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

Conservation Genetics

Volumn 13, Issue 3, 2012, Pages 649-663

  Placyk Jr , John S ^a   Fitzpatrick, Benjamin M ^b   Casper, Gary S ^c   Small, Randall L ^b   Reynolds, R Graham ^b   Noble, Daniel W A ^d   Brooks, Ronald J ^d   Burghardt, Gordon M ^b  

^a UNIVERSITY OF TEXAS AT TYLER   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^d UNIVERSITY OF GUELPH   (Canada)

Author keywords

AFLPs; Conservation genetics; Hybrid zone; mtDNA; Thamnophis

Indexed keywords

CONSERVATION GENETICS; DIVERGENCE; GENE FLOW; HUMAN ACTIVITY; HYBRID; HYBRIDIZATION; INTERSPECIFIC INTERACTION; LOCAL ADAPTATION; MITOCHONDRIAL DNA; PHYLOGEOGRAPHY; POPULATION STRUCTURE; SNAKE; TAXONOMY; TIMESCALE;

GREAT LAKES [NORTH AMERICA];

THAMNOPHIS; THAMNOPHIS BRACHYSTOMA; THAMNOPHIS BUTLERI; THAMNOPHIS RADIX;

EID: 84860494995     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-012-0315-4     Document Type: Article

References (63)

