The complex Y-chromosomal history of gorillas.

Studies of the evolutionary relationships among gorilla populations using autosomal and mitochondrial sequences suggest that male-mediated gene flow may have been important in the past, but data on the Y-chromosomal relationships among the gorilla subspecies are limited. Here, we genotyped blood and noninvasively collected fecal samples from 12 captives and 257 wild male gorillas of known origin representing all four subspecies (Gorilla gorilla gorilla, G. g. diehli, G. beringei beringei, and G. b. graueri) at 10 Y-linked microsatellite loci resulting in 102 unique Y-haplotypes for 224 individuals. We found that western lowland gorilla (G. g. gorilla) haplotypes were consistently more diverse than any other subspecies for all measures of diversity and comprised several genetically distinct groups. However, these did not correspond to geographical proximity and some closely related haplotypes were found several hundred kilometers apart. Similarly, our broad sampling of eastern gorillas revealed that mountain (G. b. beringei) and Grauer's (G. b. graueri) gorilla Y-chromosomal haplotypes did not form distinct clusters. These observations suggest structure in the ancestral population with subsequent mixing of differentiated haplotypes by male dispersal for western lowland gorillas, and postisolation migration or incomplete lineage sorting due to short divergence times for eastern gorillas.

Male-female relationships in olive baboons (Papio anubis): Parenting or mating effort?

Long-term male-female bonds and bi-parental investment in offspring are hallmarks of human society. A key question is how these traits evolved from the polygynandrously mating multimale multifemale society that likely characterized the Pan-Homo ancestor. In all three species of savanna baboons, lactating females form strong ties (sometimes called "friendships") with one or more adult males. For yellow baboons (Papio cynocephalus) and chacma baboons (Papio ursinus), several lines of evidence suggest that these relationships are a form of male parenting effort. In olive baboons (Papio anubis), females are thought to preferentially mate with their "friends", and male-female bonds may thus function as a form of mating effort. Here, we draw on behavioral and genetic data to evaluate the factors that shape male-female relationships in a well-studied population of olive baboons. We find support for the parenting effort hypothesis in that sires have stronger bonds with their infants' mothers than do other males. These bonds sometimes persist past weaning age and, in many cases, the sire of the previous infant is still a close partner of the female when she nurses her subsequent offspring. We find that males who have the strongest bonds with females that have resumed cycling, but are not currently sexually receptive, are more likely to sire the female's next offspring but the estimate is associated with large statistical uncertainty. We also find that in over one third of the cases, a female's successive infants were sired by the same male. Thus, in olive baboons, the development of stable breeding bonds and paternal investment seem to be grounded in the formation of close ties between males and anestrous females. However, other factors such as male dominance rank also influence paternity success and may preclude stability of these bonds to the extent found in human societies.

The ties that bind: Maternal kin bias in a multilevel primate society despite natal dispersal by both sexes.

In many social animals, individuals derive fitness benefits from close social bonds, which are often formed among kin of the philopatric sex. Hamadryas baboons, however, exhibit a hierarchical, multilevel social system where both sexes disperse from their natal one-male-unit (OMU). Although this would seem to hinder maintenance of kin ties, both sexes appear largely philopatric at the higher order band and clan levels, possibly allowing for bonds with same sex kin by both males and females. In order to investigate the possibility of kin bonds in hamadryas baboons, we identified kin dyads in a band without known pedigree information using a large panel of genetic markers: 1 Y-linked, 4 X-linked, and 23 autosomal microsatellites and part of the mitochondrial hypervariable region I. With these data, we performed a kinship analysis while accounting for misclassification rates through simulations and determined kinship among two types of dyads: leader and follower males and female dyads within OMUs. Leader and follower males were maternal relatives more often than expected by chance, suggesting that kinship plays a role in the formation of these relationships. Moreover, maternal female relatives were found in the same OMU more often than expected by chance, indicating that females may be motivated to maintain post-dispersal contact with maternal female kin. Our results suggest that hamadryas baboons can recognize maternal kin and that kin selection has contributed to shaping their complex social system. This implies that an ancestral maternal kin bias has been retained in hamadryas society. Am. J. Primatol. 78:731-744, 2016. © 2016 Wiley Periodicals, Inc.

