Skip to main content

Advertisement

SpringerLink
Log in

Unexpectedly low genetic divergences among populations of the threatened bog turtle (Glyptemys muhlenbergii)

  • Original paper
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

We used mitochondrial DNA sequence comparisons to assess range-wide population structure and historical patterns of differentiation among populations of the bog turtle (Glyptemys muhlenbergii). This species is one of North America’s smallest and most endangered pond turtles, and is currently found in three largely disjunct groups of populations: in the southern U.S., in the northeast, and in the Finger Lakes and Lake Ontario Plains region of western and central New York State. All the New York sites and most of the northeastern sites were glaciated during the Pleistocene. We surveyed 2793 bases pairs of mitochondrial DNA spanning three genes (cytb, nd4, and d-loop) in 41 individuals from 21 populations throughout most of the bog turtle’s distribution. We found surprisingly low levels of divergence among populations, even in southern populations that have been hypothesized as refugia during times of climate change. Our data suggest populations of bog turtle’s suffered a bottleneck, followed by a rapid post-Pleistocene expansion into northern segments of the species’ range. We discuss historical changes in habitat availability and climate that may have influenced the historical deployment of lineages in this species, and possible life history traits and habitat dynamics that might also contribute to the overall low genetic diversity across its range.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alexandrino J, Arntzen JW, Ferrand N (2002) Nested clade analysis and the genetic evidence for population expansion in the phylogeography of the golden-striped salamander, Chioglossa lusitanica (Amphibia: Urodela). Heredity 88:66–74

    Article  PubMed  CAS  Google Scholar 

  • Amato GD, Behler JL, Tryon BW, Herman DW (1997) Molecular variation in the bog turtle, Clemmys muhlenbergii. In: Proceedings of the International Conference of Conservation, Restoration and Management of Tortoises and Turtles. New York Turtle and Tortoise Society, New York, pp 259–262

  • Arévalo E, Davis SK, Sites JW Jr (1994) Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in central Mexico. Syst Biol 43:387–418

    Article  Google Scholar 

  • Austin JD, Lougheed SC, Boag PT (2004) Controlling for the effects of history and nonequilibrium conditions in gene flow estimates in northern bullfrog (Rana catesbeiana) populations. Genetics 168:1491–1506

    Article  PubMed  CAS  Google Scholar 

  • Austin JD, Lougheed SC, Neidrauer L, Check 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

    Article  PubMed  CAS  Google Scholar 

  • 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. Ann Rev Ecol Syst 18:489–522

    Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Avise JC, Bowen BW, Lamb T, Meylan AB, Bermingham E (1992) Mitochondria DNA evolution at a turtle’s pace: evidence for low genetic variability and reduced microevolutionary rate in the Testudines. Mol Biol Evol 9:457–463

    PubMed  CAS  Google Scholar 

  • Barrett SCH, Kohn JR (1991) Genetic and evolutionary consequences of small population size in plants: implications for conservation. In: Falk DA, Holsinger KE (eds), Genetics and conservation of rare plants. Oxford University Press, Oxford, pp 3–30

  • Bernatchez L, Dodson JJ (1991) Phylogeographic structure in mitochondrial DNA of the Lake Whitefish (Coregonus clupeaformis) and its relation to Pleistocene glaciations. Evolution 45:1016–1035

    Article  Google Scholar 

  • Bernatchez L, Wilson C (1998) Comparative phylogeography of Nearctic and Palearctic fishes. Mol Ecol 7:431–452

    Article  Google Scholar 

  • Breisch AR (1988). New York state recovery plan—bog turtle (Clemmys muhlenbergii). Endangered Species Unit, New York State Department of Environmental Conservation, Albany, New York

    Google Scholar 

  • Bromham L (2002) Molecular clocks in reptiles: life history influences rate of molecular evolution. Mol Biol Evol 19:302–309

    PubMed  CAS  Google Scholar 

  • Carter SL, Haas CA, Mitchell JC (1999) Home range and habitat selection of bog turtles in southwestern Virginia. J Wildlife Manage 63:853–860

    Google Scholar 

  • Carter SL, Haas CA, Mitchell JC (2000) Movement and activity of bog turtles (Clemmys muhlenbergii) in southwestern Virginia. J Herpetol 34:75–80

    Article  Google Scholar 

  • Chase JD, Dixon KR, Gates JE, Jacobs D, Taylor G (1989) Habitat characteristics, population size, and home range of the bog turtle, Clemmys muhlenbergii, in Maryland. J Herpetol 23:356–362

    Article  Google Scholar 

  • Clark AM, Bowen BW, Branch LC (1999) Effects of natural habitat fragmentation on an endemic scrub lizard (Sceloporus woodi): an historical perspective based on mitochondrial DNA gene genealogy. Mol Ecol 8:1093–1104

    Article  PubMed  CAS  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1658–1660

    Article  Google Scholar 

  • Conant R, Collins JT (1998) A field guide to reptiles and amphibians of Eastern and central North America. Houghton Mifflin, Boston

