Speciation without gene‐flow in hybridizing deer

Abstract

Under the ecological speciation model, divergent selection acts on ecological differences between populations, gradually creating barriers to gene flow and ultimately leading to reproductive isolation. Hybridisation is part of this continuum and can both promote and inhibit the speciation process. Here, we used white‐tailed (Odocoileus virginianus) and mule deer (O. hemionus) to investigate patterns of speciation in hybridizing sister species. We quantified genome‐wide historical introgression and performed genome scans to look for signatures of four different selection scenarios. Despite ample modern evidence of hybridisation, we found negligible patterns of ancestral introgression and no signatures of divergence with gene flow, rather localized patterns of allopatric and balancing selection were detected across the genome. Genes under balancing selection were related to immunity, MHC and sensory perception of smell, the latter of which is consistent with deer biology. The deficiency of historical gene‐flow suggests that white‐tailed and mule deer were spatially separated during the glaciation cycles of the Pleistocene and genome wide differentiation accrued via genetic drift. Dobzhansky‐Muller incompatibilities and selection against hybrids are hypothesised to be acting, and diversity correlations to recombination rates suggests these sister species are far along the speciation continuum.

Genomic health is dependent on long‐term population demographic history

“…Caribou samples were obtained from 67 individuals across Quebec and Labrador (Dedato et al, 2022); 53 white‐tailed deer were sampled across their North American range (Kessler et al, 2022). Additionally, 35 mountain goats were sampled across their native range from Alaska to as far south as Idaho (Martchenko & Shafer, 2022; Figure 1).…”

“…Historical estimates of N e suggest fluctuations tracking glacial cycles, with more recent estimates in the thousands (Taylor et al, 2022). The white‐tailed deer ( Odocoileus virginianus ), in contrast, is expanding northward and has accordingly high genomic diversity (Kessler et al, 2022). While white‐tailed deer currently number in the tens of millions (Kauffman et al, 2018) with historic N e estimates in the tens of thousands (Lamb et al, 2021), deer were extirpated across much their range due to colonial harvest and forestry practices (Kauffman et al, 2018); meaning this demographic expansion is very recent.…”

Genomic health is dependent on long-term population demographic history

“…Caribou samples were obtained from 67 individuals across Quebec and Labrador (Dedato et al 2022); 53 white-tailed deer were sampled across their North American range (Kessler et al 2022). Additionally, 35 mountain goats were sampled across their native range from Alaska to as far south as Idaho (Martchenko et al 2022; Figure 1).…”

“…We thank Daria Martchenko, Morgan Dedato, and Camille Kessler for help with data acquisition. Sample providers are listed in Dedato et al (2022), Martchenko & Shafer (2022), and Kessler et al (2022). We thank three anonymous reviewers for comments that strengthened this manuscript.…”

“…Historical estimates of N e suggest fluctuations tracking glacial cycles, with more recent estimates in the thousands (Taylor et al 2021). The white-tailed deer ( Odocoileus virginianus ), in contrast, is expanding northward and has accordingly high genomic diversity (Kessler et al, 2022). While white-tailed deer currently number in the 10s of millions (Kauffman et al, 2018) with historic N e estimates in the tens of thousands (Lamb et al 2021), deer were extirpated across much their range due to colonial harvest and forestry practices (Kauffman et al, 2018); meaning this demographic expansion is very recent.…”