Selection against admixture and gene regulatory divergence in a long-term primate field study

Abstract

Genetic admixture is central to primate evolution. We combined 50 years of field observations of immigration and group demography with genomic data from ~9 generations of hybrid baboons to investigate the consequences of admixture in the wild. Despite no obvious fitness costs to hybrids, we found signatures of selection against admixture similar to those described for archaic hominins. These patterns were concentrated near genes where ancestry is strongly associated with gene expression. Our analyses also show that introgression is partially predictable across the genome. This study demonstrates the value of integrating genomic and field data for revealing how “genomic signatures of selection” (e.g., reduced introgression in low-recombination regions) manifest in nature; moreover, it underscores the importance of other primates as living models for human evolution.

Genetic variance and indirect genetic effects for affiliative social behavior in a wild primate

“…The Amboseli baboon population of southern Kenya has been the subject of ongoing research for five decades (Alberts and Altmann 2012; Alberts 2019). The ancestry of baboons in this population is primarily yellow baboon, but all individuals contain low to moderate levels of anubis baboon ancestry due to naturally occurring admixture with neighboring anubis populations (Alberts and Altmann 2001; Vilgalys et al 2022). All animals in the social groups under study (the ‘study groups’) are individually recognized on sight based on unique morphological and facial features.…”

Ecology and age, but not genetic ancestry, predict fetal loss in a wild baboon hybrid zone

“…Subjects in this study were adult females from multiple social groups of wild baboons living in the Amboseli ecosystem. This baboon population has been intensively studied for over five decades, revealing both substantial variation in pregnancy outcomes and a complex history of admixture (Alberts & Altmann, 2001; Alberts & Altmann, 2012; Beehner, Onderdonk, et al, 2006; Samuels & Altmann, 1986; Tung, Charpentier, Garfield, Altmann, & Alberts, 2008; Vilgalys et al, 2022; Wall et al, 2016). All animals in this majority-yellow baboon population are multigenerational hybrids: some individuals harbor anubis ancestry from hybridization events that predate long-term observations (hereafter, historic hybrids), while others are products of both historic gene flow and a recent wave of admixture dating from the 1980’s (hereafter, recent hybrids) (Samuels & Altmann, 1986; Tung et al, 2008; Vilgalys et al, 2022; Wall et al, 2016).…”

“…This baboon population has been intensively studied for over five decades, revealing both substantial variation in pregnancy outcomes and a complex history of admixture (Alberts & Altmann, 2001; Alberts & Altmann, 2012; Beehner, Onderdonk, et al, 2006; Samuels & Altmann, 1986; Tung, Charpentier, Garfield, Altmann, & Alberts, 2008; Vilgalys et al, 2022; Wall et al, 2016). All animals in this majority-yellow baboon population are multigenerational hybrids: some individuals harbor anubis ancestry from hybridization events that predate long-term observations (hereafter, historic hybrids), while others are products of both historic gene flow and a recent wave of admixture dating from the 1980’s (hereafter, recent hybrids) (Samuels & Altmann, 1986; Tung et al, 2008; Vilgalys et al, 2022; Wall et al, 2016). The Amboseli hybrid population is located close to the center of a narrow yellow-anubis hybrid zone in southern Kenya that minimally extends into central Kenya and likely occurs wherever anubis and yellow baboon ranges meet (Charpentier et al, 2012; Maples & McKern, 1967).…”

“…However, although current scientific consensus recognizes them as distinct species (Fischer et al, 2019; Rogers et al, 2019), they interbreed to produce hybrids at the boundaries between their current geographic ranges (Charpentier et al, 2012; Jolly et al, 2011; Phillips-Conroy & Jolly, 1986). This process of interspecific exchange appears to be part of a long, complex history of independent evolution interspersed with repeated episodes of gene flow among baboon species (Rogers et al, 2019; Vilgalys et al, 2022; Wall et al, 2016; Zinner, Groeneveld, Keller, & Roos, 2009).…”

“…In males, more anubis ancestry also predicts earlier natal dispersal and increased mating success (Charpentier et al, 2008; Tung, Charpentier, Mukherjee, Altmann, & Alberts, 2012). Nevertheless, the hybrid zone is narrow relative to the large geographic ranges of the two parent species (Charpentier et al, 2012) and genomic analyses reveal selection against admixture in Amboseli (Vilgalys et al, 2022). Together with evidence that gene flow between yellow baboons and anubis baboons is a repeated occurrence in baboon evolutionary history (Rogers et al, 2019; Vilgalys et al, 2022; Wall et al, 2016), these observations suggest that fitness costs to admixture must exist, but are likely subtle and/or temporally or spatially variable.…”