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Range-wide phylogeography of Blanding’s Turtle [Emys (= Emydoidea) blandingii]

  • Mark A. JordanEmail author
  • Victoria Mumaw
  • Natalie Millspaw
  • Stephen W. Mockford
  • Fredric J. Janzen
Research Article
  • 47 Downloads

Abstract

Documentation of intraspecific genetic lineages and their evolutionary history can provide insight for current and future conservation and management actions. The Blanding’s Turtle, Emys (= Emydoidea) blandingii, is a long-lived species with a relatively narrow latitudinal distribution centered around the Great Lakes, but extending from Nebraska to Nova Scotia. It is listed as endangered or threatened throughout most of its range mainly due to habitat loss. Microsatellite loci have been predominantly used to test and generate hypotheses concerning the number of evolutionarily significant units and the history of lineage diversification in this species. Here we describe haplotypes from two mitochondrial and three nuclear loci generated from 32 localities across the species’ range to provide an additional perspective on existing patterns. Haplotype and nucleotide diversity were low in both sets of loci, with mitochondrial polymorphism comparable to the lowest found in any North American freshwater turtle. Spatial analyses of population differentiation supported the presence of two groups with a boundary in eastern Ontario that is roughly associated with the Appalachian Mountains as proposed by Mockford et al. (Conserv Gen 8:209–219, 2007). We suggest that the low diversity in these loci is likely related to periodic range contractions and expansions associated with glacial cycles and that the two groups recovered result from a deeper history of diversification. Our results are broadly consistent with previously identified range-wide structure and help to reconcile population structure found at smaller spatial scales, outcomes that will better inform conservation decision making for the species.

Keywords

Mitochondrial loci Nuclear loci Pleistocene glaciation Lineage diversification Low genetic diversity 

Notes

Acknowledgements

This research was supported by the Indiana Academy of Science and the IPFW Honors Program. We thank Christina Davy, Mike Finkler, Rusty Gonser, Dave Mifsud, Brendan Reid, and Sasha Tetzlaff for sharing samples with us. The Field Museum and the Royal Ontario Museum were helpful in providing additional samples. We also appreciate the insights shared by Phil Spinks on choosing polymorphic nuclear loci.

