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Hybridization between two gartersnake species (Thamnophis) of conservation concern: a threat or an important natural interaction?

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Abstract

Distinguishing between hybrid zones formed by secondary contact versus parapatric divergence-with-gene-flow is an important challenge for understanding the interplay of geographic isolation and local adaptation in the origin of species. Similarly, distinguishing between natural hybrid zones and those that formed as a consequence of recent human activities has important conservation implications. Recent work has demonstrated the existence of a narrow hybrid zone between the plains gartersnake (Thamnophis radix) and Butler’s gartersnake (T. butleri) in the Great Lakes region of North America, raising questions about the history and conservation value of genetically admixed populations. Both taxa are of conservation concern, and it is not clear whether to regard hybridization as a threat or a natural interaction. Here we use phylogeographic and population genetic methods to assess the timescales of divergence and hybridization, and test for evidence that the hybrid zone is of recent origin. We assayed AFLP markers and ND2 mitochondrial DNA (mtDNA) sequences from T. radix, T. butleri, and the closely related short-headed gartersnake (T. brachystoma) throughout their North American ranges. We find shallow mtDNA divergence overall and high levels of variation within the contact zone. These patterns are inconsistent with recent contact of long-diverged taxa. It is not possible to distinguish true divergence-with-gene-flow from a long-term secondary contact zone, but we infer that the hybrid zone is a long-standing, natural interaction.

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Acknowledgments

Funding for this research was provided, in part, by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC) to DWAN and the Wisconsin Department of Natural Resources to GSC (PO Nos. NMH00000094 and NMG00001205) and to GMB and colleagues at the University of Tennessee (PO No. NMD00000655). Snakes were collected under state scientific collector permits issued to JSP, GMB, GSC (Wisconsin Endangered Species Permits 325 and 424), and others that provided tissue samples. Permission to collect samples in Canada was granted by the Ministry of Natural Resources (Permit 1051102). Protocols to collect tissue samples were approved by the University of Tennessee, Knoxville Institutional Animal Care and Use Committee (IACUC) issued to GMB (Protocol L222), the University of Texas at Tyler IACUC issued to JSP (Protocol SP2009-02), and the Animal Ethics Committee at the University of Guelph issued to RJB (Protocol 09R028). We thank Thomas Anton, Howard Aprill, Kent Bekker, Jonathan Choquette, Terrence Cox, Bill Flanagan, Brian Halstead, Randy Hetzel, Richard Kik, Wayne King, and Wisconsin DNR for assistance in collection of specimens. We thank Beth Mittermaier, Stefanie Nadeau, and Kellee Taylor for laboratory assistance. For stimulating discussions and review we are indebted to Robert Hay (Wisconsin DNR), Douglas Rossman (Luther College, IA), Richard King (Northern Illinois University) and Craig Berg (Milwaukee County Zoo).

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Authors and Affiliations

  1. Department of Biology, University of Texas at Tyler, 3900 University Blvd., Tyler, TX, 75799, USA

    John S. Placyk Jr.

  2. Department of Ecology and Evolutionary Biology, University of Tennessee, 569 Dabney Hall, Knoxville, TN, 37996, USA

    Benjamin M. Fitzpatrick, Randall L. Small, R. Graham Reynolds & Gordon M. Burghardt

  3. University of Wisconsin-Milwaukee Field Station, 3095 Blue Goose Road, Saukville, WI, 53080, USA

    Gary S. Casper

  4. Department of Integrative Biology, Science Complex, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Daniel W. A. Noble & Ronald J. Brooks

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  1. John S. Placyk Jr.
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Correspondence to John S. Placyk Jr..

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John S. Placyk Jr., Benjamin M. Fitzpatrick, Gary S. Casper, and Gordon M. Burghardt contributed equally to the content of this manuscript.

Appendix

Appendix

See Table 3.

Table 3 Collection data for Butler’s gartersnakes (Thamnophis butleri), plains gartersnakes (T. radix), short-headed gartersnakes (T. brachystoma), and hybrids used in mtDNA sequencing and genealogical and phylogenetic analyses
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Placyk, J.S., Fitzpatrick, B.M., Casper, G.S. et al. Hybridization between two gartersnake species (Thamnophis) of conservation concern: a threat or an important natural interaction?. Conserv Genet 13, 649–663 (2012). https://doi.org/10.1007/s10592-012-0315-4

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