    Google Scholar 

  • Ernst CH (1977) Biological notes on the bog turtle, Clemmys muhlenbergii. Herpetologica 33:241–246

    Google Scholar 

  • Ernst CH, Lovich JE, Barbour RW (1994) Turtles of the United States and Canada. Smithsonian Institution Press, Washington DC

    Google Scholar 

  • Feldman CR, Parham JF (2002) Molecular phylogenetics of emydine turtles: taxonomic revision and the evolution of shell kinesis. Mol Phyl Evol 22:388–398

    Article  CAS  Google Scholar 

  • Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Galtier N, Depaulis F, Barton NH (2000) Detecting bottlenecks and selective sweeps from DNA sequence polymorphism. Genetics 155:981–987

    PubMed  CAS  Google Scholar 

  • Gatesy J, Desalle R, Wheeler W (1993) Alignment-ambiguous nucleotide sites and the exclusion of systematic data. Mol Phyl Evol 2:152–157

    Article  CAS  Google Scholar 

  • Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insight from sardines and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

  • Groombridge B (1982) The IUCN amphibia–reptilia red data book: Testudines, Crocodylia, Rhynchocephalia. IUCN, Gland Switzerland

    Google Scholar 

  • Hahn MW, Rausher MD, Cunningham CW (2002) Distinguishing between selection and population expansion in an experimental lineage of bacteriophage T7. Genetics 161:11–20

    PubMed  CAS  Google Scholar 

  • Herman DW (1989) Tracking the rare bog turtle. Wildlife North Carol 53:17–19

    Google Scholar 

  • Herman DW, Tryon BW (1997) Land use, development, and natural succession and their effects on bog turtle habitat in the southeastern United States. In: Van Abbema J (ed), Proceedings: Conservation, Restoration, and Management of Tortoises and Turtles: an International Conference. New York Turtle and Tortoise Society, New York, pp 364–371

    Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Article  Google Scholar 

  • Hewitt GM (1999) Post-glacial colonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Hoelzel AR (1999) Impact of population bottlenecks on genetic variation and the importance of life-history; a case study of the northern elephant seal. Biol J Linn Soc 68:23–29

    Article  Google Scholar 

  • Holman JA, Andrews KD (1994) North America quaternary cold-tolerant turtles: distributional adaptations and constraints. Boreas 23:44–52

    Article  Google Scholar 

  • Holman JA, Fritz U (2001) A new emydine species from the Middle Miocene (Barstovian) of Nebraska, USA with a new generic arrangement for the species of Clemmys sensu McDowell (1964) (Reptilia:Testudines: Emydidae). Zoologische Abhandlungen Staatliches Museum für Tierkunde Dresden 51:331–354

    Google Scholar 

  • 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 5:719–725

    Article  Google Scholar 

  • Klemens MW (1990) The herpetofauna of southwestern New England. PhD thesis, University of Kent, Canterbury, United Kingdom

  • Klemens MW (1993) Amphibians and reptiles of Connecticut and adjacent regions. State Geol Nat Hist Survey Conn Bull 112:1–318

    Google Scholar 

  • Klemens MW (2000) Turtle conservation. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Kuo CH, Janzen FJ (2003) Bottlesim: a bottleneck simulation program for long-lived species with overlapping generations. Mol Ecol Notes 3:339–373

    Article  CAS  Google Scholar 

  • Kuo CH, Janzen FJ (2004) Genetic effects of a persistent bottleneck on a natural population of ornate box turtles (Terrapene ornata). Conserv Genet 5:425–437

    Article  CAS  Google Scholar 

  • Lenk P, Fritz U, Joger U, Wink M (1999) Mitochondrial phylogeography of the European pond turtle, Emys orbicularis (Linnaeus 1758). Mol Ecol 8:1911–1922

    Article  PubMed  CAS  Google Scholar 

  • Lewis PO, Crawford DJ (1995) Pleistocene refugium endemics exhibit greater allozymic diversity than widespread congeners in the genus Polygonella (Polygonaceae). Am J Bot 82:141–149

    Article  Google Scholar 

  • Lopez JV, Culver M, Stephens JC, Johnson WE, O’Brien SJ (1997) Rates of nuclear and cytoplasmic mitochondrial DNA sequence divergence in mammals. Mol Biol Evol 14:277–286

    PubMed  CAS  Google Scholar 

  • Mindell DP, Sorenson MD, Dimcheff DE, Hasegawa M, Ast JC, Yuri T (1999) Interordinal relationships of birds and other reptiles based on whole mitochondrial genomes. Syst Biol 48:138–152

    Article  PubMed  CAS  Google Scholar 

  • Mockford SW, McEachern L, Herman TB, Snyder M, Wright JM (2004) Population genetic structure of a disjunct population of Blanding’s turtle (Emydoidea blandingii) in Nova Scotia, Canada. Biol Conserv 123:373–380

    Article  Google Scholar 

  • Moritz C (1994) Applications of mitochondrial DNA analysis in conservation: a critical review. Mol Ecol 3:401–411

    CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nevo E, Beiles A (1991) Genetic diversity and ecological heterogeneity in amphibian evolution. Copeia 3:565–592