Supplementary material

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References

  1. Amato ML, Brooks RJ, Fu J (2008) A phylogeographic analysis of populations of the wood turtle (Glyptemys insculpta) throughout its range. Mol Ecol 17:570–581Google Scholar
  2. Anthonysamy WJB, Dreslik MJ, Douglas MR, Thompson D, Klut GM, Kuhns AR, Mauger D, Kirk D, Glowacki GA, Douglas ME, Phillips CA (2017) Population genetic evaluations within a co-distributed taxonomic group: a multi-species approach to conservation planning. Anim Conserv 21:137–147CrossRefGoogle Scholar
  3. Avise JC, Bowen BW, Lamb T, Meylan AB, Bermingham E (1992) Mitochondrial DNA evolution at a turtle’s pace: evidence for low genetic variability and reduced microevolutionary rate in the Testudines. Mol Biol Evol 9:457–473Google Scholar
  4. Bleakney JS (1958a) A zoogeographical study of the amphibians and reptiles of eastern Canada. Natl Mus Can Bull 155:1–119Google Scholar
  5. Bleakney S (1958b) Postglacial dispersal of the turtle Chrysemys picta. Herpetologica 14:101–104Google Scholar
  6. Bryant D, Moulton V (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265CrossRefGoogle Scholar
  7. Congdon JD, Dunham AE, van Loben Sels R (1993) Delayed sexual maturity and demographics of Blanding’s Turtles (Emydoidea blandingii): implications for conservation and management of long-lived organisms. Conserv Biol 7:826–833CrossRefGoogle Scholar
  8. Congdon JD, Graham TE, Herman TB, Lang JW, Pappas MJ, Brecke BJ (2008) Emydoidea blandingii (Holbrook 1838) - Blanding’s Turtle. In: Rhodin AGJ, Pritchard PCH, van Dijk PP, Saumure RA, Buhlmann KA, Iverson JB (eds) Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group Chelonian Research Monographs No 5. p.^pp. 015.011–015.012Google Scholar
  9. Davy CM, Bernardo PH, Murphy RW (2014) A Bayesian approach to conservation genetics of Blanding’s turtle (Emys blandingii) in Ontario. Canada Conserv Gen 15:319–330CrossRefGoogle Scholar
  10. Dellicour S, Mardulyn P (2014) SPADS 1.0: a toolbox to perform spatial analyses on DNA sequence data sets. Mol Ecol Res 14:647–651CrossRefGoogle Scholar
  11. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581CrossRefGoogle Scholar
  12. Epps CW, Keyghobadi N (2015) Landscape genetics in a changing world: disentangling historical and contemporary influences and inferring change. Mol Ecol 24:6021–6040CrossRefGoogle Scholar
  13. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: applications to human mitochonridal DNA. Genetics 131:479–491Google Scholar
  14. Fritz U, Guicking D, Kami H, Arakelyan M, Auer M, Ayaz D, Fernández CA, Bakiev AG, Celani A, Džukić G (2007) Mitochondrial phylogeography of European pond turtles (Emys orbicularis, Emys trinacris)–an update. Amphib-Reptilia 28:418–426CrossRefGoogle Scholar
  15. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925Google Scholar
  16. Garrick RC, Sunnucks P, Dyer RJ (2010) Nuclear gene phylogeography using PHASE: dealing with unresolved genotypes, lost alleles, and systematic bias in parameter estimation. BMC Evol Biol 10:118CrossRefGoogle Scholar
  17. Hardy OJ, Vekemans X (2002) SPAGeDI: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  18. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913CrossRefGoogle Scholar
  19. Holman JA (1995) Pleistocene amphibians and reptiles in North America. Oxford University Press, New YorkGoogle Scholar
  20. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267CrossRefGoogle Scholar
  21. Joly S, Bruneau A (2006) Incorporating allelic variation for reconstructing the evolutionary history of organisms from multiple genes: an example from Rosa in North America. Syst Biol 55:623–636CrossRefGoogle Scholar
  22. Karl SA, Toonen R, Grant W, Bowen B (2012) Common misconceptions in molecular ecology: echoes of the modern synthesis. Mol Ecol 21:4171–4189CrossRefGoogle Scholar
  23. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefGoogle Scholar
  24. Kuo C-H, Janzen FJ (2004) Genetic effects of a persistent bottleneck on a natural population of ornate box turtles (Terrapene ornata). Conserv Gen 5:425–437CrossRefGoogle Scholar
