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Conservation Genetics

, Volume 19, Issue 3, pp 571–585 | Cite as

Conservation genetics of eastern hellbenders Cryptobranchus alleganiensis alleganiensis in the Tennessee Valley

  • Michael FreakeEmail author
  • Eric O’Neill
  • Shem Unger
  • Stephen Spear
  • Eric Routman
Research Article
  • 353 Downloads

Abstract

The eastern hellbender has declined across much of its range and is a candidate for listing under the Endangered Species Act. Some of the most viable remaining populations exist in the Southern Appalachian Region in the Tennessee Valley watershed; however these populations are highly isolated and fragmented, and occupy several physiographic provinces, suggesting they may exhibit significant levels of genetic differentiation. We investigated genetic and phylogeographic relationships among eastern hellbender populations across the Tennessee Valley, using nuclear microsatellite markers and mitochondrial sequence data. Our population genetic analyses of microsatellite data revealed a strong pattern of isolation by stream distance, and 4 genetically distinct populations. These four populations were mainly associated with major watersheds, although middle Tennessee samples were difficult to assign to any particular population. Our phylogeographic analysis of mtDNA resulted in a strongly supported monophyletic ingroup containing nine largely allopatric clades, which also largely corresponded to major watersheds. Our findings suggest that hellbenders from different watersheds in the Tennessee Valley should be recognized as genetically distinct populations, and care should be taken to balance the needs of rescuing declining populations with translocation or headstart programs, while also preserving genetic diversity across the region.

Keywords

Hellbender salamander Genetic structure Phylogeography Conservation Tennessee River 

Notes

Acknowledgements

We thank the many individuals who assisted in conducting fieldwork, including Lee University undergraduate students, D. Hedrick (Chattanooga Zoo), and J. Herrig (USDA National Forest Service). We also thank the following funding sources: Tennessee Wildlife Resource Agency, USDA Forest Service, Appalachian College Association, Lee University, Indiana Department of Natural Resources, University of Tennessee at Chattanooga, Purdue University, Cryptobranchid Interest Group Ron Goellner Fund.

Supplementary material

10592_2017_1033_MOESM1_ESM.pdf (63 kb)
Supplementary material 1 (PDF 62 KB)
10592_2017_1033_MOESM2_ESM.pdf (73 kb)
Supplementary material 2 (PDF 73 KB)