Fine-scale genetic assessment of sex-specific dispersal patterns in a multilevel primate society.

Like humans, hamadryas baboons (Papio hamadryas) are unusual among primates in having a multilevel social system and stable pair bonds, and are thus a useful model for the evolution of human sociality. While the kinship structure and sex-biased dispersal patterns that underlie human social organization have been extensively elucidated, the impact of these factors on the social system of hamadryas baboons is currently unclear. Here we use genetic analysis of individuals to elucidate the patterns of male and female dispersal across multiple levels of society in a wild population of hamadryas baboons. We characterized 244 members of five hamadryas bands at Filoha, Ethiopia by genotyping one Y-linked and 23 autosomal microsatellite loci and sequencing part of the mitochondrial hypervariable control region I. We found both male and female dispersal to be limited at the level of the band, with more movement of females than males among bands. By integrating long-term behavioral data for Band 1, we also found evidence for male and female philopatry at the clan level. We speculate that male philopatry at the clan level and female dispersal across one-male units and clans may enable both kin-based cooperation among males and the maintenance of kin bonds among females after dispersal. This would mean that, as in humans, kin bonds within both sexes are a core feature of the hamadryas social system, thus contributing to our understanding of the evolution of social organization in humans.

Female chimpanzees avoid inbreeding even in the presence of substantial bisexual philopatry.

Inbreeding (reproduction between relatives) often decreases the fitness of offspring and is thus expected to lead to the evolution of inbreeding avoidance strategies. Chimpanzees (Pan troglodytes) are expected to avoid inbreeding as they are long-lived, invest heavily in offspring and may encounter adult, opposite sex kin frequently, especially in populations where both males and females commonly remain in the group in which they were born (bisexual philopatry). However, it is unclear whether substantial bisexual philopatry has been a feature of chimpanzees' evolutionary history or whether it is a result of recent anthropogenic interference, as the only groups for which it has been documented are significantly impacted by human encroachment and experience notable rates of potentially unsustainable inbreeding. Here we use 14 years of observational data and a large genomic dataset of 256 481 loci sequenced from 459 individuals to document dispersal and inbreeding dynamics in an eastern chimpanzee (P. t. schweinfurthii) community with low levels of anthropogenic disturbance. We document the first case of substantial bisexual philopatry in a relatively undisturbed chimpanzee community and show that, despite an increased inbreeding risk incurred by females who do not disperse before reaching reproductive age, natal females were still able to avoid producing inbred offspring.

Reproductive inequality among males in the genus Pan.

Reproductive inequality, or reproductive skew, drives natural selection, but has been difficult to assess, particularly for males in species with promiscuous mating and slow life histories, such as bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Although bonobos are often portrayed as more egalitarian than chimpanzees, genetic studies have found high male reproductive skew in bonobos. Here, we discuss mechanisms likely to affect male reproductive skew in Pan, then re-examine skew patterns using paternity data from published work and new data from the Kokolopori Bonobo Reserve, Democratic Republic of Congo and Gombe National Park, Tanzania. Using the multinomial index (M), we found considerable overlap in skew between the species, but the highest skew occurred among bonobos. Additionally, for two of three bonobo communities, but no chimpanzee communities, the highest ranking male had greater siring success than predicted by priority-of-access. Thus, an expanded dataset covering a broader demographic range confirms that bonobos have high male reproductive skew. Detailed comparison of data from Pan highlights that reproductive skew models should consider male-male dynamics including the effect of between-group competition on incentives for reproductive concessions, but also female grouping patterns and factors related to male-female dynamics including the expression of female choice. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Shifts in Male Reproductive Tactics over the Life Course in a Polygynandrous Mammal.

In polygynous and polygynandrous species, there is often intense male-male competition over access to females, high male reproductive skew, and more male investment in mating effort than parenting effort [1]. However, the benefits derived from mating effort and parenting effort may change over the course of males' lives. In many mammalian species, there is a ∩-shaped relationship between age, condition, and resource holding power as middle-aged males that are in prime physical condition outcompete older males [2-8] and sire more infants [9-12]. Thus, males might derive more benefits from parenting effort than mating effort as they age and their competitive abilities decline [13]. Alternatively, older males may invest more effort in making themselves attractive to females as mates [14]. One way that older males might do so is by developing relationships with females and providing care for their offspring [14, 15]. Savannah baboons provide an excellent opportunity to test these hypotheses. They form stable multi-male, multi-female groups, and males compete for high ranking positions. In yellow and chacma baboons (Papio cynocephalus and P. ursinus), there is a ∩-shaped relationship between male age and dominance rank [12], and high rank enhances paternity success [12, 16]. Lactating female baboons form close ties ("primary associations" hereafter) with particular males [15-20], who support them and their infants in conflicts [15, 19] and buffer their infants from rough handling [20]. Females' primary associates are often, but not always, the sires of their current infants [16, 20-22].