  25. Lenk P, Fritz U, Joger U, Wink M (1999) Mitochondrial phylogeography of the European pond turtle, Emys orbicularis (Linnaeus 1758). Mol Ecol 8:1911–1922CrossRefGoogle Scholar
  26. Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190CrossRefGoogle Scholar
  27. McCluskey EM, Mockford SW, Sands K, Herman TB, Johnson G, Gonser RA (2016) Population genetic structure of Blanding’s Turtles (Emydoidea blandingii) in New York. J Herpetol 50:70–76CrossRefGoogle Scholar
  28. Miller MP (2005) Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96:722–724CrossRefGoogle Scholar
  29. Miller MP, Bellinger MR, Forsman ED, Haig SM (2006) Effects of historical climate change, habitat connectivity, and vicariance on genetic structure and diversity across the range of the red tree vole (Phenacomys longicaudus) in the Pacific Northwestern United States. Mol Ecol 15:145–159CrossRefGoogle Scholar
  30. Mockford S, McEachern L, Herman T, Snyder M, Wright JM (2005) Population genetic structure of a disjunct population of Blanding’s turtle (Emydoidea blandingii) in Nova Scotia, Canada. Biol Conserv 123:373–380CrossRefGoogle Scholar
  31. Mockford SW, Herman TB, Snyder M, Wright JM (2007) Conservation genetics of Blanding’s turtle and its appliction in the identification of evolutionary significant units. Conserv Gen 8:209–219CrossRefGoogle Scholar
  32. Parmley D (1992) Turtles from the late Hemphillian (latest Miocene) of Knox County, Nebraska. Tex J Sci 44:339–348Google Scholar
  33. Parris DC, Daeschler E (1995) Pleistocene turtles of Port Kennedy cave (late Irvingtonian), Montgomery County, Pennsylvania. J Paleontol 69:563–568CrossRefGoogle Scholar
  34. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  35. Ramírez-Soriano A, Ramos-Onsins SE, Rozas J, Calafell F, Navarro A (2008) Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics 179:555–567CrossRefGoogle Scholar
  36. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100CrossRefGoogle Scholar
  37. Reid BN, Mladenoff DJ, Peery MZ (2017) Genetic effects of landscape, habitat preference and demography on three co-occurring turtle species. Mol Ecol 26:781–798CrossRefGoogle Scholar
  38. Reid BN, Kass JM, Wollney S, Jensen EL, Russello MA, Viola EM, Pantophlet J, Iverson JB, Peery MZ, Raxworthy CJ, Naro-Maciel E (2018) Disentangling the genetic effects of refugial isolation and range expansion in a trans-continentally distributed species. Heredity.  https://doi.org/10.1038/s41437-018-0135-5 Google Scholar
  39. Rödder D, Lawing AM, Flecks M, Ahmadzadeh F, Dambach J, Engler JO, Habel JC, Hartmann T, Hörnes D, Ihlow F (2013) Evaluating the significance of paleophylogeographic species distribution models in reconstructing Quaternary range-shifts of Nearctic chelonians. PLoS ONE, 8:e72855CrossRefGoogle Scholar
  40. Rosenbaum PA, Robertson JM, Zamudio KR (2007) Unexpectedly low genetic divergences among populations of the threatened bog turtle (Glyptemys muhlenbergii). Conserv Gen 8:331–342CrossRefGoogle Scholar
  41. Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302CrossRefGoogle Scholar
  42. Schmidt KP (1938) Herpetological evidence for the postglacial eastward expansion of the steppe in North America. Ecology 19:396–407CrossRefGoogle Scholar
  43. Sethuraman A, McGaugh SE, Becker ML, Chandler CH, Christiansen JL, Hayden S, LeClere A, Monson-Miller J, Myers EM, Paitz RT, Refsnider JM, VanDeWalle TJ, Janzen FJ (2014) Population genetics of Blanding’s turtle (Emys blandingii) in the midwestern United States. Conserv Gen 15:61–73CrossRefGoogle Scholar
  44. Shaffer H, Minx P, Warren D, Shedlock A, Thomson R, Valenzuela N, Abramyan J, Amemiya C, Badenhorst D, Biggar K, Borchert G, Botka C, Bowden R, Braun E, Bronikowski A, Bruneau B, Buck L, Capel B, Castoe T, Czerwinski M, Delehaunty K, Edwards S, Fronick C, Fujita M, Fulton L, Graves T, Green R, Haerty W, Hariharan R, Hernandez O, Hillier L, Holloway A, Janes D, Janzen F, Kandoth C, Kong L, de Koning A, Li Y, Literman R, McGaugh S, Mork L, O’Laughlin M, Paitz R, Pollock D, Ponting C, Radhakrishnan S, Raney B, Richman J, St John J, Schwartz T, Sethuraman A, Spinks P, Storey K, Thane N, Vinar T, Zimmerman L, Warren W, Mardis E, Wilson R (2013) The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol 14:R28CrossRefGoogle Scholar
