Island demographics and trait associations in white-tailed deer

Abstract

When a population is isolated and composed of few individuals, genetic drift is the paramount evolutionary force. Inbreeding might also occur, resulting in genomic regions that are identical by descent, manifesting as runs of homozygosity (ROHs) and the expression of recessive traits; accordingly, ROH can be used to map phenotypic traits. Likewise, the genes underlying traits of interest can be revealed by comparing fixed SNPs and divergent haplotypes between affected and unaffected individuals. Populations of white-tailed deer (Odocoileus virginianus) on islands of Saint Pierre and Miquelon (SPM, France) have high incidences of leucism and malocclusions; on the Florida Keys islands (USA), deer exhibit smaller body sizes. Here we aimed to reconstruct island demography and identify the genes associated with these traits using ROHs, fixed SNPs, and divergent haplotypes as markers in a pseudo case-control design. The two island populations of interest showed reduced levels of genomic diversity, a lowNe, and a build-up of genetic load with significant divergence in Key deer. Key deer showed higher inbreeding levels, but not longer ROHs, consistent with long-term isolation and a historical bottleneck. We identified multiple trait-related genes in ROHs includingLAMTOR2which has links to hypopigmentation and HES1 which is involved in the shortening of the maxilla and mandible. Our mixed approach of linking ROH, fixed SNPs and haplotypes matched a high number (∼50) of a-priori body size candidate genes in Key deer. All three phenotypes showed patterns consistent with a complex trait and non-mendelian inheritance.

Genomic analyses capture the human-induced demographic collapse and recovery in a wide-ranging cervid

“…Together with the stable relationship of Ne/Nc over time we observed (Fig. 3), these results suggest that WTD are highly resilient; however, despite the recovery and high diversity, assessment of deleterious alleles also showed a high genetic load for WTD (Cars et al 2023;Wootton et al 2023).…”

“…S2A), all analyses suggest both populations started diverging before the isolation of the Florida Keys from the continent ~8,000 years ago (Ellsworth et al 1994;Villanova et al 2017). This separation and isolation led to a clear loss of genomic diversity and accumulation of deleterious alleles in the Florida keys (Table 1, Cars et al 2023), and they are currently listed as Endangered (U.S. Fish & Wildlife Service 1967).…”

“…This isolation led to a clear loss of genomic diversity (Table 1, Fig. S2) and accumulation of deleterious alleles in the endangered Key deer (Cars et al 2023;U.S. Fish & Wildlife Service 1967).…”

“…3), these results suggest that WTD is highly resilient. However, despite the recovery and high diversity, a detailed assessment of deleterious alleles also showed a high genetic load for WTD (Cars et al 2023;Wootton et al 2023), with a putative link to stocking efforts (Wootton et al 2023).…”