Molecular Genetics Laboratory

In the absence of multigeneration pedigrees, it is challenging but not impossible to use genetic analysis to decipher which pairs of individuals are parent-offspring or siblings, and we have described this painstaking process in detail (Städele & Vigilant 2016; Langergraber et al., 2007). Assessment of kinship and behavior is particularly interesting in chimpanzees because male chimpanzees are philopatric and thus spend their entire lives in the same group and engage in extensive affiliative and cooperative behavior. We have determined that in wild chimpanzee communities, the majority of adult individuals are unrelated to one another (Lukas et al., 2005; Langergraber et al., 2007). Furthermore, while maternal brothers cooperate at high rates, unrelated males also form close bonds, while paternal brothers exhibit no preference for one another (Langergraber et al., 2007). Similarly, although female chimpanzee also form social bonds with one another, pairs of close kin are rare (Langergraber et al., 2009). This suggests that like humans, chimpanzees are quite flexible in their choice of cooperative partners. Wild white-faced capuchin females typically have several maternal and paternal female relatives in the group, but only exhibit preferences for maternal kin (Perry et al., 2008) and along with the evidence from chimpanzees this suggests that preferences for paternal kin may not be widespread in primates. Both male and female gorillas disperse and thus are not expected to be in groups with their relatives. However, analysis of multiple groups of western gorillas suggested that male silverback gorillas may range near relatives, and suggested that this may account for the somewhat puzzling accounts of reduced aggression observed (Bradley et al., 2004). Despite dispersing one or more times, female gorillas also have the potential for interactions with kin, as they often end up in a group containing a female relative (Bradley et al., 2007; Arandjelovic et al., 2014) as do female hamadryas baboons (Städele et al, 2016). In both mountain gorillas and in capuchin monkeys we have focused on behavior of the dominant males, mothers and infants to begin to understand social or biological cues for kinship (Rosenbaum et al., 2015; Rosenbaum et al., 2016; Godoy et al., 2016).

Primate males compete for reproductive opportunities, and genetic analysis is necessary to determine who has succeeded in fathering offspring.  In chimpanzees, males with high social rank generally have higher reproductive success (Vigilant et al., 2001; Boesch et al., 2006; Newton-Fisher et al., 2010) although this advantage varies with group size and other factors (Inoue et al., 2008). Male-female dyadic associations influence the distribution of paternities in chimpanzees (Langergraber et al, 2013) and Assamese macaques (Ostner et al., 2013).  Furthermore, cooperative relationships among male Assamese macaques affect rank and influence the distribution of paternities in the group (Schülke et al., 2010). Mature male orang-utans may remain gracile or develop pronounced secondary sexual characteristics such as large size and cheek pads, and each strategy may have situation-dependent advantages in obtaining paternities (Banes et al., 2015). In mountain gorilla groups containing more than one male, the dominant male sires the majority of the offspring but apparently cannot prevent subordinates from also achieving some reproductive success (Bradley et al., 2005; Nsubuga et al., 2008).  In primate groups in which the dominant male sires the majority of the offspring, he is usually deposed before his daughters reach breeding age and so inbreeding is avoided.  However, in some groups of wild white-faced capuchin monkeys, males may have lengthy tenures as the alpha male. We found that fathers and daughters avoided breeding in such groups, even though the alpha was otherwise reproductively dominant (Muniz et al., 2006; Muniz et al., 2010). Similarly, dominant mountain gorilla males and their resident daughters do not produce offspring, but other forms of inbreeding are not avoided (Vigilant et al., 2015). In capuchin monkeys breeding of both parent-offspring and sibling pairs is avoided, and inbred offspring reproduce later, demonstrating a fitness cost to inbreeding (Godoy et al., 2016).

Do discontinuous habitats hinder dispersal among population fragments? In continuous habitats, does the environment play a role in structuring dispersal movements? more Based on a study of black and white colobus monkeys, we suggested that often neither observation nor genetic data alone suffice to elucidate patterns of sex-biased dispersal in group-living species (Harris et al., 2009). Indeed, genetic analysis revealed greater than expected male-mediated gene flow in bonobos (Schubert et al., 2011) but refuted suggestions of dispersal of dependent offspring in chimpanzees (Langergraber et a., 2014).  We demonstrated that the species-typical pattern of male philopatry and dispersal is likely retained even in a chimpanzee population living in an extreme savannah habitat (Moore et al., 2015).  Hamadryas baboons are one of the few primates to have a multilevel society akin to that in humans, and we used genetic analysis to elucidate the extent of sex biases in dispersal at each level (Städele et al., 2015). Gorillas exhibit both male and female dispersal, and so are especially interesting for the comprehensive study of dispersal dynamics and its consequences. In a study of the highly endangered Cross River gorillas, we showed that dispersal among fragments appears to be ongoing, which is encouraging for efforts to protect their habitat and dispersal corridors (Bergl and Vigilant, 2007). Population genetic structure of the Bwindi mountain gorillas suggests that females prefer to disperse to nearby groups that have diet choices similar to those they are accustomed to, and thus that these female mountain gorillas are potentially exhibiting a previously unsuspected natal habitat bias (Guschanski et al., 2008).  Genetic structure analysis of the entire Virungas mountain gorilla population showed that males tend to disperse farther than females in this population (Roy et al., 2014). The geographic distribution of genetic diversity in western gorillas shows that rivers are an impediment to gene flow (Fünfstück et al., 2015a). In contrast, the pattern of isolation-by-distance shown across the range of eastern and central chimpanzees is not consistent with differentiation between these purported subspecies (Fünfstück et al., 2015b).

