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'.

Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees.

Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

Recognition of visual kinship signals in chimpanzees (Pan troglodytes) by humans (Homo sapiens).

Associating with kin provides individual benefits but requires that these relationships be detectable. In humans, facial phenotype matching might help assess paternity; however, evidence for it is mixed. In chimpanzees, concealing visual cues of paternity may be beneficial due to their promiscuous mating system and the considerable risk of infanticide by males. On the other hand, detecting kin can also aid chimpanzees in avoiding inbreeding and in forming alliances that improve kin-mediated fitness. Although previous studies assessing relatedness based on facial resemblance in chimpanzees exist, they used images of captive populations in whom selection pressures and reproductive opportunities are controlled and only assessed maternity or paternity of adult offspring. In natural populations, the chances of infanticide are highest during early infancy, suggesting that young infants would benefit most from paternity concealment, whereas adults and subadults would benefit from the detection of all types of kin, including half-siblings. In our experiment, we conducted an online study with human participants, in which they had to assess the relatedness of chimpanzees based on facial similarity. To address previous methodological constraints, we used chimpanzee images across all ages, as well as maternal and paternal half-siblings. We found that kin status was detected above chance across all relatedness categories, with easier kin detection of father-offspring pairs, females, and older chimpanzees. Together, these findings support the existence of paternity confusion in infant chimpanzees and provide a possible mechanism for incest avoidance and kin-based social alliances in older individuals. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Patterns and consequences of age-linked change in local relatedness in animal societies.

The ultimate payoff of behaviours depends not only on their direct impact on an individual, but also on the impact on their relatives. Local relatedness-the average relatedness of an individual to their social environment-therefore has profound effects on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual's lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their effects on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly affect lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together, this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.

Mountain gorillas maintain strong affiliative biases for maternal siblings despite high male reproductive skew and extensive exposure to paternal kin.

Evolutionary theories predict that sibling relationships will reflect a complex balance of cooperative and competitive dynamics. In most mammals, dispersal and death patterns mean that sibling relationships occur in a relatively narrow window during development and/or only with same-sex individuals. Besides humans, one notable exception is mountain gorillas, in which non-sex-biased dispersal, relatively stable group composition, and the long reproductive tenures of alpha males mean that animals routinely reside with both maternally and paternally related siblings, of the same and opposite sex, throughout their lives. Using nearly 40,000 hr of behavioral data collected over 14 years on 699 sibling and 1235 non-sibling pairs of wild mountain gorillas, we demonstrate that individuals have strong affiliative preferences for full and maternal siblings over paternal siblings or unrelated animals, consistent with an inability to discriminate paternal kin. Intriguingly, however, aggression data imply the opposite. Aggression rates were statistically indistinguishable among all types of dyads except one: in mixed-sex dyads, non-siblings engaged in substantially more aggression than siblings of any type. This pattern suggests mountain gorillas may be capable of distinguishing paternal kin but nonetheless choose not to affiliate with them over non-kin. We observe a preference for maternal kin in a species with a high reproductive skew (i.e. high relatedness certainty), even though low reproductive skew (i.e. low relatedness certainty) is believed to underlie such biases in other non-human primates. Our results call into question reasons for strong maternal kin biases when paternal kin are identifiable, familiar, and similarly likely to be long-term groupmates, and they may also suggest behavioral mismatches at play during a transitional period in mountain gorilla society.

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.

Quantitative estimates of glacial refugia for chimpanzees (Pan troglodytes) since the Last Interglacial (120,000 BP).

Paleoclimate reconstructions have enhanced our understanding of how past climates have shaped present-day biodiversity. We hypothesize that the geographic extent of Pleistocene forest refugia and suitable habitat fluctuated significantly in time during the late Quaternary for chimpanzees (Pan troglodytes). Using bioclimatic variables representing monthly temperature and precipitation estimates, past human population density data, and an extensive database of georeferenced presence points, we built a model of changing habitat suitability for chimpanzees at fine spatio-temporal scales dating back to the Last Interglacial (120,000 BP). Our models cover a spatial resolution of 0.0467° (approximately 5.19 km2 grid cells) and a temporal resolution of between 1000 and 4000 years. Using our model, we mapped habitat stability over time using three approaches, comparing our modeled stability estimates to existing knowledge of Afrotropical refugia, as well as contemporary patterns of major keystone tropical food resources used by chimpanzees, figs (Moraceae), and palms (Arecacae). Results show habitat stability congruent with known glacial refugia across Africa, suggesting their extents may have been underestimated for chimpanzees, with potentially up to approximately 60,000 km2 of previously unrecognized glacial refugia. The refugia we highlight coincide with higher species richness for figs and palms. Our results provide spatio-temporally explicit insights into the role of refugia across the chimpanzee range, forming the empirical foundation for developing and testing hypotheses about behavioral, ecological, and genetic diversity with additional data. This methodology can be applied to other species and geographic areas when sufficient data are available.

