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Population genetic and genomic analyses of Western Massasauga (Sistrurus tergeminus ssp.): implications for subspecies delimitation and conservation

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Abstract

The Western Massasauga (Sistrurus tergeminus) is a small North American rattlesnake found west of the Mississippi River. Sistrurus tergeminus has previously been divided into two putative subspecies, Desert (S. t. edwardsii) and Prairie Massasaugas (S. t. tergeminus) based upon qualitative variation in morphology, coloration, and habitat. The Desert Massasauga subspecies has been formally petitioned for federal listing under the U.S. Endangered Species Act. Our overarching goal was to evaluate genetic structure and genomic differentiation between specimens of the two putative subspecies in an effort to inform ongoing conservation assessments. To that end, we generated whole genome sequence data for both putative taxa and then developed nearly 200 genetic markers from different fractions of the genome (~ 50 intergenic and ~ 50 genic markers from each of the two subspecies) to test for population structure across much of the Western Massasauga range. Mean genomic divergence between subspecies was 0.0041 ± 0.0080 (Kimura’s 2-parameter distance) for nuclear sequences and 0.0175 ± 0.0031 for mitochondrial sequences, both exceedingly low values which approach the minimum of zero. Admixture analyses and F-statistics both indicated that regardless of how the markers were partitioned, genetic structure was oriented far more along a geographic axis (isolation-by-distance) than a taxonomic axis (i.e., between putative subspecies). Overall, our analyses provide little support that formal protection of the purported Desert Massasauga is warranted based on the homogeneity of the collective Western Massasauga gene pool.

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Data availability

Sequencing reads and assemblies have been submitted to NCBI under BioProject accession PRJNA668351.

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Analyses were conducted in R or Unix environments and scripts are available in the Online Resources.

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Acknowledgements

We thank Andrew Holycross, Lisle Gibbs, Stephen Mackessy, Paul Crump, Jason Jones, Doug Burkett, Ian Latella, Sean Graham, Nathan Rains, and Dan Walker for providing samples of Sistrurus tergeminus and Sistrurus catenatus. We also acquired tissue samples from the Texas Natural History Collection (Travis LaDuc), Gladys Porter Zoo (Thomas deMaar), Museum of Southwestern Biology (Tom Giermakowski), Sternberg Museum of Natural History (Curtis Schmidt), Sam Noble Oklahoma Museum of Natural History (Jessa Watters), and Texas State University (Michael R. J. Forstner). We thank Lisle Gibbs, Alex Ochoa, and Scott Martin for their generosity in sharing the Sistrurus catenatus nuclear and mitochondrial genome assemblies. We thank Drew R. Schield for his help in obtaining and navigating the Crotalus viridis genome assembly. We also thank Drs. Lisle Gibbs, Anna Brüniche-Olsen, Phillip San Miguel, Janna Willoughby, Alex Ochoa and members of the DeWoody Lab for their invaluable feedback and advice at many different parts of the process. This research was supported in part by the National Institute for Food and Agriculture, National Fish and Wildlife Foundation, U.S. Fish and Wildlife Service, and Texas Parks and Wildlife Department. Field work was conducted under the authority of Permits issued by the Texas Parks and Wildlife Department (SPR-0506-662) and the New Mexico Department of Game and Fish (NMDGF Sci# 3742) to Toby J. Hibbitts. This study was approved by the Texas A&M University Institutional Animal Care and Use Committee (AUP 2016-178). This is publication number 1657 of the Biodiversity Research and Teaching Collections at Texas A&M University.

Funding

This research was supported in part by the National Institute for Food and Agriculture, National Fish and Wildlife Foundation, U.S. Fish and Wildlife Service, and Texas Parks and Wildlife Department.

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Correspondence to Rian Bylsma.

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Field work was conducted under the authority of Permits issued by the Texas Parks and Wildlife Department (SPR-0506-662) and the New Mexico Department of Game and Fish (NMDGF Sci# 3742) to Toby J. Hibbitts. This study was approved by the Texas A&M University Institutional Animal Care and Use Committee (AUP 2016-178).

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Bylsma, R., Walkup, D.K., Hibbitts, T.J. et al. Population genetic and genomic analyses of Western Massasauga (Sistrurus tergeminus ssp.): implications for subspecies delimitation and conservation. Conserv Genet 23, 271–283 (2022). https://doi.org/10.1007/s10592-021-01420-8

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  • DOI: https://doi.org/10.1007/s10592-021-01420-8

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