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Conservation Genetics

, Volume 13, Issue 2, pp 443–454 | Cite as

Conservation genetics of an endemic mountaintop salamander with an extremely limited range

  • Claire S. O. Bayer
  • Andrew M. Sackman
  • Kelly Bezold
  • Paul R. Cabe
  • David M. MarshEmail author
Research Article

Abstract

Montane regions can promote allopatric speciation and harbor unique species with small ranges. The southern Appalachians are a biodiversity hotspot for salamanders, and several montane endemics occur in the region. Here, we present the first DNA sequence data for Plethodon sherando, a terrestrial salamander recently discovered in the Blue Ridge Mountains of Virginia. We sequenced two mitochondrial regions (cyt-b and CO1) from salamanders at reference sites near the center of P. sherando’s range and from two contact zones where P. sherando populations are replaced by Plethodon cinereus, the Northern Red-Backed salamander. We then used these sequence data to examine divergence and hybridization between the two taxa. We found P. sherando and P. cinereus morphotypes from contact zones to be reciprocally monophyletic and highly divergent (~17%). P. sherando exhibited very low sequence diversity (π = 0.0010) as compared to P. cinereus from the same locations (π = 0.0096). Salamander morphology in the contact zone was as distinct as morphology at reference sites, and discriminant function analysis based on morphology successfully classified 98% of salamanders to their mitochondrial lineage. Phylogenetic analysis of cyt-b sequences showed P. sherando to be sister to Plethodon serratus (the Southern Red-Backed salamander) rather than P. cinereus or any nearby mountaintop endemics. Our results suggest that P. sherando is a distinct lineage that is not subject to substantial introgression from P. cinereus and that may have a history of geographic isolation. Given its limited range (<80 km2), we believe P. sherando should merit a conservation status similar to that of other mountaintop salamanders in the region.

Keywords

Plethodonsherando Big Levels salamander Plethodon cinereus mtDNA Phylogeography Population genetics 

Notes

Acknowledgments

We thank Shane Ramee and members of the 2009 Field Herpetology class for help with collecting salamanders. Briana Gregory and Woodrow Friend assisted with DNA extractions and Jennifer Schieltz and Caroline Bovay contributed to the GIS analysis. We thank Richard Highton, Nadia Ayoub, and two anonymous reviewers for helpful comments on earlier drafts of this manuscript. This research was covered by Virginia state collection permit #33510 and IACUC animal care and use permit DM0109. Financial support for this study was provided by the U.S. Forest Service, a Howard Hughes Medical Institute award to Washington & Lee University under the Undergraduate Science Education Program, and an H. F. Lenfest grant to D Marsh.