  45. Smith PW (1957) An analysis of post-Wisconin biogeography of the prairie peninsula region based on distributional phenomena among terrestrial vertebrate populations. Ecology 38:205–218CrossRefGoogle Scholar
  46. Spinks PQ, Shaffer HB (2005) Range-wide molecular analysis of the western pond turtle (Emys marmorata): cryptic variation, isolation by distance, and their conservation implications. Mol Ecol 14:2047–2064CrossRefGoogle Scholar
  47. Spinks PQ, Shaffer HB (2009) Conflicting mitochondrial and nuclear phylogenies for the widely disjunct Emys (Testudines: Emydidae) species complex, and what they tell us about biogeography and hybridization. Syst Biol 58:1–20CrossRefGoogle Scholar
  48. Spinks PQ, Thomson RC, Shaffer HB (2010) Nuclear gene phylogeography reveals the historical legacy of an ancient inland sea on lineages of the western pond turtle, Emys marmorata in California. Mol Ecol 19:542–556CrossRefGoogle Scholar
  49. Spinks PQ, Thomson RC, Shaffer HB (2014) The advantages of going large: genome-wide SNPs clarify the complex population history and systematics of the threatened western pond turtle. Mol Ecol 23:2228–2241CrossRefGoogle Scholar
  50. Spinks PQ, Thomson RC, McCartney-Melstad E, Shaffer HB (2016) Phylogeny and temporal diversification of the New World pond turtles (Emydidae). Mol Phylogenet Evol 103:85–97CrossRefGoogle Scholar
  51. Starkey DE, Shaffer HB, Burke RL, Forstner MRJ, Iverson JB, Janzen FJ, Rhodin AGJ, Ultsch GR (2003) Molecular systematics, phylogeography, and the effects of Pleistocene glaciation in the painted turtle (Chrysemys picta) complex. Evolution 57:119–128CrossRefGoogle Scholar
  52. Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169CrossRefGoogle Scholar
  53. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989CrossRefGoogle Scholar
  54. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595Google Scholar
  55. Team QD (2009) QGIS Geographic Information System. Open Source Geospatial Foundation, ChicagoGoogle Scholar
  56. Toews DP, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930CrossRefGoogle Scholar
  57. Vamberger M, Stuckas H, Sacco F, D’Angelo S, Arculeo M, Cheylan M, Corti C, Lo Valvo M, Marrone F, Wink M (2015) Differences in gene flow in a twofold secondary contact zone of pond turtles in southern Italy (Testudines: Emydidae: Emys orbicularis galloitalica. E. o. hellenica, E. trinacris). Zool Scr 44:233–249CrossRefGoogle Scholar
  58. van Dijk PP, Harding J (2011) Glyptemys insculpta (errata version published in 2016), The IUCN Red List of Threatened Species. https://dx.doi.org/10.2305/IUCN.UK.2011-1.RLTS.T4965A11102820.en. Accessed 18 April 2018
  59. Velo-Antón G, García-París M, Rivera AC (2008) Patterns of nuclear and mitochondrial DNA variation in Iberian populations of Emys orbicularis (Emydidae): conservation implications. Conserv Gen 9:1263–1274CrossRefGoogle Scholar
  60. Wang IJ (2010) Recognizing the temporal distinctions between landscape genetics and phylogeography. Mol Ecol 19:2605–2608CrossRefGoogle Scholar
  61. Weeks AR, Sgro CM, Young AG, Frankham R, Mitchell NJ, Miller KA, Byrne M, Coates DJ, Eldridge MD, Sunnucks P (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evol Appl 4:709–725CrossRefGoogle Scholar
  62. Weisrock DW, Janzen FJ (2000) Comparative molecular phylogeography of North American softshell turtles (Apalone): implications for regional and wide-scale historical evolutionary forces. Mol Phylogenet Evol 14:152–164CrossRefGoogle Scholar
  63. Willoughby JR, Sundaram M, Lewis TL, Swanson BJ (2013) Population decline in a long-lived species: the wood turtle in Michigan. Herpetologica 69:186–198CrossRefGoogle Scholar
  64. Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of BiologyPurdue University Fort WayneFort WayneUSA
  2. 2.Biology DepartmentAcadia UniversityWolfvilleCanada
  3. 3.Department of Ecology, Evolution and Organismal BiologyIowa State UniversityAmesUSA

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