References

  1. Ahlstedt SA, Powell JR, Butler RS, Fagg MT, Hubbs DW, Novak SF, Palmer SR, Johnson PD (2004) Historical and current examination of freshwater mussels (Bivalvia: Margaritiferidae, Unionidae) in the Duck River basin, Tennessee. Tennessee Wildlife Resources Agency, Nashville. Available from https://www.researchgate.net/profile/Jeff_Powell2/publication/260176288_Historical_and_Current_Examination_of_Freshwater_Mussels_Bivalvia_Margaritiferidae_Unionidae_in_the_Duck_River_Basin_Tennessee/links/0a85e52fe3a78b5fd8000000/Historical-and-Current-Examination-of-Freshwater-Mussels-Bivalvia-Margaritiferidae-Unionidae-in-the-Duck-River-Basin-Tennessee.pdf. Accessed 10 June 2017
  2. Bodinof C, Briggler J, Duncan M, Milspaugh J (2011) Historic occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in hellbender Cryptobranchus alleganiensis populations from Missouri. Dis Aquat Org 96:1–7.  https://doi.org/10.3354/dao02380 CrossRefPubMedGoogle Scholar
  3. Bodinof CM, Briggler JT, Junge RE et al (2012) Postrelease movements of captive-reared Ozark hellbenders (Cryptobranchus alleganiensis bishopi). Herpetologica 68:160–173CrossRefGoogle Scholar
  4. Bothner R, Gottlieb JA (1991) A study of the New York state populations of the hellbender, Cryptobranchus alleganiensis alleganiensis (Daudin). Proc Rochester Acad Sci 17:41–54Google Scholar
  5. Bouzat JL, Johnson JA, Toepfer JE et al (2009) Beyond the beneficial effects of translocations as an effective tool for the genetic restoration of isolated populations. Conserv Genet 10:191–201.  https://doi.org/10.1007/s10592-008-9547-8 CrossRefGoogle Scholar
  6. Briggler JT, Ultrup J, Davidson C et al (2007) Hellbender population and habitat viability assessment. Apple Valley, MinnesotaGoogle Scholar
  7. Burgmeier NG, Unger SD, Meyer JL et al (2011a) Health and habitat quality assessment for the eastern hellbender (Cryptobranchus alleganiensis alleganiensis) in Indiana, USA. J Wildl Dis 47:836–848CrossRefPubMedGoogle Scholar
  8. Burgmeier NG, Unger SD, Sutton TM, Williams RN (2011b) Population status of the eastern hellbender (Cryptobranchus alleganiensis alleganiensis) in Indiana. J Herpetol 45:195–201CrossRefGoogle Scholar
  9. Caruso NM, Sears MW, Adams DC, Lips KR (2014) Widespread rapid reductions in body size of adult salamanders in response to climate change. Glob Change Biol 20:1751–1759.  https://doi.org/10.1111/gcb.12550 CrossRefGoogle Scholar
  10. Chhatre VE, Emerson KJ (2017) StrAuto: automation and parallelization of STRUCTURE analysis. BMC Bioinform 18:192.  https://doi.org/10.1186/s12859-017-1593-0 CrossRefGoogle Scholar
  11. Crowhurst RS, Faries KM, Collantes J et al (2011) Genetic relationships of hellbenders in the Ozark highlands of Missouri and conservation implications for the Ozark subspecies (Cryptobranchus alleganiensis bishopi). Conserv Genet 12:637–646.  https://doi.org/10.1007/s10592-010-0170-0 CrossRefGoogle Scholar
  12. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361.  https://doi.org/10.1007/s12686-011-9548-7 CrossRefGoogle Scholar
  13. 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.  https://doi.org/10.1111/j.1365-294X.2005.02553.x CrossRefPubMedGoogle Scholar
  14. Foster RL, McMillan AM, Roblee KJ (2009) Population status of hellbender salamanders (Cryptobranchus alleganiensis) in the Allegheny River drainage of New York State. J Herpetol 43:579–588..  https://doi.org/10.1670/08-156.1 CrossRefGoogle Scholar
  15. Freake MJ, DePerno CS (2017) Importance of demographic surveys and public lands for the conservation of eastern hellbenders Cryptobranchus alleganiensis alleganiensis in southeast USA. PLoS ONE 12:e0179153.  https://doi.org/10.1371/journal.pone.0179153 CrossRefPubMedPubMedCentralGoogle Scholar
  16. GADNR (2015) Georgia State Wiuldlife Action Plan. Available from http://georgiawildlife.com/sites/default/files/wrd/pdf/swap/SWAP2015MainReport_92015.pdf. Accessed 16 June 2017
  17. Gilpin S, Soule M (1986) Minimum viable populations: processes of species extinction. In: Soule ME, Sinauer (eds) Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland, pp 19–34Google Scholar
  18. Hecht-Kardasz KA, Nickerson MA, Freake M, Colclough P (2012) Population structure of the Hellbender (Cryptobranchus alleganiensis) in a Great Smoky Mountains stream. Bull Fla Mus Nat Hist 51:227–241Google Scholar
  19. Hedrick PW (2001) Conservation genetics: where are we now? Trends Ecol Evol 16:629–636CrossRefGoogle Scholar