References

  1. Adams DC (2004) Character displacement via aggressive interference in Appalachian salamanders. Ecology 85:2664–2670CrossRefGoogle Scholar
  2. Adams DC, West ME, Collyer ML (2007) Location-specific sympatric morphological divergence as a possible response to species interactions in West Virginia Plethodon salamander communities. J Anim Ecol 76:289–295PubMedCrossRefGoogle Scholar
  3. Anderson E, Maldonado-Ocampo J (2010) A regional perspective on the diversity and conservation of the tropical Andean fishes. Conserv Biol 25:30–39PubMedCrossRefGoogle Scholar
  4. Arif S, Wicknick JA, Adams DC (2007) Bioclimatic modeling, morphology, and behavior reveal alternative mechanisms regulating the distributions of two parapatric salamander species. Evol Ecol Res 9:843–854Google Scholar
  5. Babik W, Branicki W, Crnobnja-Isailović J, Cogălniceanu D, Sas I, Olgun K, Poyarkov NA, Garcia-País M, Arntzen JW (2005) Phylogeography of two European newt species—discordance between mtDNA and morphology. Mol Ecol 14:2475–2491PubMedCrossRefGoogle Scholar
  6. Bensasson D, Zhang D-X, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16:314–321PubMedCrossRefGoogle Scholar
  7. Cabe P, Hanlon T, Aldrich M, Connors L, Marsh D (2007) Fine-scale population differentiation and gene flow in a terrestrial salamander (Plethodon cinereus) living in continuous habitat. Heredity 98:53–60PubMedCrossRefGoogle Scholar
  8. Carpenter D, Jung R, Sites J (2001) Conservation genetics of the endangered Shenandoah Salamander (Plethodon shenandoah, Plethodontidae). Anim Conserv 4:111–119CrossRefGoogle Scholar
  9. Chan C, Ballantyne K, Aikman H, Fastier D, Daugherty C, Chambers G (2006) Genetic analysis of interspecific hybridization in the world’s only Forbes’ parakeet (Cyanoramphus forbesi) natural population. Conserv Genet 7:493–506CrossRefGoogle Scholar
  10. Colliard C, Sicilia A, Turrisi G, Arculeo M, Perrin N, Stöck M (2010) Strong reproductive barriers in a narrow hybrid zone of west-mediterranean green toads (Bufo viridis subgroup) with Plio-Pleistocene divergence. BMC Evol Biol 10:232PubMedCrossRefGoogle Scholar
  11. Connors LM, Cabe PR (2003) Isolation of dinucleotide microsatellite loci from red-backed salamanders (Plethodon cinereus). Mol Ecol Notes 3:131–133CrossRefGoogle Scholar
  12. Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference, and the multispecies coalescent. Trends Ecol Evol 24:332–340PubMedCrossRefGoogle Scholar
  13. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis sampling trees. BMC Evol Biol 7:214PubMedCrossRefGoogle Scholar
  14. Duellman WE, Sweet SS (1999) Distribution patterns of amphibians in the Nearctic region of North America. In: Duellman WE (ed) Patterns of distribution of amphibians. Johns Hopkins Univ. Press, Baltimore, pp 31–109Google Scholar
  15. Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, SeattleGoogle Scholar
  16. Fraley C, Raftery AE (2006) MCLUST version 3 for R: normal mixture modeling and model-based clustering. Technical report. Department of Statistics, University of Washington, SeattleGoogle Scholar
  17. Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends Ecol Evol 25:325–331PubMedCrossRefGoogle Scholar
  18. Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
  19. Hastie T, Tibshirani R, Friedman JH (2001) Elements of statistical learning. Springer, New YorkGoogle Scholar
  20. Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. PNAS 101:14812–14817PubMedCrossRefGoogle Scholar
  21. Hegde SG, Nason JD, Clegg JM, Ellstrand NC (2006) The evolution of California’s wild radish has resulted in the extinction of its progenitors. Evolution 60:1187–1197PubMedGoogle Scholar
  22. Highton R (1995) Speciation in Eastern North American salamanders of the genus Plethodon. Annu Rev Ecol Syst 26:579–600CrossRefGoogle Scholar
  23. Highton R (1998) Frequency of hybrids between introduced and native populations of the salamander Plethodon jordani in their first generation of sympatry. Herpetologica 54:143–153Google Scholar
  24. Highton R (1999) Geographic protein variation and speciation in the salamanders of the Plethodon cinereus group with the description of two new species. Herpetologica 55:43–90Google Scholar
  25. Highton R (2004) A new species of woodland salamander of the Plethodon cinereus group from the Blue Ridge Mountains of Virginia. Jeffersoniana 14:1–22Google Scholar
  26. Highton R, Worthington R (1967) A new salamander of the genus Plethodon from Virginia. Copeia 1967:617–626CrossRefGoogle Scholar
  27. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  28. Jaeger RG, Forester DC (1993) Social behavior of plethodontid salamanders. Herpetologica 49:163–175Google Scholar
  29. Johnson JA, Dunn PO, Bouzat JL (2007) Effects of recent population bottlenecks on reconstructing the demographic history of prairie chickens. Mol Ecol 16:2203–2222PubMedCrossRefGoogle Scholar
  30. Kleindorfer S, Chapman TW, Winkler H, Sulloway FJ (2006) Adaptive divergence in contiguous populations of Darwin’s Small Ground Finch (Geospiza fuliginosa). Evol Ecol Res 8:357–372Google Scholar
  31. Knowles L (2001) Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshopprers. Mol Ecol 10:691–701PubMedCrossRefGoogle Scholar
