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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 and results in the loss of genetic diversity. 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. 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, both considered genetic defects; on the Florida Keys islands (USA) deer exhibit smaller body sizes, a polygenic trait. Here we aimed to reconstruct island demography and identify the genes associated with these traits in a pseudo case-control design. The two island populations showed reduced levels of genomic diversity and a build-up of deleterious mutations compared to mainland deer; there was also significant genome-wide divergence in Key deer. Key deer showed higher inbreeding levels, but not longer ROHs, consistent with long-term isolation. We identified multiple trait-related genes in ROHs including LAMTOR2 which has links to pigmentation changes, and NPVF which is linked to craniofacial abnormalities. Our mixed approach of linking ROHs, fixed SNPs and haplotypes matched a high number (~50) of a-priori body size candidate genes in Key deer. This suite of biomarkers and candidate genes should prove useful for population monitoring, noting all three phenotypes show patterns consistent with a complex trait and non-Mendelian inheritance.

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Fig. 1
Fig. 2: Deer demographic history.
Fig. 3: Genome health metrics.
Fig. 4: Summary of deleterious mutations.

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Data availability

Raw reads for the 25 deer additional individuals were deposited on the NCBI Sequence Read Archive (Accession number PRJNA830519). All scripts are available on GitLab (https://gitlab.com/WiDGeT_TrentU/undergrad-theses/-/tree/master/%20Cars_2023).

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Acknowledgements

Participation from hunters, managers and community members is essential to this research. We want to thank the community of St-Pierre and Miquelon that provided samples. Additional Florida Key samples were provided by George Zaragoza; the remaining providers are found listed in (Kessler et al. 2023). BC was supported by a Natural Sciences and Engineering Research Council (NSERC) Undergraduate Student Research Award and the Trent Summer Work Experience Program. This work was supported by NSERC Discovery Grant (ABAS; SDC); ComputeCanada Resources for Research Groups (ABAS); Canadian Foundation for Innovation (ABAS): John R. Evans Leaders Fund (ABAS) and the Ontario Early Researcher Award (ABAS). We thank four anonymous referees and the Editor for valuable comments. Trent University is located on the traditional territory of the Michi Saagiig Anishnaabeg.

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BC and ABAS conceived the study, BC, CK, EH, SDC, DK, ABAS collected the samples, BC and CK performed the molecular laboratory work and the bioinformatic analyses with contribution from ABAS. BC and ABAS wrote the initial draft of the manuscript, all authors reviewed and commented on the manuscript.

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Correspondence to Aaron B. A. Shafer.

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All experiments have been conducted as per the guidelines of the Trent University Research Ethics Board. No approval of research ethics committees was required to accomplish the goals of this study because sequencing work was conducted on samples donated by hunters or collected as roadkill.

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Cars, B.S., Kessler, C., Hoffman, E.A. et al. Island demographics and trait associations in white-tailed deer. Heredity 133, 1–10 (2024). https://doi.org/10.1038/s41437-024-00685-2

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