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.

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.

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.

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.

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.

Group augmentation, collective action, and territorial boundary patrols by male chimpanzees.

How can collective action evolve when individuals benefit from cooperation regardless of whether they pay its participation costs? According to one influential perspective, collective action problems are common, especially when groups are large, but may be solved when individuals who have more to gain from the collective good or can produce it at low costs provide it to others as a byproduct. Several results from a 20-y study of one of the most striking examples of collective action in nonhuman animals, territorial boundary patrolling by male chimpanzees, are consistent with these ideas. Individuals were more likely to patrol when (i) they had more to gain because they had many offspring in the group; (ii) they incurred relatively low costs because of their high dominance rank and superior physical condition; and (iii) the group size was relatively small. However, several other findings were better explained by group augmentation theory, which proposes that individuals should bear the short-term costs of collective action even when they have little to gain immediately if such action leads to increases in group size and long-term increases in reproductive success. In support of this theory, (i) individual patrolling effort was higher and less variable than participation in intergroup aggression in other primate species; (ii) males often patrolled when they had no offspring or maternal relatives in the group; and (iii) the aggregate patrolling effort of the group did not decrease with group size. We propose that group augmentation theory deserves more consideration in research on collective action.

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.

Reduced bonobo MHC class I diversity predicts a reduced viral peptide binding ability compared to chimpanzees.

BACKGROUND: The highly polymorphic genes of the major histocompatibility complex (MHC) class I are involved in defense against viruses and other intracellular pathogens. Although several studies found reduced MHC class I diversity in bonobos in comparison to the closely related chimpanzee, it is unclear if this lower diversity also influences the functional ability of MHC class I molecules in bonobos. Here, we use a bioinformatic approach to analyze the viral peptide binding ability of all published bonobo MHC class I molecules (n = 58) in comparison to all published chimpanzee MHC class I molecules (n = 161) for the class I loci A, B, C and A-like. RESULTS: We examined the peptide binding ability of all 219 different MHC class I molecules to 5,788,712 peptides derived from 1432 different primate viruses and analyzed the percentage of bound peptides and the overlap of the peptide binding repertoires of the two species. We conducted multiple levels of analysis on the "species"-, "population"- and "individual"-level to account for the characterization of MHC variation in a larger number of chimpanzees and their broader geographic distribution. We found a lower percentage of bound peptides in bonobos at the B locus in the "population"-level comparison and at the B and C loci in the "individual"-level comparison. Furthermore, we found evidence of a limited peptide binding repertoire in bonobos by tree-based visualization of functional clustering of MHC molecules, as well as an analysis of peptides bound by both species. CONCLUSION: Our results suggest a reduced MHC class I viral peptide binding ability at the B and C loci in bonobos compared to chimpanzees. The effects of this finding on the immune defense against viruses in wild living bonobos are unclear. However, special caution is needed to prevent introduction and spread of new viruses to bonobos, as their defensive ability to cope with new viruses could be limited compared to chimpanzees.

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.

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.

Aggression by male bonobos against immature individuals does not fit with predictions of infanticide.

The selective advantage of male infanticide is enhancement of reproductive success of the aggressor. This implies that aggression is directed at individuals sired by others, infant loss shortens the mother's inter-birth interval, and the aggressor has a greater likelihood of siring the next offspring of the victims' mother. As these conditions are not always met, the occurrence of male infanticide is expected to vary, and hominoid primates offer an interesting example of variation in male infanticide. Infanticide has been reported in gorillas and chimpanzees but appears to be absent in orangutans and bonobos. One argument for the absence of infanticide in bonobos is reduction of male aggression. However, given that male aggression against immature individuals occurs and that females engage in behavior that is considered to be counterstrategy against male infanticide, the risk of male infanticide may pose a potential threat. Here, we explored whether aggression by male bonobos fits predictions of male infanticide. Male aggression toward immature individuals was rare and did not have lethal consequences, but the majority of observed cases exposed targets to risks of injury. Males did not target their own offspring less frequently than unrelated immatures, and the risk of being the target of male aggression increased with the targets' age. Overall, these results do not match the predictions of the adaptive male infanticide hypothesis. Instead, aggression by males may promote the emigration of the targets and older males may reinforce their superior status toward individuals that will soon compete for the same resources.

Discovery of gorilla MHC-C expressing C1 ligand for KIR.

