dewsbury. In order to give a highly condensed and yet meaningful overview, the main findings are represented in four tables, one for male nonprimates, one for female nonprimates, one for male primates, and one for female primates. In the tables for males, findings are analyzed in terms of six different indicators of RS, and in the tables for females, in terms of eight RS indicators.Outside the primate order, evidence largely supported the hypothesis that high-ranking males enjoy greater RS than do subordinate males. For females, studies are more evenly divided between those supporting the hypothesis that high rank and RS are positively correlated and those indicating no significant rank-RS relationship. This may reflect both the lower saliency of hierarchical relationships among females, as well as the lower variability in RS among females, relative to males.Among primates, a complex picture has emerged, especially in the case of males. Much of the complexity appears due to the importance of age and seniority in affecting dominance rank. Also, in some primate species, female preferences for sex partners seem to have little to do with the male's dominance rank, at least at the time mating takes place. Nevertheless, the majority of studies suggest that high- to middle-ranking males have at least a slight lifetime reproductive advantage over the lowest ranking males.     

New World primates,new frontiers: Insights from the woolly spider monkey,or muriqui (Brachyteles arachnoides)

Despite over 25 years of intensive research, much of our knowledge of primate behavior has been limited to a small number of Old World, semiterrestrial species. With the exception of chimpanzees, these species share consistent patterns of behavior, including aggressive competition between males, male dominance over females, male dispersal and female kin groups, that have come to characterize the Order Primates. However, as research has expanded to include a number of newly studied species, such generalizations about primate behavior are no longer appropriate. Data presented on the wooly spider monkey, or muriqui (Brachyteles arachnoides), provide examples of the ways in which traditional views of primate behavior are being reconsidered. In muriquis, and in several other New World monkeys, female kin groups do not occur because females disperse from their natal groups. In addition, aggressive competition between males is virtually absent; and, female muriquis appear to be codominant with males. Constraints on sexual dimorphism may help to explain why muriquis (and other New World primates) differ so fundamentally from the better known semi-terrestrial Old World monkeys.Logo of the 1988 International Primatological Society.     

The social structure of primates

A comprehensive comparative study of the social structure of primates revealed: There is no social structure which can be considered typical and discriminative for primates. The varying social structures of the extant primate genera cannot be derived from each other: In contrast it seems that the basic, ancestral condition was that of solitary living animals, loosely aggregated. It can be assumed that the development to a gregarious society took place in two entirely different ways. In terms of primate phylogeny this different development can be shown for the prosimians as well as for the old world and new world monkeys as independently occurring processes. One way of behavioral specialization resulted in close pair bonds or in small family groups, whereas the other led to female groups. The presupposition for the forming of a society based on female groups is the close contact between the individuals and in addition to this, a remarkable social tolerance of females to each other. Social specializations which can be considered transitional from the basic condition are frequently found in prosimians. The kinds of social structures of the particular genera are in close relation to their taxonomic positions in the phylogenetic scala. The number of males in larger social groups of primates is substantially irrelevant as the groups are socially most dependent on the females. The protecting males are socially peripheral. The social units of most of the primate species are matrilocal and endure for several generations. In contrast, the social units of the gibbons and of the pongids are patrilocal and are established anew by the females in each generation. Consequently the social unit disintegrates on the death of the male. In all genera studied, male and female individuals present considerable behavioral differences which can be found even in juveniles. Primates are able to discriminate well known and confident individuals from other less confident; they prefer more confident individuals to less confident ones, and less confident to non-confident. As a consequence of this discriminative ability there is a clear preference for near when compared to distant relatives. The complexity of the social relations is brought about by this ability to discriminate combined with the longevity of primates. This is a characteristic and discriminative feature of the primate order. Dominance relations occur in every social group of primates. Linear hierarchies of dominance have been developed only once in prosimians (Lemur) and also once in simians (Cercopithecinae). Therefore, liner hierarchies are not typical for primates.     

Inbreeding Avoidance in Male Primates: A Response to Female Mate Choice?

Inbreeding often has negative fitness consequences for primates, which have led to the evolution of inbreeding avoidance strategies in a number of species. In polygynous primates, females may suffer a higher fitness cost from inbreeding than males and are thus expected to exhibit a lower tolerance for inbreeding. Nevertheless, it is apparent that inbreeding avoidance behaviours are common in both female and male polygynous primates. In this perspectives article, I review the evidence that female mate choice can lead to male inbreeding avoidance behaviours in polygynous primates. I conclude that male inbreeding avoidance may be strongly driven by female mate choice at both proximate and ultimate levels. To better understand the extent to which this pattern applies across the primate order, studies are needed on the separate effects of participating in inbred matings and producing inbred offspring on male and female lifetime reproductive success . It would also be useful to examine how inbreeding avoidance strategies vary across primate mating systems. Finally, measuring the covariance between female choice and male inbreeding avoidance behaviour, and between male inbreeding avoidance behaviour and male fitness, would help to clarify the role of female mate choice in the evolution of male inbreeding avoidance.     

