Conservation Genetics

, Volume 15, Issue 1, pp 61–73 | Cite as

Population genetics of Blanding’s turtle (Emys blandingii) in the midwestern United States

  • Arun Sethuraman
  • Suzanne E. McGaugh
  • Morgan L. Becker
  • Christopher H. Chandler
  • James L. Christiansen
  • Sue Hayden
  • Andrea LeClere
  • Jennifer Monson-Miller
  • Erin M. Myers
  • Ryan T. Paitz
  • Jeanine M. Refsnider
  • Terry J. VanDeWalle
  • Fredric J. Janzen
Research Article


Blanding’s turtle (Emys blandingii) has declined substantially in North America due to anthropogenic activities, leaving populations smaller and increasingly fragmented spatially. We sampled 212 turtles to evaluate variation at eight microsatellite loci within and among 18 populations of E. blandingii across its primary range in the midwestern United States (Illinois, Iowa, Minnesota, and Nebraska). All loci and populations were highly polymorphic. Our analyses also detected considerable genetic structure within and among the sampled localities, and revealed ancestral gene flow of E. blandingii in this region north and east from an ancient refugium in the central Great Plains, concordant with post-glacial recolonization timescales. The data further implied unexpected ‘links’ between geographically disparate populations in Nebraska and Illinois. Our study encourages conservation decisions to be mindful of the genetic uniqueness of populations of E. blandingii across its primary range.


North American phylogeography Population genetics Gene flow Turtles 

Supplementary material

10592_2013_521_MOESM1_ESM.pdf (751 kb)
Supplementary material (PDF 751 kb)


