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

Abstract

Admixture has profoundly influenced evolution across the tree of life, including in humans and other primates1,2. However, we have limited insight into the genetic and phenotypic consequences of admixture in primates, especially during its key early stages. Here, we address this gap by combining 50 years of field observations with population and functional genomic data from yellow (Papio cynocephalus) and anubis (P. anubis) baboons in Kenya, in a longitudinally studied population that has experienced both historical and recent admixture3. We use whole-genome sequencing to characterize the extent of the hybrid zone, estimate local ancestry for 442 known individuals, and predict the landscape of introgression across the genome. Despite no major fitness costs to hybrids, we identify signatures of selection against introgression that are strikingly similar to those described for archaic hominins4–6. These signatures are strongest near loci with large ancestry effects on gene expression, supporting the importance of gene regulation in primate evolution and the idea that selection targeted large regulatory effects following archaic hominin admixture7,8. Our results show that genomic data and field observations of hybrids are important and mutually informative. They therefore demonstrate the value of other primates as living models for phenomena that we cannot observe in our own lineage.

Mechanisms of inbreeding avoidance in a wild primate

“…We also re-ran the main model to include admixture-related variables: as noted above, the Amboseli baboon population includes yellow-anubis baboon hybrids (P. cynocepha lus 3 P. anubis), and genetic ancestry is known to affect consortship formation in this population 18 (STAR Methods). The results were qualitatively similar to the main model, even with the reduced sample size resulting from including only animals with genome-wide admixture scores 43 (Table S1). The adolescent model: Inbreeding avoidance when females were subfertile Evidence from several mammals suggests that females may be most likely to mate with kin when they are least likely to conceive.…”

“…Genetic ancestry in the population is largely from the yellow baboon (P. cynocephalus), but admixture over time with anubis baboons (P. anubis; also known as the olive baboon) means that nearly all animals in the population are hybrids. 11,12,43,53 The study system has been described in-depth elsewhere. 13,52…”

Predictability and parallelism in the contemporary evolution of hybrid genomes

“…These include broad selection against minor parent ancestry across the genome (presumably due to the mechanisms outlined above) and stronger depletion of minor parent ancestry in regions of the genome with a high density of conserved or coding elements [ 8 , 12 , 34 , 35 ]. Another key variable highlighted by empirical and theoretical studies is the importance of the interplay between recombination rate and selection, with several groups finding that selection on hybrids generates a positive correlation between local recombination rate and minor parent ancestry [ 8 , 34 – 40 ]. This correlation is thought to be driven by how the local recombination rate impacts the decoupling of neutral or adaptive alleles from alleles that are deleterious in hybrids.…”

Mate choice enhances post-zygotic barriers to gene flow via ancestry bundling

“…In addition, Tung et al (2012) found that males with more anubis ancestry are favoured in mate choice overall, and that there is also ancestry-based assortative mating. If, as genomic evidence suggests (Vilgalys et al 2021), the minor parent ancestry (anubis) has historically been deleterious in this population, then our calculations above imply that it is the ancestry correlation coefficient within mating pairs that determines the impact of ancestry bundling on the purging of anubis ancestry. In particular, while there is a directional mating advantage of anubis ancestry, this is part of overall direct selection on ancestry, and therefore included in the selection gradient along with other factors, while assortative mating increases ancestry variance (see section "The rate of purging is proportional to the population ancestry variance" above).…”

“…One system where this is possible is the long-term study of baboons in Kenya's Amboseli basin (Alberts & Altmann 2001). There, yellow baboons (Papio cynocephalus) and anubis baboons (P. anubis) hybridize (Alberts & Altmann 2001, and genomic analyses indicate that the minor anubis ancestry has been purged over time (Vilgalys et al 2021). Tung et al (2012) used long-term observations of mating behaviour in this system to investigate the determinants of mating success and mate pair composition, revealing ancestry-based assortative mating.…”