Male-Driven Differences in Chimpanzee (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) Population Genetic Structure Across Three Habitats in Cameroon and Nigeria

Complex ecological pressures affect the social dynamics of many primate species, but it is unclear how they affect primate speciation. Molecular tools are often used to answer questions about the evolutionary histories and social systems of primates. Mitochondrial DNA (mtDNA), in particular, is frequently used to answer many of these questions, but because it is passed from mothers to offspring it reveals only the histories of females. In many species, including chimpanzees, females generally disperse from their natal groups while males are philopatric, and thus differences in dispersal patterns likely leave different signatures in the genome. We previously analyzed samples from 187 unrelated male and female chimpanzees in Nigeria and Cameroon using 21 autosomal microsatellites and mtDNA sequences. Here, we examine the contributions of males and females in shaping the genetic history of these chimpanzees by genotyping a subset of 56 males at 12 Y-chromosome microsatellites. We found that Y-chromosome population structure differed from the results of analysis of mtDNA haplotypes. The results also revealed that males in rainforest habitats (Guinean and Congolian rainforests) are more closely related to one another than those inhabiting the savanna-woodland mosaic ecotone in central Cameroon. In contrast, the pattern of female relatedness did not differ across habitats. We hypothesize that these differences in population structure and patterns of relatedness among males in different habitat types may be due to differences in the community dynamics of chimpanzees in the ecotone vs. rainforests, and that these factors contribute to making Cameroon an engine of diversification for chimpanzees. Broadly, these results demonstrate the importance of habitat variation in shaping social systems, population genetics, and primate speciation.     

Female Reproductive Seasonality and Male Influxes in Wild Mandrills (<Emphasis Type="Italic">Mandrillus sphinx</Emphasis>)

The correlates of variation in the number of males in primate groups form a long-standing question in primatology. We investigated female reproductive seasonality and the numbers of males in groups of wild mandrills (Mandrillus sphinx) in a 25-month camera-trap survey with 160 camera locations in Moukalaba-Doudou National Park, Gabon. We used 1760 videos to analyze group composition, including the presence of females with newborn infants and with sexual swellings, the number of males present in groups, and male spatial positioning in groups. Female reproduction was seasonal, with a peak in the number of newborns in the mid-rainy season and a peak in the number of females with sexual swellings in the early dry season. The number of males in the group increased in the dry season, with a much greater increase in the number of mature males (sevenfold) than in submature males (twofold). The peak number of mature males, but not submature males, in the group lagged significantly behind the peak in the number of females with sexual swellings, suggesting that submature males enter groups before mature males and/or that mature males stay in the group longer after the peak of females with sexual swellings. Mature, but not submature, males appeared frequently near females with sexual swellings. In conclusion, we found a clear relationship between the presence of receptive females and the number of males in the group, and evidence that male competitive ability influences male strategies.     

Do Female Mandrills Prefer Brightly Colored Males?

Although secondary sexual adornments are widespread in male primates, few studies have examined female choice for these characters. Mandrills (Mandrillus sphinx) present an extreme example of sexual dimorphism, with males exhibiting an array of striking adornments. The most dominant adult male in a group exhibits the brightest and most extensive red coloration, while the other males are less brightly colored. I examined whether female mandrills prefer brightly colored males using data on periovulatory sexual behavior during the 1996 mating season for all males 8 years old (n = 5) and all parous females (n = 9) in a semifree-ranging colony at CIRMF, Gabon. Brightness of male coloration is significantly positively correlated with time spent within 2 m of females, female responsibility for proximity, number of sexual presentations received, % approaches accepted by females, and % inspections with which females cooperated. Females also groomed only the brightest male. Behaviors indicating female preference are not correlated significantly with male dominance rank, and partial correlations confirm that the influence of male color on female behavior is stronger than that of male rank. With the influence of male dominance rank controlled, correlation coefficients between female behaviors and male mating success are high and positive. In further support of the hypothesis that females show mate choice for brightly colored males, independent of dominance rank, I report an unusual case wherein the alpha male fell in rank without loss of coloration. He experienced no significant change in female responsibility for proximity, sexual presentations received, or female reaction to approaches or inspections, though he was no longer observed to mate. Accordingly, female mandrills attend to differences in male secondary sexual characters and favor brightly colored males. As brightly colored males are also dominant this reinforces the influence of male-male competition on male reproductive success and may explain the very high reproductive skew in mandrill males and their extraordinary appearance.     