We recently used data from apes to estimate generation times and suggest that population splits between the incipient gorilla, chimpanzee and human species were substantially older than previously suggested (Langergraber et al., 2012). We used Y-chromosome data to show that, as in humans, patrilocal chimpanzee communities show signs of genetic continuity for hundreds or thousands of years (Langergraber et al., 2014). Studies of cultural behaviors in chimpanzees need to carefully account for genetic similarity between populations as an explanation for patterns of cultural variation (Langergraber et al., 2011) and hypotheses for the evolution of complex cooperation in humans are insufficient if they cannot exclude chimpanzees (Langergraber et al., 2011). By generating ~ 15 kb of autosomal DNA sequence data from representatives of western and eastern gorillas and using coalescent modeling approaches we inferred that the western and eastern gorilla species split about 1 million years ago but continued to exchange migrants until perhaps as recently as 80,000 years ago (Thalmann et al., 2007), a result supported by subsequent whole genome analyses (Scally et al., 2012). We found that the eastern lowland and mountain gorilla populations split around 10,000 years ago followed around 5000 years ago by the split of the two mountain gorilla populations and their decrease in size and genetic diversity (Roy et al., 2014). The low diversity observed in the Cross River gorillas, a small disjunct population of western gorillas, was investigated using both contemporary (Bergl et al., 2008) and museum samples (Thalmann et al, 2011) and linked to a population size decrease in the deeper past as well as the last few hundred years.  There are many species of gibbons, some of which hybridize where their populations meet, and we conducted extensive study of gibbon population histories with a particular focus on Hylobates using mtDNA, Y-chromosome, and genomic sequencing (Chan et al., 2010; Chan et al., 2012, Chan et al., 2013).

Estimating the number of individuals in a wildlife population is difficult, but genetic mark-recapture methods have the potential to not only provide an abundance estimate, as well as information concerning individual relationships, dispersal, and population structure. We have shown that genetic population estimation approaches are more precise than counting indirect signs, such as night nests made by gorillas (Bradley et al., 2008; Guschanski et al., 2009; Vigilant & Guschanski 2009; Arandjelovic et al., 2011) We analyzed hundreds of samples collected over several years in Loango, Gabon and derive estimates of the numbers of gorillas and chimpanzees using the area, as well as group compositions, minimum ranging patterns, and group dynamics (Arandjelovic et al., 2010, 2011, 2014).  In collaborative work with the Chinese Academy of Sciences (Zoology, Beijing) we assessed the population size, structure and genetic diversity of an important population of Sichuan snub-nosed monkeys (Chang et al., 2011; Chang et al., 2012). We have applied genetic mark-recapture to chimpanzees living in forest fragments (Chancellor et al., 2012; McCarthy et al., 2015) as well as savannah (Moore & Vigilant 2014 a, b). In recent work we applied genetic mark-recapture approaches to a chimpanzee population of known size in order to quantify accuracy and precision and identify sources of bias (Granjon et al., 2016). The difficulty of encountering and sampling all individuals, even within the limited range of a mountain gorilla population (Roy et al., 2014), highlights the importance of intense sampling (and consequent laboratory) effort for attaining a precise population estimate, and we recently conducted a pilot project using dogs to detect feces in a rugged Cross River gorilla habitat (Arandjelovic et al., 2015).

Genetic analysis of loci assumed to be functionally neutral, such as mtDNA or microsatellites, has been the focus of most studies in wild primate populations. Challenges associated with the use of low quality, low concentration DNA from noninvasive sources, such as feces, chewed fruit or hair, has hindered application of the large- scale sequencing approaches useful to understand functionally relevant genomic variation. The immune genes of the MHC represent the most variable portion of the genome, and analysis of MHC variation can provide information on how individuals and populations have responded to pathogens over time. Our first investigation of MHC variation using traditional sequencing approaches applied to DNA from noninvasive samples showed that it was not yet feasible to analyze large numbers of noninvasive samples (Lukas et al., 2004). We recently used short read high throughput sequencing to characterize novel MHC Class II sequences from gorillas using noninvasive DNA (Hans et al., 2015). Ongoing work is aimed at using varied high throughput sequencing approaches to characterize MHC variation in gorillas, chimpanzees and bonobos for inference of past selective events and elucidation of current patterns of diversity among populations. In collaboration with the PanAf project  http://www.eva.mpg.de/primat/research-groups/great-ape-evolutionary-ecology-and-conservation/panaf.html we are interested in the genomic variation underlying the ecological, cultural and geographic variation across the extant populations of chimpanzees.