Genome-wide ancestry and introgression in a Zambian baboon hybrid zone

Abstract

Hybridization in nature offers unique insights into the process of natural selection in incipient species and their hybrids. In order to evaluate the patterns and targets of selection, we examine a recently discovered baboon hybrid zone in the Kafue River valley of Zambia, where Kinda baboons (Papio kindae) and gray-footed chacma baboons (P. ursinus griseipes) coexist with hybridization. We genotyped baboons at 14,962 variable genome-wide autosomal markers using double-digest RADseq. We compare ancestry patterns from this genome-wide dataset to previously reported ancestry from mitochondrial-DNA and Y-chromosome sources. We also fit a Bayesian genomic cline model to scan for genes with extreme patterns of introgression. We show that the Kinda baboon Y chromosome has penetrated the species boundary to a greater extent than either mitochondrial DNA or the autosomal chromosomes. We also find evidence for overall restricted introgression in the JAK/STAT signaling pathway. Echoing results in other species including humans, we find evidence for enhanced and/or directional introgression of immune-related genes or pathways including the toll-like receptor pathway, the blood coagulation pathway, and the LY96 gene. Finally we show enhanced introgression and excess chacma baboon ancestry in the sperm tail gene ODF2. Together, our results elucidate the dynamics of introgressive hybridization in a primate system while highlighting genes and pathways under selection. evaluating the actions of selection on species-specific traits (Barton & Hewitt 1989; Harrison 1990) including aspects of physiology, morphology, and behavior. At the DNA level, natural selection impacts the patterns by which genetic regions are exchanged between hybridizing lineages, with the direction and rate of introgression influenced by their selective advantage or disadvantage in differentiated genomic backgrounds (Gompert & Buerkle 2011). Regions containing variants that reduce the fitness of hybrids, for example, experience limited penetration of species boundaries while regions containing variants that increase the fitness of hybrids experience more rapid penetration of species boundaries. The latter process characterizes adaptive introgression (Hedrick 2013).Our present study centers on a hybrid zone between Kinda (Papio kindae) and gray-footed chacma baboons (P. ursinus griseipes) in the Kafue River valley in central Zambia ( Figure S1). Here, the distributions of the two species adjoin in and around the area of Kafue National Park, with Kinda and chacma baboons occupying respectively the northern and southern areas of the region. After previous speculation regarding potential overlap

Sex-mediated gene flow of grayfoot chacma baboons (Papio ursinus griseipes) in a highly seasonal habitat in Gorongosa National Park

“…One cause for the large phenotypic diversity found in these populations is thought to be related to ancient events of gene flow between grayfoot chacma, yellow and/or Kinda baboons in the area (Santander et al, 2022). Gene flow between species of the genus Papio is not uncommon (Sørensen et al, 2023), with individuals in admixture zones frequently showing phenotypic traits resembling more than one baboon species (although Sørensen et al, 2023 describe an admixture area with a phenotypically homogenous population), and admixed populations display increased genetic variation when compared to neighboring populations of parental species (e.g., Charpentier et al, 2012;Chiou et al, 2021;Jolly et al, 2011;Sørensen et al, 2023). Specifically, northerly populations of grayfoot chacma are thought to have gone through events of introgressive hybridization with yellow baboons (Keller et al, 2010;Sithaldeen et al, 2015;Sørensen et al, 2023;Santander et al, 2022;Zinner et al, 2009).…”

The Diversity of Primates: From Biomedicine to Conservation Genomics

“…Methylation-based enrichment has recently been used to analyze genome-wide ancestry and introgression in Kinda and chacma baboons across a hybridation zone (136). Restriction siteassociated DNA sequencing (RAD-seq) has been used to reduce genomic complexity for SNP generation in multiple species of primates (136,143,144) to study phylogeography, speciation, and hybridization. Finally, fluorescence-activated cell sorting has recently been used to isolate primate epithelial cells directly from the fecal samples to study population structure and local adaptation in capuchin monkeys (119).…”

“…Collecting samples from unhabituated primates is notoriously challenging. Such sampling is possible in cases where primates assemble in large, terrestrial groups (136), but rare for arboreal and cryptic taxa.…”