  20. Hendry AP, Lohmann LG, Conti E et al (2010) Evolutionary biology in biodiversity science, conservation, and policy: a call to action. Evolution 64(5):1517–1528.  https://doi.org/10.1111/j.1558-5646.2010.00947.x PubMedCrossRefGoogle Scholar
  21. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332.  https://doi.org/10.1111/j.1755-0998.2009.02591.x CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hudson RR, Coyne JA (2002) Mathematical consequences of the genealogical species concept. Evolution 56:1557–1565.  https://doi.org/10.1111/j.0014-3820.2002.tb01467.x CrossRefPubMedGoogle Scholar
  23. Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649.  https://doi.org/10.1093/bioinformatics/bts199 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701.  https://doi.org/10.1093/molbev/mss020 CrossRefPubMedGoogle Scholar
  25. Lankau R, Jørgensen PS, Harris DJ, Sih A (2011) Incorporating evolutionary principles into environmental management and policy: evolutionary environmental management. Evol Appl 4:315–325.  https://doi.org/10.1111/j.1752-4571.2010.00171.x CrossRefPubMedPubMedCentralGoogle Scholar
  26. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452.  https://doi.org/10.1093/bioinformatics/btp187 CrossRefPubMedGoogle Scholar
  27. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  28. Martel A, Blooi M, Adriaensen C et al (2014) Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science 346:630–631CrossRefPubMedPubMedCentralGoogle Scholar
  29. Mast MA, Turk JT (1999) Environmental characteristics and water quality of hydrologic benchmark network stations in the eastern United States, 1963–1995. U.S. G.P.O.; Free on application to the U.S. Geological Survey, Information Services, Washington, DC, DenverGoogle Scholar
  30. Mayasich J, Grandmaison D, Phillips C (2003) Eastern hellbender status assessment report. Nat Resour Res Inst Tech Rep 9:1–41Google Scholar
  31. Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures: invited technical review. Mol Ecol Resour 11:5–18.  https://doi.org/10.1111/j.1755-0998.2010.02927.x CrossRefPubMedGoogle Scholar
  32. Meirmans PG, Van Tienderen PH (2004) genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794.  https://doi.org/10.1111/j.1471-8286.2004.00770.x CrossRefGoogle Scholar
  33. Miller BT, Miller JL (2005) Prevalence of physical abnormalities in eastern Hellbender (Cryptobranchus alleganiensis alleganiensis) populations of middle Tennessee. Southeast Nat 4:513–520CrossRefGoogle Scholar
  34. NCWRC (2015) North Carolina State Wildlife Action Plan. Available from: http://www.ncwildlife.org/Portals/0/Conserving/documents/2015WildlifeActionPlan/NC-WAP-2015-All-Documents.pdf. Accessed 16 June 2017
  35. Nickerson MA, Mays CE (1973a) The hellbenders: North American “giant salamanders. Milwaukee Public Mus Special Publ Biol Geol 1:1–106Google Scholar
  36. Nickerson MA, Mays CE (1973b) A study of the Ozark Hellbender Cryptobranchus alleganiensis bishopi. Ecology 54:1164..  https://doi.org/10.2307/1935586 CrossRefGoogle Scholar
  37. Nickerson MA, Krysko KL, Owen RD (2002) Ecological status of the hellbender (Cryptobranchus alleganiensis) and the mudpuppy (Necturus maculosus) salamanders in the Great Smoky Mountains National Park. J N C Acad Sci 118:27–34Google Scholar
  38. Peterson CL, Wilkinson RF Jr, Topping MS, Metter DE (1983) Age and growth of the Ozark hellbender (Cryptobranchus alleganiensis bishopi). Copeia 1:225–231CrossRefGoogle Scholar
  39. Peterson CL, Metter DE, Miller BT et al (1988) Demography of the hellbender Cryptobranchus alleganiensis in the Ozarks. Am Midl Nat 119:291–303CrossRefGoogle Scholar
  40. Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, WashingtonGoogle Scholar
  41. Phillips CA (1994) Geographic distribution of mitochondrial DNA variants and the historical biogeography of the spotted salamander, Ambystoma maculatum. Evolution 48:597–607.  https://doi.org/10.2307/2410472 CrossRefPubMedGoogle Scholar
  42. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  43. Pugh MW, Groves JD, Williams LA, Gangloff MM (2013) A previously undocumented locality of eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) in the Elk River, Carter County, TN. Southeast Nat 12:137–142.  https://doi.org/10.1656/058.012.0111 CrossRefGoogle Scholar
  44. Pugh MW, Hutchins M, Madritch M et al (2015) Land-use and local physical and chemical habitat parameters predict site occupancy by hellbender salamanders. Hydrobiologia.  https://doi.org/10.1007/s10750-015-2570-0 CrossRefGoogle Scholar