In comparison to humans and chimpanzees, gorillas show low diversity at MHC class I genes (Gogo), as reflected by an overall reduced level of allelic variation as well as the absence of a functionally important sequence motif that interacts with killer cell immunoglobulin-like receptors (KIR). Here, we use recently generated large-scale genomic sequence data for a reassessment of allelic diversity at Gogo-C, the gorilla orthologue of HLA-C. Through the combination of long-range amplifications and long-read sequencing technology, we obtained, among the 35 gorillas reanalyzed, three novel full-length genomic sequences including a coding region sequence that has not been previously described. The newly identified Gogo-C*03:01 allele has a divergent recombinant structure that sets it apart from other Gogo-C alleles. Domain-by-domain phylogenetic analysis shows that Gogo-C*03:01 has segments in common with Gogo-B*07, the additional B-like gene that is present on some gorilla MHC haplotypes. Identified in ~ 50% of the gorillas analyzed, the Gogo-C*03:01 allele exclusively encodes the C1 epitope among Gogo-C allotypes, indicating its important function in controlling natural killer cell (NK cell) responses via KIR. We further explored the hypothesis whether gorillas experienced a selective sweep which may have resulted in a general reduction of the gorilla MHC class I repertoire. Our results provide little support for a selective sweep but rather suggest that the overall low Gogo class I diversity can be best explained by drastic demographic changes gorillas experienced in the ancient and recent past.

Insights into hominid evolution from the gorilla genome sequence.

Gorillas are humans' closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human-chimpanzee and human-chimpanzee-gorilla speciation events at approximately 6 and 10 million years ago. In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.

Population-level assessment of genetic diversity and habitat fragmentation in critically endangered Grauer's gorillas.

OBJECTIVES: The critically endangered Grauer's gorilla (Gorilla beringei graueri) has experienced an estimated 77% population decline within a single generation. Although crucial for informed conservation decisions, there is no clear understanding about population structure and distribution of genetic diversity across the species' highly fragmented range. We fill this gap by studying several core and peripheral Grauer's gorilla populations throughout their distribution range. MATERIALS AND METHODS: We generated genetic profiles for a sampling of an unstudied population of Grauer's gorillas from within the species' core range at 13 autosomal microsatellite loci and combined them with previously published and newly generated data from four other Grauer's gorilla populations, two mountain gorilla populations, and one western lowland gorilla population. RESULTS: In agreement with previous studies, the genetic diversity of Grauer's gorillas is intermediate, falling between western lowland and mountain gorillas. Among Grauer's gorilla populations, we observe lower genetic diversity and high differentiation in peripheral compared with central populations, indicating a strong effect of genetic drift and limited gene flow among small, isolated forest fragments. DISCUSSION: Although genetically less diverse, peripheral populations are frequently essential for the long-term persistence of a species and migration between peripheral and core populations may significantly enrich the overall species genetic diversity. Thus, in addition to central Grauer's gorilla populations from the core of the distribution range that clearly deserve conservation attention, we argue that conservation strategies aiming to ensure long-term species viability should include preserving peripheral populations and enhancing habitat connectivity.

Non-invasive genetic censusing and monitoring of primate populations.

Knowing the density or abundance of primate populations is essential for their conservation management and contextualizing socio-demographic and behavioral observations. When direct counts of animals are not possible, genetic analysis of non-invasive samples collected from wildlife populations allows estimates of population size with higher accuracy and precision than is possible using indirect signs. Furthermore, in contrast to traditional indirect survey methods, prolonged or periodic genetic sampling across months or years enables inference of group membership, movement, dynamics, and some kin relationships. Data may also be used to estimate sex ratios, sex differences in dispersal distances, and detect gene flow among locations. Recent advances in capture-recapture models have further improved the precision of population estimates derived from non-invasive samples. Simulations using these methods have shown that the confidence interval of point estimates includes the true population size when assumptions of the models are met, and therefore this range of population size minima and maxima should be emphasized in population monitoring studies. Innovations such as the use of sniffer dogs or anti-poaching patrols for sample collection are important to ensure adequate sampling, and the expected development of efficient and cost-effective genotyping by sequencing methods for DNAs derived from non-invasive samples will automate and speed analyses.

Genetic analysis suggests dispersal among chimpanzees in a fragmented forest landscape in Uganda.

