Male-Mediated Gene Flow in Patrilocal Primates

Abstract

BackgroundMany group–living species display strong sex biases in dispersal tendencies. However, gene flow mediated by apparently philopatric sex may still occur and potentially alters population structure. In our closest living evolutionary relatives, dispersal of adult males seems to be precluded by high levels of territoriality between males of different groups in chimpanzees, and has only been observed once in bonobos. Still, male–mediated gene flow might occur through rare events such as extra–group matings leading to extra–group paternity (EGP) and female secondary dispersal with offspring, but the extent of this gene flow has not yet been assessed.Methodology/Principal FindingsUsing autosomal microsatellite genotyping of samples from multiple groups of wild western chimpanzees (Pan troglodytes verus) and bonobos (Pan paniscus), we found low genetic differentiation among groups for both males and females. Characterization of Y–chromosome microsatellites revealed levels of genetic differentiation between groups in bonobos almost as high as those reported previously in eastern chimpanzees, but lower levels of differentiation in western chimpanzees. By using simulations to evaluate the patterns of Y–chromosomal variation expected under realistic assumptions of group size, mutation rate and reproductive skew, we demonstrate that the observed presence of multiple and highly divergent Y–haplotypes within western chimpanzee and bonobo groups is best explained by successful male–mediated gene flow.Conclusions/SignificanceThe similarity of inferred rates of male–mediated gene flow and published rates of EGP in western chimpanzees suggests this is the most likely mechanism of male–mediated gene flow in this subspecies. In bonobos more data are needed to refine the estimated rate of gene flow. Our findings suggest that dispersal patterns in these closely related species, and particularly for the chimpanzee subspecies, are more variable than previously appreciated. This is consistent with growing recognition of extensive behavioral variation in chimpanzees and bonobos.

The Malagarasi River Does Not Form an Absolute Barrier to Chimpanzee Movement in Western Tanzania

“…They live in communities characterized by linear male dominance hierarchies and territorial defense, often showing lethal inter-group aggression [14]. Most females (50–90%) disperse from their natal group at sexual maturity to reproduce in another community [15], and in eastern chimpanzees especially, male migration rarely, if ever, occurs [16]. Given this female dispersal bias, mtDNA has commonly been used to reconstruct population history, both on large [17], [18] and small [19] scales.…”

Great ape Y Chromosome and mitochondrial DNA phylogenies reflect subspecies structure and patterns of mating and dispersal

“…Several studies have applied MSY-specific STRs, discovered by assaying the orthologs of human Y-STRs for amplifiability and polymorphism (Erler et al 2004). The resulting haplotypes are variable in all great ape populations and have been useful in revealing aspects of sex-biased dispersal in bonobos (Eriksson et al 2006), chimpanzees (Schubert et al 2011;Langergraber et al 2014), western lowland gorillas (Douadi et al 2007;Inoue et al 2013), and orangutans (Nater et al 2011;Nietlisbach et al 2012).…”

Primate Groups and Their Correlates

“…A possible explanation for this finding is that the rate of extragroup paternity might be elevated enough (6-10%) to introduce sufficient male gene flow between social groups (Schubert et al, 2011). A possible explanation for this finding is that the rate of extragroup paternity might be elevated enough (6-10%) to introduce sufficient male gene flow between social groups (Schubert et al, 2011).…”