  45. Quinn SA, Gibbs JP, Hall MH, Petokas PJ (2013) Multiscale factors influencing distribution of the eastern hellbender salamander (Cryptobranchus alleganiensis alleganiensis) in the northern segment of its range. J Herpetol 47:78–84CrossRefGoogle Scholar
  46. Rissler L, Apodaca J (2007) Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the black salamander (Aneides flavipunctatus). Syst Biol 56:924–942.  https://doi.org/10.1080/10635150701703063 CrossRefPubMedGoogle Scholar
  47. Ronquist F, Teslenko M, van der Mark P et al (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542.  https://doi.org/10.1093/sysbio/sys029 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedPubMedCentralGoogle Scholar
  49. Routman E, Wu R, Templeton AR (1994) Parsimony, molecular evolution, and biogeography: the case of the North American giant salamander. Evolution 48:1799–1809.  https://doi.org/10.2307/2410509 CrossRefPubMedGoogle Scholar
  50. Sabatino SJ, Routman EJ (2009) Phylogeography and conservation genetics of the hellbender salamander (Cryptobranchus alleganiensis). Conserv Genet 10:1235–1246.  https://doi.org/10.1007/s10592-008-9655-5 CrossRefGoogle Scholar
  51. Shaffer ML, Stein BA (2000) Safeguarding our precious heritage. Precious heritage: The status of biodiversity in the United States. Oxford University Press, New York, pp 301–321Google Scholar
  52. Smith J, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23(1):23–35.  https://doi.org/10.1017/S0016672300014634 CrossRefPubMedGoogle Scholar
  53. Templeton AR, Shaw K, Routman E, Davis SK (1990) The genetic consequences of habitat fragmentation. Ann Mo Bot Gard 77:13–27.  https://doi.org/10.2307/2399621 CrossRefGoogle Scholar
  54. Tonione M, Johnson JR, Routman EJ (2011) Microsatellite analysis supports mitochondrial phylogeography of the hellbender (Cryptobranchus alleganiensis). Genetica 139:209–219.  https://doi.org/10.1007/s10709-010-9538-9 CrossRefPubMedGoogle Scholar
  55. Trauth SE, Wilhide JD, Daniel P (1992) Status of the Ozark hellbender Cryptobranchus bishopi (Urodela: Cryptobranchidae), in the Spring River, Fulton County, Arkansas. Proc Ark Acad Sci 46:83–86Google Scholar
  56. TWRA (2015) Tennessee State Wildlife Action Plan. Available from http://www.tnswap.com/swap.cfm. Accessed 16 June 2017
  57. Unger SD, Fike JA, Sutton T et al (2010) Isolation and development of 12 polymorphic tetranucleotide microsatellite markers for the eastern hellbender (Cryptobranchus alleganiensis alleganiensis). Conserv Genet Resour 2:89–91.  https://doi.org/10.1007/s12686-009-9170-0 CrossRefGoogle Scholar
  58. Unger SD, Rhodes OE, Sutton TM, Williams RN (2013) Population genetics of the eastern hellbender (Cryptobranchus alleganiensis alleganiensis) across multiple spatial scales. PLoS ONE 8:e74180.  https://doi.org/10.1371/journal.pone.0074180 CrossRefPubMedPubMedCentralGoogle Scholar
  59. United States Fish and Wildlife Service (2011a) Endangered and threatened wildlife and plants; endangered status for the ozark hellbender salamander. 50 CFR Part 23. Fed Regist 76:61956‒61978Google Scholar
  60. United States Fish and Wildlife Service (2011b) Inclusion of the hellbender, including the eastern hellbender and the ozark hellbender, in appendix III of the convention on international trade in endangered species of wild fauna and flora (CITES). 50 CFR Part 23. Fed Regist 76:61978–61985Google Scholar
  61. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538.  https://doi.org/10.1111/j.1471-8286.2004.00684.x CrossRefGoogle Scholar
  62. Weeks AR, Sgro CM, Young AG et al (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective: translocations in changing environments. Evol Appl 4:709–725.  https://doi.org/10.1111/j.1752-4571.2011.00192.x CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wheeler BA, Prosen E, Mathis A, Wilkinson RF (2003) Population declines of a long-lived salamander: a 20+-year study of hellbenders, Cryptobranchus alleganiensis. Biol Conserv 109:151–156CrossRefGoogle Scholar
  64. Williams RD, Gates JE, Hocutt CH, Taylor GJ (1981) The hellbender: a nongame species in need of management. Wildl Soc Bull 9:94–100Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Natural Sciences and MathematicsLee UniversityClevelandUSA
  2. 2.Department of Biology, Geology and Environmental ScienceUniversity of Tennessee at ChattanoogaChattanoogaUSA
  3. 3.Department of BiologyWingate UniversityWingateUSA
  4. 4.The WildsCumberlandUSA
  5. 5.Department of BiologySan Francisco State UniversitySan FranciscoUSA

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