  32. Kozak K, Wiens J (2006) Does niche conservatism promote speciation? A case study in North American salamanders. Evolution 60:2604–2621PubMedGoogle Scholar
  33. Kozak KH, Wiens JJ (2010) Niche conservatism drives elevational diversity patterns in Appalachian salamanders. Am Nat 176:40–54PubMedCrossRefGoogle Scholar
  34. LaSorte F, Jetz W (2010) Projected range contractions of montane biodiversity under global warming. Proc R Soc B Biol Sci 277:3401–4310CrossRefGoogle Scholar
  35. Lawler JJ, Shafer SL, White D, Kareiva P, Maurer EP, Blaustein AR, Bartlein PJ (2009) Projected climate-induced faunal change in the Western Hemisphere. Ecology 90:588–597PubMedCrossRefGoogle Scholar
  36. Lovett JC (1998) Continuous change in Tanzanian moist forest tree communities with elevation. J Trop Ecol 14:719–722CrossRefGoogle Scholar
  37. Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237PubMedCrossRefGoogle Scholar
  38. Mallet J, Beltrán M, Neukirchen W, Linares M (2007) Natural hybridization in heliconiine butterflies: the species boundary as a continuum. BMC Evol Biol 7:28PubMedCrossRefGoogle Scholar
  39. Marsh D, Page RB, Hanlon TJ, Corritone R, Little EE, Seifert DE, Cabe PR (2008) Effects of roads on patterns of genetic differentiation in red-backed salamanders, Plethodon cinereus. Conserv Genet 9:603–613CrossRefGoogle Scholar
  40. McCain CM (2005) Elevational gradients in diversity of small mammals. Ecology 86:366–372CrossRefGoogle Scholar
  41. Milanovich J, Peterman W, Nibbelink N, Maerz J (2010) Project loss of a salamander diversity hotspot as a consequence of project global climate change. PLoS ONE 5:e12189PubMedCrossRefGoogle Scholar
  42. Moritz C, Patton JL, Conroy CJ, Parra JL, White GC et al (2008) Impact of a century of climate change on small-mammal communities in Yosemite National Park, USA. Science 322:261–264PubMedCrossRefGoogle Scholar
  43. Mueller R (2006) Evolutionary rates, divergence dates, and the performance of mitochondrial genes in Bayesian phylogenetic analysis. Syst Biol 55:289–300PubMedCrossRefGoogle Scholar
  44. Myers N, Mittermeier R, Mittermeier C, Fonseca G, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858PubMedCrossRefGoogle Scholar
  45. Pauley T (2007) Revised notes on the range of the Cheat Mountain Salamander, Plethodon nettingi. Proc W Va Acad Sci 79:16–21Google Scholar
  46. Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, WashingtonGoogle Scholar
  47. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256PubMedCrossRefGoogle Scholar
  48. Rhymer J, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109CrossRefGoogle Scholar
  49. Rissler LJ, Smith WH (2010) Mapping amphibian contact zones and phylogeographic break hotspots across the United States. Mol Ecol 19:5404–5416PubMedCrossRefGoogle Scholar
  50. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  51. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  52. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedGoogle Scholar
  53. Smith MA, Poyarkov NA, Hebert PDN (2008) CO1 DNA barcoding amphibians: take the chance, meet the challenge. Mol Ecol Resour 8:235–246PubMedCrossRefGoogle Scholar
  54. Steele C, Carstens BC, Storfer A, Sullivan J (2005) Testing hypotheses of speciation timing in Dicamptodon copei and Dicamptodon aterrimus (Caudata: Dicamptodontidae). Mol Phylogenet Evol 36:90–100PubMedCrossRefGoogle Scholar
  55. Szymura JM, Uzzell T, Spolsky C (2000) Mitochondrial DNA variation in the hybridizing fire-bellied toads, Bombina bombina and B. variegata. Mol Ecol 9:891–899PubMedCrossRefGoogle Scholar
  56. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  57. Terborgh J (1977) Bird species diversity on an Andean elevational gradient. Ecology 58:1007–1019CrossRefGoogle Scholar
  58. United States Forest Service (2011) George Washington National Forest plan revision. http://www.fs.fed.us/. Accessed 11 November 2011
  59. Weisrock D, Kozak H, Larson A (2005) Phylogeographic analysis of mitochondrial gene flow and introgression in the salamander, Plethodon shermani. Mol Ecol 14:1457–1472PubMedCrossRefGoogle Scholar
  60. Wiens J, Engstrom T, Chippindale P (2006) Rapid diversification, incomplete isolation, and the “speciation clock” in North American Salamanders (genus Plethodon): testing the hybrid swarm hypothesis of rapid radiation. Evolution 60:2585–2603PubMedGoogle Scholar
  61. Wilson R, Gutiérrez D, Gutiérrez J, Monserrat V (2007) An elevational shift in butterfly species richness and composition accompanying recent climate change. Glob Change Biol 3:1873–1887CrossRefGoogle Scholar
  62. Xu T, Abbot R, Milne R, Mao K, Du F, Wu G, Ciren Z, Miehe G, Liu J (2010) Phylogeography and allopatric divergence of cypress species (Cupressus L.) in the Qinghai-Tibetan Plateau and adjacent regions. BMC Evol Biol 10:194PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Claire S. O. Bayer
    • 1
  • Andrew M. Sackman
    • 1
  • Kelly Bezold
    • 1
  • Paul R. Cabe
    • 1
  • David M. Marsh
    • 1
    Email author
  1. 1.Department of BiologyWashington and Lee UniversityLexingtonUSA

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