  1. Alacs EA, Janzen FJ, Scribner KT (2007) Genetic issues in freshwater turtle and tortoise conservation. Chelonian Res Monogr 4:107–123Google Scholar
  2. Amato ML, Brooks RJ, Fu J (2008) A phylogeographic analysis of populations of the wood turtle (Glyptemys insculpta) throughout its range. Mol Ecol 17:570–581PubMedGoogle Scholar
  3. 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 25:316–329PubMedCrossRefGoogle Scholar
  4. Avise JC (2010) Perspective: conservation genetics enters the genomics era. Conserv Genet 11:665–669CrossRefGoogle Scholar
  5. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography—the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522Google Scholar
  6. Beaudry F, deMaynadier PG, Hunter ML Jr (2008) Identifying road mortality threat at multiple spatial scales for semi-aquatic turtles. Biol Conserv 141:2550–2563CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer-Verlag, New YorkCrossRefGoogle Scholar
  8. Byrne M, Yeates DK, Joseph L et al (2008) Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Mol Ecol 17:4398–4417PubMedCrossRefGoogle Scholar
  9. Christiansen JL (1998) Perspectives on Iowa’s declining amphibians and reptiles. J Iowa Acad Sci 105:109–114Google Scholar
  10. Congdon JD, Keinath DA (2006) Blanding’s Turtle (Emydoidea blandingii): a technical conservation assessment. USDA Forest Service, Rocky Mountain Region. Accessed Feb 2013
  11. Congdon JD, Van Loben Sels RC (1993) Relationships of reproductive traits and body-size with attainment of sexual maturity and age in Blanding’s Turtles (Emydoidea blandingii). J Evol Biol 6:547–557CrossRefGoogle Scholar
  12. Congdon JD, Dunham AE, Van Loben Sels RC (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
  13. Congdon JD, Nagle RD, Osentoski MR, Kinney OM, Van Loben Sels RC (2003) Life history and demographic aspects of aging in the long-lived turtle (Emydoidea blandingii). In: Finch CE, Robine J-M, Christen Y (eds) Brain and longevity. Springer, Germany, pp 15–31CrossRefGoogle Scholar
  14. Earl DA, vonHoldt BM (2012) Structure harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  15. Ehlers J, Gibbard P (2008) Extent and chronology of Quaternary glaciation. Episodes 31:211–218Google Scholar
  16. Ernst CH, Lovich JE (2009) Turtles of the United States and Canada, 2nd edn. Johns Hopkins, BaltimoreGoogle Scholar
  17. Ersts PJ (2010) Geographic Distance Matrix Generator (version 1.2.3). American Museum of Natural History, Center for Biodiversity and Conservation. Accessed Feb 2011
  18. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  19. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567PubMedCrossRefGoogle Scholar
  20. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial-DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  21. Fontanella FM, Feldman CR, Siddall ME, Burbrink FT (2008) Phylogeography of Diadophis punctatus: extensive lineage diversity and repeated patterns of historical demography in a trans-continental snake. Mol Phylogenet Evol 46:1049–1070PubMedCrossRefGoogle Scholar
  22. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  23. Fritz U, Schmidt C, Ernst CH (2011) Competing generic concepts for Blanding’s, Pacific and European pond turtles (Emydoidea, Actinemys and Emys)-which is best? Zootaxa 2791:41–53Google Scholar
  24. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  25. Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760PubMedCrossRefGoogle Scholar
  26. Hoffmann M, Hilton-Taylor C, Angulo A et al (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509PubMedCrossRefGoogle Scholar
  27. Holman JA (1995) Pleistocene amphibians and reptiles in North America. Oxford Monographs on Geology and Geophysics No. 32, OxfordGoogle Scholar
  28. Howes BJ, Brown JW, Gibbs HL, Herman TB, Mockford SW, Prior KA, Weatherhead PJ (2009) Directional gene flow patterns in disjunct populations of the black ratsnake (Pantherophis obsoletus) and the Blanding’s turtle (Emydoidea blandingii). Conserv Genet 10:407–417CrossRefGoogle Scholar
  29. Howeth JG, McGaugh SE, Hendrickson DA (2008) Contrasting demographic and genetic estimates of dispersal in the endangered Coahuilan box turtle: a contemporary approach to conservation. Mol Ecol 17:4209–4221PubMedCrossRefGoogle Scholar
  30. Jackson CJ, Kaye JM (1974) The occurrence of Blanding’s turtle, Emydoidea blandingii, in the Late Pleistocene of Mississippi (Testudines: Testudinae). Herpetologica 30:417–419Google Scholar
  31. Janzen FJ, Krenz JG, Haselkorn TS, Brodie ED Jr, Brodie ED III (2002) Molecular phylogeography of common garter snakes (Thamnophis sirtalis) in western North America: implications for regional historical forces. Mol Ecol 11:1739–1751PubMedCrossRefGoogle Scholar
  32. Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA 75:2868–2872PubMedCrossRefGoogle Scholar
  33. King TL, Julian SE (2004) Conservation of microsatellite DNA flanking sequence across 13 emydid genera assayed with novel bog turtle (Glyptemys muhlenbergii) loci. Conserv Genet 5:719–725CrossRefGoogle Scholar
  34. Lee-Yaw JA, Irwin JT, Green DM (2008) Postglacial range expansion from northern refugia by the wood frog, Rana sylvatica. Mol Ecol 17:867–884PubMedCrossRefGoogle Scholar
  35. Lewis P, Zaykin D (2008) GDA v1.1 Accessed Feb 2010
  36. McGuire JM, Scribner KT, Congdon JD (2013) Spatial aspects of movements, mating patterns, and nest distributions influence gene flow among population subunits of Blanding’s turtles (Emydoidea blandingii). Conserv Genet. doi:10.1007/s10592-013-0493-8 Google Scholar
  37. Mickelson DM, Colgan PM (2003) The southern Laurentide Ice Sheet. Develop Quat Sci 1:1–16Google Scholar