Recent genetic connectivity and clinal variation in chimpanzees.

Much like humans, chimpanzees occupy diverse habitats and exhibit extensive behavioural variability. However, chimpanzees are recognized as a discontinuous species, with four subspecies separated by historical geographic barriers. Nevertheless, their range-wide degree of genetic connectivity remains poorly resolved, mainly due to sampling limitations. By analyzing a geographically comprehensive sample set amplified at microsatellite markers that inform recent population history, we found that isolation by distance explains most of the range-wide genetic structure of chimpanzees. Furthermore, we did not identify spatial discontinuities corresponding with the recognized subspecies, suggesting that some of the subspecies-delineating geographic barriers were recently permeable to gene flow. Substantial range-wide genetic connectivity is consistent with the hypothesis that behavioural flexibility is a salient driver of chimpanzee responses to changing environmental conditions. Finally, our observation of strong local differentiation associated with recent anthropogenic pressures portends future loss of critical genetic diversity if habitat fragmentation and population isolation continue unabated.

The development of affiliative and coercive reproductive tactics in male chimpanzees.

Like many animals, adult male chimpanzees often compete for a limited number of mates. They fight other males as they strive for status that confers reproductive benefits and use aggression to coerce females to mate with them. Nevertheless, small-bodied, socially immature adolescent male chimpanzees, who cannot compete with older males for status nor intimidate females, father offspring. We investigated how they do so through a study of adolescent and young adult males at Ngogo in Kibale National Park, Uganda. Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males. Two other factors, affiliation and aggression, also influenced mating success. Specifically, the strength of affiliative bonds that males formed with females and the amount of aggression males directed toward females predicted male mating success. The effect of male aggression toward females on mating success increased as males aged, especially when they directed it toward females with whom they shared affiliative bonds. These results mirror sexual coercion in humans, which occurs most often between males and females involved in close, affiliative relationships.

Postweaning maternal care increases male chimpanzee reproductive success.

Humans are unusual among animals for continuing to provision and care for their offspring until adulthood. This "prolonged dependency" is considered key for the evolution of other notable human traits, such as large brains, complex societies, and extended postreproductive lifespans. Prolonged dependency must therefore have evolved under conditions in which reproductive success is gained with parental investment and diminished with early parental loss. We tested this idea using data from wild chimpanzees, which have similarly extended immature years as humans and prolonged mother-offspring associations. Males who lost their mothers after weaning but before maturity began reproducing later and had lower average reproductive success. Thus, persistent mother-immature son associations seem vital for enhancing male reproductive success, although mothers barely provision sons after weaning. We posit that these associations lead to social gains, crucial for successful reproduction in complex social societies, and offer insights into the evolution of prolonged dependency.

Atypically High Reproductive Skew in a Small Wild Chimpanzee Community in a Human-Dominated Landscape.

Social rank is positively correlated with reproductive success in numerous species, albeit demographic factors often influence those patterns. In multimale primate species, reproductive skew tends to decrease with increasing numbers of males and sexually receptive females. Alpha male chimpanzees (Pan troglodytes) often sire a disproportionate, though somewhat variable, percentage of offspring compared to other males. In a small community of eastern chimpanzees inhabiting a human-dominated landscape in Bulindi, Uganda, we found extraordinarily high levels of alpha male reproductive success over a 5-year period (7/8 offspring = 88%), despite the presence of multiple subordinate males. The skew exceeds that reported in other studies of chimpanzees as well as closely related bonobos (Pan paniscus). Our findings underscore the role of demographic and social factors in male reproductive success and also suggest that conclusions about species differences may be premature. The interaction of small community size, dispersal limitations, and male reproductive strategies like those found here may decrease genetic diversity and increase the risk of concomitant inbreeding in chimpanzee communities under strong anthropogenic pressure.

Sexual dimorphism in chimpanzee (Pan troglodytes schweinfurthii) and human age-specific fertility.

Across vertebrates, species with intense male mating competition and high levels of sexual dimorphism in body size generally exhibit dimorphism in age-specific fertility. Compared with females, males show later ages at first reproduction and earlier reproductive senescence because they take longer to attain adult body size and musculature, and maintain peak condition for a limited time. This normally yields a shorter male duration of effective breeding, but this reduction might be attenuated in species that frequently use coalitionary aggression. Here, we present comparative genetic and demographic data on chimpanzees from three long-term study communities (Kanyawara: Kibale National Park, Uganda; Mitumba and Kasekela: Gombe National Park, Tanzania), comprising 581 male risk years and 112 infants, to characterize male age-specific fertility. For comparison, we update estimates from female chimpanzees in the same sites and append a sample of human foragers (the Tanzanian Hadza). Consistent with the idea that aggressive mating competition favors youth, chimpanzee males attained a higher maximum fertility than females, followed by a steeper decline with age. Males did not show a delay in reproduction compared with females, however, as adolescents in both sites successfully reproduced by targeting young, subfecund females, who were less attractive to adults. Gombe males showed earlier reproductive senescence and a shorter duration of effective breeding than Gombe females. By contrast, older males in Kanyawara generally continued to reproduce, apparently by forming coalitions with the alpha. Hadza foragers showed a distinct pattern of sexual dimorphism in age-specific fertility as, compared with women, men gained conceptions later but continued reproducing longer. In sum, both humans and chimpanzees showed sexual dimorphism in age-specific fertility that deviated from predictions drawn from primates with more extreme body size dimorphism, suggesting altered dynamics of male-male competition in the two lineages. In both species, coalitions appear important for extending male reproductive careers.