1. Alfaro ME, Arnold SJ (2001) Molecular systematics and evolution of Regina and the Thamnophiine snakes. Mol Phylogenet Evol 21: 408-423.
2. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Malden.
3. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16: 613-622.
4. Anderson E (1948) Hybridization of the habitat. Evolution 2: 1-9.
5. Austin JD, Lougheed SC, Neidrauer L, Chek AA, Boag PT (2002) Cryptic lineages in a small frog: the post-glacial history of the spring peeper, Pseudacris crucifer (Anura: Hylidae). Mol Phylogenet Evol 25: 316-329.
6. Ayres DR, Smith DL, Zaremba K, Klohr S, Strong DR (2004) Spread of exotic cordgrasses and hybrids (Spartina sp.) in the tidal marshes of San Francisco Bay, California, USA. Biol Invasions 6: 221-231.
7. Barton NH, Gale KS (1993) Genetic analysis of hybrid zones. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York.
8. 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.
9. Bloomquist EW, Lemey P, Suchard MA (2010) Three roads diverged? Routes to phylogeographic inference. Trends Ecol Evol 25: 626-632.
10. Casper GS (2003) Analysis of amphibian and reptile distributions using presence-only data. PhD dissertation, University of Wisconsin, Madison, Wisconsin.
11. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9: 1657-1659.
12. 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, Oxford.
13. Creer S, Thorpe RS, Malhotra A, Chou W-H, Stenson AG (2004) The utility of AFLPs for supporting mitochondrial DNA phylogeographical analyses in the Taiwanese bamboo viper, Trimeresurus stejnegeri. J Evol Biol 17: 100-107.
14. 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: 244-250.
15. Dalrymple GH, Reichenbach NG (1984) Management of an endangered species of snake in Ohio, USA. Biol Conserv 30: 195-200.
16. de Queiroz A, Lawson R, Lemos-Espinal JA (2002) Phylogenetic relationships of North American garter snakes (Thamnophis) based on four mitochondrial genes: how much DNA sequence is enough? Mol Phylogenet Evol 22: 315-329.
17. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11: 2571-2581.
18. Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton.
19. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14: 2611-2620.
20. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164: 1567-1587.
21. Fitzpatrick BM, Shaffer HB (2007) Hybrid vigor between native and introduced salamanders raises new challenges for conservation. Proc Natl Acad Sci USA 104: 15793-15798.
22. Fitzpatrick BM, Placyk JS Jr, Niemiller ML, Casper GS, Burghardt GM (2008) Distinctiveness in the face of gene flow: hybridization between specialist and generalist gartersnakes. Mol Ecol 17: 4107-4117.
23. Ford NB (1982) Species specificity of sex pheromone trails of sympatric and allopatric garter snakes. Copeia 1982: 10-13.
24. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133: 693-709.
25. Futuyma DJ (2009) Evolution, 2nd edn. Sinauer Associates, Inc., Sunderland.
26. 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, DC.
27. Harding JH (1997) Amphibians and reptiles of the great lakes region. The University of Michigan Press, Ann Arbor.
28. Harrison RG (1993) Hybrids and hybrid zones: historical perspective. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York.
29. 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 Tennessee.
30. Kumazawa Y, Ota H, Nishida M, Ozawa T (1996) Gene rearrangements in snake mitochondrial genomes: highly concerted evolution of control-region-like sequences duplicated and inserted into a tRNA gene cluster. Mol Biol Evol 13: 1242-1254.
31. Laurie CC, Nickerson DA, Anderson AD, Weir BS, Livingston RJ, Dean MD, Smith KL, Schadt EE, Nachman MW (2007) Linkage disequilibrium in wild mice. PLOS Genetics 3: e144. doi: 110. 1371/journal. pgen. 0030144.
32. Lewontin RC (1974) The genetic basis of evolutionary change. Columbia University Press, New York.
33. Long JC (1991) The genetic structure of admixed populations. Genetics 127: 417-428.
34. Mims MC, Hulsey CD, Fitzpatrick BM, Streelman JT (2010) Geography disentangles introgression from ancestral polymorphism in Lake Malawi cichlids. Mol Ecol 19: 940-951.
35. Muhlfeld CC, Kalinowski ST, McMahon TE, Taper ML, Painter S, Leary RF, Allendorf FW (2009) Hybridization rapidly reduces fitness of a native trout in the wild. Biol Lett 5: 328-331.
36. Nice CC, Anthony N, Gelembiuk G, Raterman D, French-Constant R (2005) The history and geography of diversification within the butterfly genus Lycaeides in North America. Mol Ecol 14: 1741-1754.
37. Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18: 375-402.
38. O'Brien SJ, Mayr E (1991) Bureaucratic mischief: recognizing endangered species and subspecies. Science 251: 1187-1188.
39. Peter BM, Wegmann D, Excoffier L (2010) Distinguishing between population bottleneck and population subdivision by a Bayesian model choice procedure. Mol Ecol 19: 4648-4660.
40. Placyk JS Jr, Burghardt GM, Small RL, King RB, Casper GS, Robinson JW (2007) Post- glacial recolonization of the Great Lakes region by the common gartersnake (Thamnophis sirtalis) inferred from mtDNA sequences. Mol Phylogenet Evol 43: 452-467.
41. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
42. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
43. Rambaut A, Drummond AJ (2007) Tracer v1. 4. Available from http://beast. bio. ed. ac. uk/Tracer.
44. Rhymer JM, Simberloff DS (1996) Genetic extinction through hybridization and introgression. Annu Rev Ecol Syst 27: 83-109.
45. 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: 970-978.
46. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
47. Rossman DA, Ford NB, Seigel RA (1996) The garter snakes: evolution and ecology. University of Oklahoma Press, Norman.
48. Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174-175.
49. Ryan ME, Johnson JR, Fitzpatrick BM (2009) Invasive hybrid tiger salamander genotypes impact native amphibians. Proc Natl Acad Sci USA 106: 11166-11171.
50. Savolainen V, Anstett M-C, Lexer C, Hutton I, Clarkson JJ, Norup MV, Powell MP, Springate D, Salamin N, Baker WJ (2006) Sympatric speciation in palms on an oceanic island. Nature 441: 210-213.
51. Schwartz MK, Pilgrim KL, McKelvey KS, Lindquist EL, Claar JJ, Loch S, Ruggiero LF (2004) Hybridization between Canada lynx and bobcats: genetic results and management implications. Conserv Genet 5: 349-355.
52. Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol 17: 30-44.
53. Swofford D (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4. 0b10. Sinauer Associates, Sunderland.
54. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
55. Taylor EB, Boughman JW, Groenenboom M, Sniatynski M, Schluter D, Gow JL (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol Ecol 15: 343-355.
56. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonucleases mapping and DNA sequence data. III. Cladogram estimation. Genetics 132: 619-633.
57. Thompson JD, Gibson TJ, Plewnial F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
58. Venables WN, Ripley BD (2002) Modern applied statistics with S-Plus, 4th edn. Springer, New York.
59. Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15: 1039-1053.
60. Wynn DE, Moody SM (2006) Ohio turtle, lizard, and snake atlas. Ohio Biological Survey, Columbus.
61. Zamudio KR, Savage WK (2003) Historical isolation, range expansion, and secondary contact of two highly divergent mitochondrial lineages in spotted salamanders (Ambystoma maculatum). Evolution 57: 1631-1652.
62. Zhivotovsky LA (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Mol Ecol 8: 907-913.
63. Zink RM (2005) Natural selection on mitochondrial DNA in Parus and its relevance for phylogeographic studies. Proc R Soc Biol 272: 71-78.