  38. Mockford SW, Snyder M, Herman TB (1999) A preliminary examination of genetic variation in a peripheral population of Blanding’s turtle, Emydoidea blandingii. Mol Ecol 8:323–327PubMedCrossRefGoogle Scholar
  39. Mockford SW, McEachern L, Herman TB, Synder 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
  40. Mockford SW, Herman TB, Snyder M, Wright JM (2007) Conservation genetics of Blanding’s turtle and its application in the identification of evolutionarily significant units. Conserv Genet 8:209–219CrossRefGoogle Scholar
  41. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  42. Placyk JS, Burghardt GM Jr, Small RL, King RB, Casper GS, Robinson JW (2007) Post-glacial recolonization of Michigan by the common gartersnake (Thamnophis sirtalis) inferred from mtDNA sequences. Mol Phylogenet Evol 43:452–467PubMedCrossRefGoogle Scholar
  43. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  44. Rambaut A, Drummond AJ (2007) Tracer v1.4. Accessed Feb 2010
  45. Raymond M, Rousset F (1995) GENEPOP (Version-1.2)—population-genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  46. Rhodin AGJ, van Dijk PP (2011) Emydoidea blandingii. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1 Accessed 15 Aug 2012
  47. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  48. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  49. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedGoogle Scholar
  50. Rubin CS, Warner RE, Bouzat JL, Paige KN (2001) Population genetic structure of Blanding’s turtles (Emydoidea blandingii) in an urban landscape. Biol Conserv 99:323–330CrossRefGoogle Scholar
  51. Shaffer HB (2009) Turtles (Testudines). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, Oxford, pp 398–401Google Scholar
  52. Smith PW (1957) An analysis of post-Wisconsin biogeography of the prairie peninsula region based on distributional phenomena among terrestrial vertebrate populations. Ecology 38:205–218CrossRefGoogle Scholar
  53. Sommer RS, Lindqvist C, Persson A, Bringsoe H, Rhodin AGJ, Schneeweiss N, Siroky P, Bachmann L, Fritz U (2009) Unexpected early extinction of the European pond turtle (Emys orbicularis) in Sweden and climatic impact on its Holocene range. Mol Ecol 18:1252–1262PubMedCrossRefGoogle Scholar
  54. Spinks PQ, Shaffer HB (2009) Range-wide molecular analysis of the western pond turtle (Emys marmorata): cryptic variation, isolation by distance, and their conservation implications. Mol Ecol 14:2047–2064PubMedCrossRefGoogle Scholar
  55. 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 57:119–128PubMedGoogle Scholar
  56. Stiff BJ, Hansel AK (2004) Quaternary glaciations in Illinois. In: Ehlers J, Gibbard PL (eds) Quaternary glaciations: extent and chronology 2: Part II North America. Elsevier, Amsterdam, pp 71–82CrossRefGoogle Scholar
  57. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786PubMedCrossRefGoogle Scholar
  58. Sutherland WJ, Aveling R, Bennun L et al (2012) A horizon scan of global conservation issues for 2012. Trends Ecol Evol 27:12–18PubMedCrossRefGoogle Scholar
  59. Ursenbacher S, Carlsson M, Helfer V, Tegelstrom H, Fumagalli L (2006) Phylogeography and Pleistocene refugia of the adder (Vipera berus) as inferred from mitochondrial DNA sequence data. Mol Ecol 15:3425–3437PubMedCrossRefGoogle Scholar
  60. Van Devender TR, King JE (1975) Fossil Blanding’s turtles, Emydoidea blandingii (Holbrook), and the late Pleistocene vegetation of western Missouri. Herpetologica 31:208–212Google Scholar
  61. van Oosterhout C, Weetman D, Hutchinson WF (2006) Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Mol Ecol Notes 6:255–256CrossRefGoogle Scholar
  62. Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513PubMedGoogle Scholar
  63. Weir BS (1996) Genetic data analysis II. Sinauer, SunderlandGoogle Scholar
  64. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  65. 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 14:152–164PubMedCrossRefGoogle Scholar
  66. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedGoogle Scholar
  67. Wooding S, Ward RH (1997) Phylogeography and Pleistocene evolution in the North American black bear. Mol Biol Evol 14:1096–1105PubMedCrossRefGoogle Scholar
  68. You FM, Luo MC, Gu YQ, Lazo GR, Deal K, Dvorak J, Anderson OD (2007) GenoProfiler: batch processing of high-throughput capillary fingerprinting data. Bioinformatics 23:240–242PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Arun Sethuraman
    • 1
  • Suzanne E. McGaugh
    • 2
  • Morgan L. Becker
    • 1
  • Christopher H. Chandler
    • 3
  • James L. Christiansen
    • 4
  • Sue Hayden
    • 5
  • Andrea LeClere
    • 6
  • Jennifer Monson-Miller
    • 7
  • Erin M. Myers
    • 8
  • Ryan T. Paitz
    • 9
  • Jeanine M. Refsnider
    • 10
  • Terry J. VanDeWalle
    • 11
  • Fredric J. Janzen
    • 1
  1. 1.Department of Ecology, Evolution, & Organismal BiologyIowa State UniversityAmesUSA
  2. 2.Department of BiologyDuke UniversityDurhamUSA
  3. 3.Department of Biological SciencesState University of New YorkOswegoUSA
  4. 4.Department of BiologyDrake UniversityDes MoinesUSA
  5. 5.McHenry County Conservation DistrictRichmondUSA
  6. 6.Department of Genetics, Cell Biology, and DevelopmentUniversity of MinnesotaMinneapolisUSA
  7. 7.Program in Law, Health, and the Life SciencesUniversity of MinnesotaMinneapolisUSA
  8. 8.Department of Biology & BiochemistryUniversity of HoustonHoustonUSA
  9. 9.School of Biological SciencesIllinois State UniversityNormalUSA
  10. 10.Department of Environmental Science, Policy, and ManagementUniversity of CaliforniaBerkeleyUSA
  11. 11.Stantec Consulting Services Inc.IndependenceUSA

Personalised recommendations