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].

Nomenclature report 2019: major histocompatibility complex genes and alleles of Great and Small Ape and Old and New World monkey species.

The major histocompatibility complex (MHC) is central to the innate and adaptive immune responses of jawed vertebrates. Characteristic of the MHC are high gene density, gene copy number variation, and allelic polymorphism. Because apes and monkeys are the closest living relatives of humans, the MHCs of these non-human primates (NHP) are studied in depth in the context of evolution, biomedicine, and conservation biology. The Immuno Polymorphism Database (IPD)-MHC NHP Database (IPD-MHC NHP), which curates MHC data of great and small apes, as well as Old and New World monkeys, has been upgraded. The curators of the database are responsible for providing official designations for newly discovered alleles. This nomenclature report updates the 2012 report, and summarizes important nomenclature issues and relevant novel features of the IPD-MHC NHP Database.

Correction to: Nomenclature report 2019: major histocompatibility complex genes and alleles of great and small ape and old and new world monkey species.

The original version of this article contained a spelling error in the Acknowledgments regarding the name of the funding organisation supporting GM and JAH. UKRI-BBSCR should have been UKRI-BBSRC, as is now indicated correctly below.

Differences in MHC-B diversity and KIR epitopes in two populations of wild chimpanzees.

The major histocompatibility complex (MHC) class I genes play a critical role within the immune system, both by the presentation of antigens from intracellular pathogens to immunocompetent cells and by the interaction with killer cell immunoglobulin-like receptors (KIR) on natural killer cells (NK cells). Genes of the MHC are highly diverse, and MHC variation can have effects on the immune functionality of individuals; hence, comparisons of MHC diversity among closely related phylogenetic taxa may give insight into the factors responsible for the shaping of its diversity. The four geographically separated chimpanzee subspecies differ in their overall genetic diversity, have different population histories, and are confronted with different pathogens in their natural habitat, all of which may affect MHC class I DNA sequence diversity. Here, we compare the MHC-B exon two DNA sequence diversity from 24 wild western and 46 wild eastern chimpanzees using necropsy and noninvasively collected fecal samples, respectively. We found a higher MHC-B exon two nucleotide diversity, in our western than eastern chimpanzees. The inclusion of previously published MHC-B exon two data from other western and eastern chimpanzees supported this finding. In addition, our results confirm and extend the finding of a very low C1 epitope frequency at eastern chimpanzee MHC-B molecules, which likely affects the ability of these molecules to interact with NK cells. While the understanding of the differing pathogen environments encountered by disparate populations of a species is a challenging endeavor, these findings highlight the potential for these pathogens to selectively shape immune system variation.

Males with a mother living in their group have higher paternity success in bonobos but not chimpanzees.

In many group-living mammals, mothers may increase the reproductive success of their daughters even after they are nutritionally independent and fully grown [1]. However, whether such maternal effects exist for adult sons is largely unknown. Here we show that males have higher paternity success when their mother is living in the group at the time of the offspring's conception in bonobos (N = 39 paternities from 4 groups) but not in chimpanzees (N = 263 paternities from 7 groups). These results are consistent with previous research showing a stronger role of mothers (and females more generally) in bonobo than chimpanzee societies.

Infant carrying by a wild chimpanzee father at Bulindi, Uganda.

Although infanticide by wild adult male chimpanzees has been reported from multiple sites, affiliative infant carrying by males is rare. We observed infant carrying by an alpha male chimpanzee at Bulindi (Uganda) on two consecutive mornings and collected faecal samples from the newborn infant female, her mother and all candidate fathers to determine whether the alpha male was the infant's father using a likelihood-based method of paternity assignment. In contrast to previous observations of male care of orphans, in this case the mother was present during observations. Further, unlike reports of male aggression towards infants, the infant was reunited with her mother on the third morning, and survived. Neither mother nor infant presented visible injuries. The alpha male never directed aggression towards the infant. Rather, he displayed attentive behaviours, for example by holding the infant to his chest, supporting her while moving, grooming her, and 'cuddling' and 'rocking' her. Paternity results revealed with a high degree of certainty that the alpha male was the infant's father. There are several alternative explanations for the male's behaviour, but this unusual case also highlights the need for further studies to determine under what circumstances adult male chimpanzees can recognise their own offspring.