Habitat fragmentation is a leading threat to global biodiversity. Dispersal plays a key role in gene flow and population viability, but the impact of fragmentation on dispersal patterns remains poorly understood. Among chimpanzees, males typically remain in their natal communities while females often disperse. However, habitat loss and fragmentation may cause severe ecological disruptions, potentially resulting in decreased fitness benefits of male philopatry and limited female dispersal ability. To investigate this issue, we genotyped nearly 900 non-invasively collected chimpanzee fecal samples across a fragmented forest habitat that may function as a corridor between two large continuous forests in Uganda, and used the spatial associations among co-sampled genotypes to attribute a total of 229 individuals to 10 distinct communities, including 9 communities in the corridor habitat and 1 in continuous forest. We then used parentage analyses to infer instances of between-community dispersal. Of the 115 parent-offspring dyads detected with confidence, members of 39% (N = 26) of mother-daughter dyads were found in different communities, while members of 10% (N = 5) of father-son dyads were found in different communities. We also found direct evidence for one dispersal event that occurred during the study period, as a female's sample found first in one community was found multiple times in another community 19 months later. These findings suggest that even in fragmented habitats, chimpanzee males remain in their natal communities while females tend to disperse. Corridor enhancement in unprotected forest fragments could help maintain gene flow in chimpanzees and other species amid anthropogenic pressures.

Long-term group membership and dynamics in a wild western lowland gorilla population (Gorilla gorilla gorilla) inferred using non-invasive genetics.

The social organization of a group-living animal is defined by a balance between group dynamic events such as group formation, group dissolution, and dispersal events and group stability in membership and over time. Understanding these processes, which are relevant for questions ranging from disease transmission patterns to the evolution of polygyny, requires long-term monitoring of multiple social units over time. Because all great ape species are long-lived and elusive, the number of studies on these key aspects of social organization are limited, especially for western lowland gorillas (Gorilla gorilla gorilla). In this study, we used non-invasive genetic samples collected within an approximately 100 km2 area of Loango National Park, Gabon to reconstruct group compositions and changes in composition over more than a decade. We identified 98 gorillas and 11 mixed sex groups sampled during 2014-2017. Using published data from 85 individuals and 12 groups surveyed between 2005 and 2009 at the same locality, we tracked groups and individuals back in time. The identification of 11 silverbacks via parentage analyses and the genetic tracking of 39 individuals across studies allowed us to infer six group formations, five group dissolutions, and 40 dispersal events within 12 years. We also observed four groups persisting across the sampling periods with a maximum inferred existence of nearly 17 years and exhibiting variation in membership stability. Our results highlight the variation in composition and stability among groups of western lowland gorillas and illustrate the power of non-invasive genetic sampling for long-term monitoring.

Gorilla MHC class I gene and sequence variation in a comparative context.

Comparisons of MHC gene content and diversity among closely related species can provide insights into the evolutionary mechanisms shaping immune system variation. After chimpanzees and bonobos, gorillas are humans' closest living relatives; but in contrast, relatively little is known about the structure and variation of gorilla MHC class I genes (Gogo). Here, we combined long-range amplifications and long-read sequencing technology to analyze full-length MHC class I genes in 35 gorillas. We obtained 50 full-length genomic sequences corresponding to 15 Gogo-A alleles, 4 Gogo-Oko alleles, 21 Gogo-B alleles, and 10 Gogo-C alleles including 19 novel coding region sequences. We identified two previously undetected MHC class I genes related to Gogo-A and Gogo-B, respectively, thereby illustrating the potential of this approach for efficient and highly accurate MHC genotyping. Consistent with their phylogenetic position within the hominid family, individual gorilla MHC haplotypes share characteristics with humans and chimpanzees as well as orangutans suggesting a complex history of the MHC class I genes in humans and the great apes. However, the overall MHC class I diversity appears to be low further supporting the hypothesis that gorillas might have experienced a reduction of their MHC repertoire.

MHC class I diversity in chimpanzees and bonobos.

Major histocompatibility complex (MHC) class I genes are critically involved in the defense against intracellular pathogens. MHC diversity comparisons among samples of closely related taxa may reveal traces of past or ongoing selective processes. The bonobo and chimpanzee are the closest living evolutionary relatives of humans and last shared a common ancestor some 1 mya. However, little is known concerning MHC class I diversity in bonobos or in central chimpanzees, the most numerous and genetically diverse chimpanzee subspecies. Here, we used a long-read sequencing technology (PacBio) to sequence the classical MHC class I genes A, B, C, and A-like in 20 and 30 wild-born bonobos and chimpanzees, respectively, with a main focus on central chimpanzees to assess and compare diversity in those two species. We describe in total 21 and 42 novel coding region sequences for the two species, respectively. In addition, we found evidence for a reduced MHC class I diversity in bonobos as compared to central chimpanzees as well as to western chimpanzees and humans. The reduced bonobo MHC class I diversity may be the result of a selective process in their evolutionary past since their split from chimpanzees.