Non-Reproductive Sexual Behavior in Wild White-Thighed Colobus Monkeys (Colobus vellerosus).

Rare behaviors are often missing from published papers, hampering phylogenetic analyses. Here, we report, for the first time, masturbation and same-sex sexual behavior (SSB) in both male and female black-and-white colobus monkeys. We recorded these behaviors during 32 months of observation (1573 h of focal animal sampling) on Colobus vellerosus collected at the Boabeng-Fiema Monkey Sanctuary in Ghana. Males were observed masturbating and involved in SSB more than females. Subadult males were the age-sex class that engaged in both of these behaviors most often and a third of all SSB observed in young males occurred when they were forming an all-male band (AMB), which are temporally transient social groups in this species. Our data support that masturbation in males may be a sexual outlet for individuals that do not have a current sexual partner, while in females it may function in mate attraction by advertising receptivity. SSB may occur as an evolutionary byproduct but given the temporal clustering of observed events in males prior to AMB formation, our data best support the hypothesis that these behaviors facilitate male-male bonding (i.e., act as social glue). Within AMB's, males engage in coalitionary behavior to take over social groups containing females and strong bonds are important for success and later access to females, which could have selected for SSB in C. vellerosus.

Joint intergroup aggression in female colobus monkeys (Colobus vellerosus) is associated with grooming bonds, male participation, and group size.

Cooperative home range defense is common in primates, despite a collective action problem that arises when group members benefit from winning the intergroup encounter regardless of whether they participate. The costs associated with this collective action problem may be mitigated by residing in small groups, residing with kin, or by forming strong bonds with group members. The potential to decouple the effects of these variables provided an opportunity to investigate which of these three variables best explains coparticipation in intergroup encounters among adult and subadult female colobus at Boabeng-Fiema, Ghana. Because males are often the main participants, we also investigated the relationship between female-female coparticipation and adult and subadult male participation. We collected intergroup behaviors from 94 adult and subadult individuals in eight groups during 1 year. We quantified female grooming bond strength and approach rates using focal samples. We classified female dyads as close kin (i.e., halfsiblings or more closely related) or nonkin based on partial pedigrees and genotypes generated from 17 STR loci. Female-female coparticipation was higher in dyads with stronger grooming bonds but was not associated with dyadic kinship, approach rate, or age class. Female coparticipation decreased with increasing female group size as expected if there is a collective action problem. Females coparticipated less in groups with more males and male intergroup aggression, possibly because there is less need for female-female cooperation if males are participating in the intergroup encounter. Females in smaller groups may not only benefit from increased female-female cooperation during intergroup encounters, they are also likely to reside with a higher-quality alpha male, both of which may increase the likelihood of winning intergroup encounters. There may be strong selection for facultative female dispersal in populations like the Boabeng-Fiema colobus in which small groups are associated with multiple benefits and cooperation is not affected by kinship.

Divergence in gut microbial communities mirrors a social group fission event in a black-and-white colobus monkey (Colobus vellerosus).

Host behavior and social factors have increasingly been implicated in structuring the composition of gut microbial communities. In social animals, distinct microbial communities characterize different social groups across a variety of taxa, although little longitudinal research has been conducted that demonstrates how this divergence occurs. Our study addresses this question by characterizing the gut microbial composition of an African Old World monkey, the black-and-white colobus (Colobus vellerosus), before and after a social group fission event. Gut microbial taxonomic composition of these monkeys was profiled using the V-4 hypervariable region of the bacterial 16S ribosomal RNA gene, and pairwise-relatedness values were calculated for all individuals using 17 short tandem repeat loci and partial pedigree information. The two social groups in this study were found to harbor distinct microbial signatures after the fission event from which they emerged, while these communities were not divergent in the same individuals before this event. Three genera were found to differ in abundance between the two new social groups: Parabacteroides, Coprococcus, and Porphyromonadaceae. Additionally, although this fission happened partially along lines of relatedness, relatedness did not structure the differences that we found. Taken together, this study suggests that distinct gut microbial profiles can emerge in social groups in <1 year and recommends further work into more finely mapping the timescales, causes, and potentially adaptive effects of this recurring trend toward distinct group microbial signatures.

Infant mortality in white-faced capuchins: The impact of alpha male replacements.

