Hybridization between two gartersnake species (Thamnophis) of conservation concern: a threat or an important natural interaction?
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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.
KeywordsAFLPs Conservation genetics Hybrid zone mtDNA Thamnophis
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).
- Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, MaldenGoogle Scholar
- Barton NH, Gale KS (1993) Genetic analysis of hybrid zones. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New YorkGoogle Scholar
- Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logicielsous Windows TM pour la genetique des populations. http://www.genetix.univ-montp2.fr/genetix/genetix.htm
- Casper GS (2003) Analysis of amphibian and reptile distributions using presence-only data. PhD dissertation, University of Wisconsin, Madison, WisconsinGoogle Scholar
- Crandall KA, Templeton AR, Sing CF (1994) Intraspecific phylogenetics: problems and solutions. In: Scotland RW, Siebert DJ, Williams DM (eds) Models in phylogeny reconstruction. Clarendon Press, OxfordGoogle Scholar
- Dalrymple GH, Reichenbach NG (1981) Interactions between the prairie garter snake (Thamnophis radix) and the common garter snake (T. sirtalis) in Killdeer Plains, Wyandot County, Ohio. Ohio Biol Surv Biol Notes 15:244–250Google Scholar
- Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, PrincetonGoogle Scholar
- Futuyma DJ (2009) Evolution, 2nd edn. Sinauer Associates, Inc., SunderlandGoogle Scholar
- Haig SM, Allendorf FW (2006) Hybrid policies under the U.S. Endangered Species Act. In: Scott JM, Gobble DD, Davis F (eds) The endangered species act at thirty: conserving biodiversity in human-dominated landscapes. Island Press, Washington, DCGoogle Scholar
- Harding JH (1997) Amphibians and reptiles of the great lakes region. The University of Michigan Press, Ann ArborGoogle Scholar
- Harrison RG (1993) Hybrids and hybrid zones: historical perspective. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New YorkGoogle Scholar
- Kirby LE (2005) A comparative study of behavior in neonate gartersnakes, Thamnophis butleri and T. radix (Colubridae), in an area of potential hybridization. MA thesis, University of Tennessee, Knoxville TennesseeGoogle Scholar
- Lewontin RC (1974) The genetic basis of evolutionary change. Columbia University Press, New YorkGoogle Scholar
- Rambaut A, Drummond AJ (2007) Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer
- Rhymer JM, Williams MJ, Braun MJ (1994) Mitochondrial analysis of gene flow between New Zealand mallards (Anas platyrhynchos) and grey ducks (A. superciliosa). Auk 111:970–978Google Scholar
- Rossman DA, Ford NB, Seigel RA (1996) The garter snakes: evolution and ecology. University of Oklahoma Press, NormanGoogle Scholar
- Swofford D (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates, SunderlandGoogle Scholar
- Venables WN, Ripley BD (2002) Modern applied statistics with S-Plus, 4th edn. Springer, New YorkGoogle Scholar
- Wynn DE, Moody SM (2006) Ohio turtle, lizard, and snake atlas. Ohio Biological Survey, ColumbusGoogle Scholar