A roadmap for high-throughput sequencing studies of wild animal populations using noninvasive samples and hybridization capture.

Large-scale genomic studies of wild animal populations are often limited by access to high-quality DNA. Although noninvasive samples, such as faeces, can be readily collected, DNA from the sample producers is usually present in low quantities, fragmented, and contaminated by microorganism and dietary DNAs. Hybridization capture can help to overcome these impediments by increasing the proportion of subject DNA prior to high-throughput sequencing. Here we evaluate a key design variable for hybridization capture, the number of rounds of capture, by testing whether one or two rounds are most appropriate, given varying sample quality (as measured by the ratios of subject to total DNA). We used a set of 1,780 quality-assessed wild chimpanzee (Pan troglodytes schweinfurthii) faecal samples and chose 110 samples of varying quality for exome capture and sequencing. We used multiple regression to assess the effects of the ratio of subject to total DNA (sample quality), rounds of capture and sequencing effort on the number of unique exome reads sequenced. We not only show that one round of capture is preferable when the proportion of subject DNA in a sample is above ~2%-3%, but also explore various types of bias introduced by capture, and develop a model that predicts the sequencing effort necessary for a desired data yield from samples of a given quality. Thus, our results provide a useful guide and pave a methodological way forward for researchers wishing to plan similar hybridization capture studies.

To grunt or not to grunt: Factors governing call production in female olive baboons, Papio anubis.

Vocal signals often play an important role in synchronizing the activities of group members, coordinating decisions about when and where to travel, and facilitating social interactions in which there are potential conflicts of interest. Here, we show that when female olive baboons (Papio anubis) give low amplitude grunts after approaching other females, they are less likely to behave aggressively toward their partners and more likely to handle their partners' infants and interact affiliatively with them. In addition, females are more likely to grunt after they approach lower ranking females than after they approach higher ranking females and are less likely to grunt after they approach their own mothers and daughters than after they approach other females. These patterns, which are strikingly similar to patterns previously reported in chacma baboons (Papio ursinus) support the hypothesis that grunts function as signals of benign intent. Moreover, they suggest that actors' decisions about whether to grunt or remain silent are influenced by the social context, particularly their partners' likely response to their approach. Taken together, the patterning of grunts in olive and chacma baboon suggests that these vocalizations play an important in reducing uncertainty about actors' intentions and facilitate nonaggressive social interactions.

Strategies for determining kinship in wild populations using genetic data.

Knowledge of kin relationships between members of wild animal populations has broad application in ecology and evolution research by allowing the investigation of dispersal dynamics, mating systems, inbreeding avoidance, kin recognition, and kin selection as well as aiding the management of endangered populations. However, the assessment of kinship among members of wild animal populations is difficult in the absence of detailed multigenerational pedigrees. Here, we first review the distinction between genetic relatedness and kinship derived from pedigrees and how this makes the identification of kin using genetic data inherently challenging. We then describe useful approaches to kinship classification, such as parentage analysis and sibship reconstruction, and explain how the combined use of marker systems with biparental and uniparental inheritance, demographic information, likelihood analyses, relatedness coefficients, and estimation of misclassification rates can yield reliable classifications of kinship in groups with complex kin structures. We outline alternative approaches for cases in which explicit knowledge of dyadic kinship is not necessary, but indirect inferences about kinship on a group- or population-wide scale suffice, such as whether more highly related dyads are in closer spatial proximity. Although analysis of highly variable microsatellite loci is still the dominant approach for studies on wild populations, we describe how the long-awaited use of large-scale single-nucleotide polymorphism and sequencing data derived from noninvasive low-quality samples may eventually lead to highly accurate assessments of varying degrees of kinship in wild populations.