Infanticide is common in the context of alpha male replacements (AMR), particularly in groups where alpha males experience high reproductive skew and the infants are unlikely to be related to a new alpha male. We examined the relationship between the rate of infant mortality, infant age, and the occurrence and type of AMR in white-faced capuchin monkeys (Cebus capucinus imitator) of the Santa Rosa population in Sector Santa Rosa, Área de Conservación Guanacaste. Specifically, we investigated how the source of the new alpha male (coresident or extragroup) and relative aggression level during AMRs influenced infant mortality in this species. Between 1986 and 2015, we recorded 221 births in five study groups. Infants present at the time of an AMR, or born within 5.5 months following an AMR (i.e., conceived prior to AMR), experienced significantly higher mortality than those born during periods of group stability. Infant age was a significant predictor of infant survival, with the probability of surviving increasing by 0.4% for each additional day older an infant was at the time of the AMR. Infant mortality rates did not differ between AMRs by coresident males and extragroup males, possibly because the degree of relatedness between infants and new alphas did not significantly differ between coresident and extragroup AMRs. Infant mortality rates did not differ significantly between aggressive AMRs and more peaceful AMRs. Our results are consistent with predictions derived from the sexual selection hypothesis (SSH) of infanticide and suggest that future studies examine the role of testosterone as an underlying proximate mechanism for the aggression leading to this behavior. We argue that the sexual selection and generalized aggression hypotheses (GAH) of infanticide are best considered as different levels of analysis rather than competing hypotheses.

Female sociality and sexual conflict shape offspring survival in a Neotropical primate.

Most mammals live in social groups in which members form differentiated social relationships. Individuals may vary in their degree of sociality, and this variation can be associated with differential fitness. In some species, for example, female sociality has a positive effect on infant survival. However, investigations of such cases are still rare, and no previous study has considered how male infanticide might constrain effects of female sociality on infant survival. Infanticide is part of the male reproductive strategy in many mammals, and it has the potential to override, or even reverse, effects of female reproductive strategies, including sociality. Therefore, we investigated the relationships between female sociality, offspring survival, and infanticide risk in wild white-faced capuchin monkeys using long-term data from Santa Rosa, Costa Rica. Female capuchins formed differentiated bonds, and bond strength was predicted by kin relationship, rank difference, and the presence of female infants. Most females formed stable bonds with their top social partners, although bond stability varied considerably. Offspring of highly social females, who were often high-ranking females, exhibited higher survivorship during stable periods compared with offspring of less social females. However, offspring of highly social females were more likely to die or disappear during periods of alpha male replacements, probably because new alpha males are central to the group, and therefore more likely to target the infants of highly social, central females. This study shows that female sociality in mammals can have negative fitness consequences that are imposed by male behavior.

The influence of male takeovers on female dispersal in Colobus vellerosus.

Male takeovers affect male tenure, female mate choice and ultimately, individual reproductive success in group-living primates. In social systems with female philopatry and high male reproductive skew, male takeovers largely determine female mate choice, whereas in species with female dispersal, females have the option of deserting a new male. We focused on a species with facultative female dispersal to investigate which factors promote female desertion of males after takeover, using 15 cases (12 for which we have complete data on the takeover process and the female dispersal outcome). These cases took place in nine groups of Colobus vellerosus between 2001 and 2013 at the Boabeng-Fiema Monkey Sanctuary, Ghana. Quick takeovers were usually achieved by single adult males and were never followed by female dispersal. Slow takeovers involved several males, and these takeovers were regularly accompanied by female emigration. Infant attacks and infanticide by males occurred during both kinds of takeovers, but females with dependent offspring never dispersed, regardless of whether their infant was attacked or killed by the new male(s). Subadult females, who were not constrained by the presence of infants, dispersed more often after slow takeovers than after quick takeovers. Whether female dispersal post-takeover is an expression of female mate choice, or occurs to avoid the social upheaval surrounding slow takeovers, remains to be investigated. Am. J. Primatol. 79:e22436, 2017. © 2015 Wiley Periodicals, Inc.

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator).

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug-of-war) or by how easily females can be monopolized (priority-of-access). These models have rarely been investigated in species with exceptionally long male tenures, such as white-faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white-faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession model's assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha male's probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well-established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.

Paternal kin recognition and infant care in white-faced capuchins (Cebus capucinus).

Evidence for paternal kin recognition and paternally biased behaviors is mixed among primates. We investigate whether infant handling behaviors exhibit paternal kin biases in wild white-faced capuchins monkeys (Cebus capucinus) by comparing interactions between infants and genetic sires, potential sires, siblings (full sibling, maternal, and paternal half-siblings) and unrelated handlers. We used a linear mixed model approach to analyze data collected on 21 focal infants from six groups in Sector Santa Rosa, Costa Rica. Our analyses suggest that the best predictor of adult and subadult male interactions with an infant is the male's dominance status, not his paternity status. We found that maternal siblings but not paternal siblings handled infants more than did unrelated individuals. We conclude that maternal but not paternal kinship influence patterns of infant handling in white-faced capuchins, regardless of whether or not they can recognize paternal kin. Am. J. Primatol. 78:659-668, 2016. © 2016 Wiley Periodicals, Inc.

Female parity, maternal kinship, infant age and sex influence natal attraction and infant handling in a wild colobine (Colobus vellerosus).