Evolution of human growth spurts

This study investigates subadult growth spurts in a large sample of anthropoid primates, including humans. Analyses of body mass growth curves show that humans are not unique in the expression of female and male body mass growth spurts. Subadult growth spurts are observed in both New World and Old World anthropoid primates and are more common in males than in females. Allometric analyses of growth spurts indicate that many aspects of primate growth spurts are strongly correlated with species size. Small species tend not to exhibit growth spurts. Although male and female scaling patterns for velocity and size measures are comparable, scaling relations of variables that measure the timing of growth spurts differ by sex. These patterns can he related to sexual differences in life histories. Scaling analyses further show that humans do not depart substantially from patterns that describe other anthropoid primates. Thus, in relative terms, human growth spurts are not exceptional compared to this sample of primates. The long absolute delay in the initiation of the human growth spurt may be of substantial evolutionary importance and serves to distinguish humans from other primates. In essence, humans exhibit growth spurts that are comparable to other primates in many respects. However, human growth spurts are shifted to very late absolute ages. © 1996 Wiley-Liss, Inc.     

Comparison of the social systems of primates and feral horses: data from a newly established horse research site on Serra D’Arga,northern Portugal

Horses are phylogenetically distant from primates, but considerable behavioral links exist between the two. The sociality of horses, characterized by group stability, is similar to that of primates, but different from that of many other ungulates. Although horses and primates are good models for exploring the evolution of societies in human and non-human animals, fewer studies have been conducted on the social system of horses than primates. Here, we investigated the social system of feral horses, particularly the determinant factors of single-male/multi-male group dichotomy, in light of hypotheses derived from studies of primate societies. Socioecological data from 26 groups comprising 208 feral horses on Serra D’Arga, northern Portugal suggest that these primate-based hypotheses cannot adequately explain the social system of horses. In view of the sympatric existence of multi- and single-male groups, and the frequent intergroup transfers and promiscuous mating of females with males of different groups, male–female relationships of horses appear to differ from those of polygynous primates.     

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’.     

Longevity factor in hominoid social organization

In most primate groups emigration of the maturing young of one or the other sex tends to serve as an incest avoidance mechanism. Among most primate species it is the males who change groups. This supports the theory that, in terms of reproductive success, males should compete for mates and females should compete for resources. In hominoids the combination of increased longevity and greater female discrimination in mate selection seems responsible for female emigration. This may relate to the high frequency of patrilocality and male control of resources among human groups.     

Dynamics of male residence and female oestrus during a breeding season of blue monkeys in the Kakamega Forest, Kenya

Blue monkeys (Cercopithecus mitis stuhlmanni) are seasonal breeders with a dynamic mating system in which typical one‐male social units are regularly disrupted and replaced by multi‐male ones. The number of males in the group is correlated with the number of oestrous females. We used observations of male presence and female oestrus on individual days during a 6‐month period to assess whether the presence of multiple males in a group stimulates female oestrus or whether oestrous females attract multiple males to the group. We confirmed prior observations with our finding that the number of males in a group was significantly correlated (r_s = 0.435, P < 0.0001) with the number of oestrous females across 126 observation days. A transition matrix did not show an obvious relationship between day‐to‐day changes in the numbers of oestrous females and males. However, cross‐correlation analysis provided stronger support for the idea that the number of oestrous females attracts males to a group than for the idea that the influx of strange males stimulates oestrus in female blue monkeys. Autocorrelation analysis showed that while female oestrus appeared to show a high degree of synchrony, as expected in a seasonal breeder, there was no evidence that the number of males accompanying a group of females influenced the likelihood of other males joining or leaving the group. Overall, our results confirm that female oestrous behaviour stimulates changes in male residence patterns. However, other observations suggest that changes in male residence may also stimulate female oestrus in some circumstances.     

Grooming relationships between breeding females and adult group members in cooperatively breeding moustached tamarins (Saguinus mystax)

Grooming is the most common form of affiliative behavior in primates that apart from hygienic and hedonistic benefits offers important social benefits for the performing individuals. This study examined grooming behavior in a cooperatively breeding primate species, characterized by single female breeding per group, polyandrous matings, dizygotic twinning, delayed offspring dispersal, and intensive helping behavior. In this system, breeding females profit from the presence of helpers but also helpers profit from staying in a group and assisting in infant care due to the accumulation of direct and indirect fitness benefits. We examined grooming relationships of breeding females with three classes of partners (breeding males, potentially breeding males, (sub)adult non-breeding offspring) during three reproductive phases (post-partum ovarian inactivity, ovarian activity, pregnancy) in two groups of wild moustached tamarins (Saguinus mystax). We investigated whether grooming can be used to regulate group size by either "pay-for-help" or "pay-to-stay" mechanisms. Grooming of breeding females with breeding males and non-breeding offspring was more intense and more balanced than with potentially breeding males, and most grooming occurred during the breeding females' pregnancies. Grooming was skewed toward more investment by the breeding females with breeding males during the phases of ovarian activity, and with potentially breeding males during pregnancies. Our results suggest that grooming might be a mechanism used by female moustached tamarins to induce mate association with the breeding male, and to induce certain individuals to stay in the group and help with infant care.