Primate females often inspect, touch and groom others' infants (natal attraction) and they may hold and carry these infants in a manner resembling maternal care (infant handling). While natal attraction and infant handling occur in most wild colobines, little is known about the factors influencing the expression of these behaviors. We examined the effects of female parity, kinship, and dominance rank, as well as infant age and sex in wild Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, Ghana. We collected data via focal sampling of females in 2008 and 2009 (N = 61) and of infants in 2010 (N = 12). Accounting for the individuals who interacted with our focal subjects, this study includes 74 females and 66 infants in 8 groups. We recorded female agonistic interactions ad libitum to determine dominance ranks. We used partial pedigree information and genotypes at 17 short tandem repeat loci to determine kinship. We knew female parity, infant age and sex from demographic records. Nulliparous females showed more natal attraction and infant handling than parous females, which may suggest that interactions with infants are more adaptive for nulliparous females because they learn mothering skills through these behaviors. Compared to non-kin, maternal kin were more likely to handle infants. Maternal kin may be permitted greater access to infants because mothers are most familiar with them. Handlers may incur inclusive fitness benefits from infant handling. Dominance rank did not affect female interactions with infants. The youngest infants received the most natal attraction and infant handling, and male infants were handled more than female infants. The potential benefits of learning to mother and inclusive fitness, in combination with the relatively low costs of natal attraction and infant handling, may explain the high rates of these behaviors in many colobines.

Familiarity is more important than phenotypic similarity in shaping social relationships in a facultative female dispersed primate, Colobus vellerosus.

Animals often bias affiliative behaviors toward kin, but it is unclear what mechanism most species use to discriminate kin. We investigated if facultative dispersed female primates use phenotype matching and/or familiarity to discriminate female kin. We studied 38 adult female Colobus vellerosus at Boabeng-Fiema, Ghana. We determined dyadic co-residency status and age proximity using long-term demographic data, R-values from 17 short tandem repeat loci, and interaction rates using focal samples collected during one year. Approach rates were not strongly affected by how long females had resided together, which contrasts to the familiarity hypothesis. Females approached and groomed maternal kin more than other females, which supports the mother-mediated familiarity hypothesis. Females did not discriminate paternal half siblings from non-kin, and they did not prefer to interact with females of similar age. Short-term co-resident kin did not bias affiliation toward each other, indicating that female colobus cannot consistently recognize less familiar kin via phenotype matching or that biasing behaviors toward less familiar kin is not beneficial. Despite showing facultative dispersal that may reduce the accuracy of using familiarity as a kin recognition mechanism, female choice of social partners was based on familiarity, which conforms to the pattern observed in many female philopatric primates.

Kinship and similarity in residency status structure female social networks in black-and-white colobus monkeys (Colobus vellerosus).

Kinship shapes female social networks in many primate populations in which females remain in their natal group to breed. In contrast, it is unclear to which extent kinship affects the social networks in populations with female dispersal. Female Colobus vellerosus show routine facultative dispersal (i.e., some females remain philopatric and others disperse). This dispersal pattern allowed us to evaluate if facultative dispersed females form social networks shaped by an attraction to kin, to social partners with a high resource holding potential, or to similar social partners in terms of maturational stage, dominance rank, and residency status. During 2008 and 2009, we collected behavioral data via focal and ad libitum sampling of 61 females residing in eight groups at Boabeng-Fiema, Ghana. We determined kinship based on partial pedigrees and genotypes at 17 short tandem repeat loci. Kinship influenced coalition and affiliation networks in three groups consisting of long-term resident females with access to a relatively high number of female kin. In contrast, similar residency status was more important than kinship in structuring the affiliation network in one of two groups that contained recent female immigrants. In populations with female dispersal, the occurrence of kin structured social networks may not only depend on the kin composition of groups but also on how long the female kin have resided together. We found no consistent support for females biasing affiliation toward partners with high resource holding potential, possibly due to low levels of contest competition and small inter-individual differences in resource holding potential.

Between-group variation in female dispersal, kin composition of groups, and proximity patterns in a black-and-white colobus monkey (Colobus vellerosus).

A growing body of evidence shows within-population variation in natal dispersal, but the effects of such variation on social relationships and the kin composition of groups remain poorly understood. We investigate the link between dispersal, the kin composition of groups, and proximity patterns in a population of black-and-white colobus (Colobus vellerosus) that shows variation in female dispersal. From 2006 to 2011, we collected behavioral data, demographic data, and fecal samples of 77 males and 92 females residing in eight groups at Boabeng-Fiema, Ghana. A combination of demographic data and a genetic network analysis showed that although philopatry was female-biased, only about half of the females resided in their natal groups. Only one group contained female-female dyads with higher average relatedness than randomly drawn animals of both sexes from the same group. Despite between-group variation in female dispersal and kin composition, female-female dyads in most of the study groups had higher proximity scores than randomly drawn dyads from the same group. We conclude that groups fall along a continuum from female dispersed, not kin-based, and not bonded to female philopatric, kin-based, and bonded. We found only partial support for the predicted link between dispersal, kin composition, and social relationships. In contrast to most mammals where the kin composition of groups is a good predictor of the quality of female-female relationships, this study provides further support for the notion that kinship is not necessary for the development and maintenance of social bonds in some gregarious species.