    Article  Google Scholar 

  • Nunney L (1991) The influence of age structure and fecundity on effective population size. Proc Roy Soc Ser B 246:71–76

    Article  CAS  Google Scholar 

  • Obbard ME, Brooks RJ (1979) Factors affecting basking in a northern population of the common snapping turtle Chelydra serpentina. Can J Zool 57:435–440

    Article  Google Scholar 

  • Obbard ME, Brooks RJ (1981a) Fate of overwintered clutches of the common snapping turtle (Chelydra serpentina) in Algonquin Park, Ontario. Can Field Nat 95:350–352

    Google Scholar 

  • Obbard ME, Brooks RJ (1981b) A radio telemetry and mark recapture study of activity in the common snapping turtle Chelydra serpentina. Copeia 1981:630–637

    Article  Google Scholar 

  • Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Ver 2. University of Hawaii, Honolulu

    Google Scholar 

  • Pereira L, Dupanloup I, Rosser ZH, Jobling MA, Barbujani G (2001) Y-chromosome mismatch distributions in Europe. Mol Biol Evol 18:1259–1271

    PubMed  CAS  Google Scholar 

  • Pesole G, Gissi C, De Chirico A, Saccone C (1999) Nucleotide substitution rate of mammalian mitochondrial genomes. ␣J Mol Evol 48:427–434

    Article  PubMed  CAS  Google Scholar 

  • Peterson MA, Denno RF (1998a) The influence of dispersal and diet breadth on patterns of genetic isolation by distance in phytophagous insects. Am Nat 152:428–446

    Article  CAS  Google Scholar 

  • Peterson MA, Denno RF (1998b) Life history strategies and the genetic structure of phytophagous insect populations. In: Mopper S, Strauss S (eds), Genetic structure and local adaptation in natural insect populations: effects of ecology, life history, and behavior. Chapman and Hall, New York, ␣pp 263–322

    Google Scholar 

  • Phillips CA, Dimmick WW, Carr JL (1996) Conservation genetics of the common snapping turtle (Chelydra serpentina). Conserv Biol 10:397–405

    Article  Google Scholar 

  • Riberon A, Miaud C, Grossenbacher K, Taberlet P (2001) Phylogeography of the alpine salamander, Salamandra atra (Salamandridae) and the influence of the Pleistocene climatic oscillations on population divergence. Mol Ecol 10:2555–2560

    Article  PubMed  CAS  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Rogers AR, Fraley AE, Bamshad MJ, Watkins WE, Jorde LB (1996) Mitochondrial mismatch analysis is insensitive to the mutational process. Mol Biol Evol 13:895–902

    PubMed  CAS  Google Scholar 

  • Ross TR (1999) Phylogeography and conservation genetics of the Iowa pleistocene snail. Mol Ecol 8:1363–1373

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Springs Harbor Laboratory Press, New York

    Google Scholar 

  • 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 152:1079–1089

    PubMed  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. Ver 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of Geneva

  • Scribner KT, Smith MH, Gibbons JW (1984) Genetic differentiation among local populations of the yellow-bellied slider turtle Pseudemys scripta. Herpetologica 40:382–387

    Google Scholar 

  • Scribner KT, Evans J, Morreale SJ, Smith MH, Gibbons JW (1986) Genetic variability among populations of the yellow-bellied slider turtle (Pseudemys scripta) from aquatically and terrestrially separated habitats. Copeia 1986:691–700

    Article  Google Scholar 

  • Scribner KT, Congdon JD, Chesser RK, Smith MH (1993) Annual differences in female reproductive success affect spatial and cohort-specific genotypic heterogeneity in painted turtles. Evolution 47:1360–1373

    Article  Google Scholar 

  • Shackleton NJ, Opdyke ND (1977) Oxygen isotope and paleomagnetic evidence for early Northern Hemisphere glaciation. Nature 270:216–219

    Article  CAS  Google Scholar 

  • Shackleton NJ, Backman J, Zimmerman H, Kent DV, Hall MA, Roberts DG, Schnikter D, Baldauf JG, Desprairies A, Homrighausen R, Huddlestun P, Keene JB, Kaltenback AJ, Krumsiek KAO, Morton AC, Murray JW, and Westberg-Smith J (1984) Oxygen isotope calibration of the onset of ice rafting and the history of glaciation in the North Atlantic region. Nature 307:620–623

    Article  CAS  Google Scholar 

  • Shaffer HB, Meylan P, McKnight ML (1997) Tests of turtle phylogeny: molecular, morphological and paleontological approaches. Syst Biol 46:235–268

    Article  PubMed  CAS  Google Scholar 

  • 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 14:2047–2064

    Article  PubMed  CAS  Google Scholar 

  • Starkey DE, Shaffer HB, Burke RL, Forstner MRJ, Iverson JB, Janzen FJ, Rhodin AG, Ultsch GR (2003) Molecular systematics, phylogeography, and the effects of Pleistocene glaciation in the painted turtle (Chrysemys picta) complex. Evolution 57:119–128

    Article  PubMed  CAS  Google Scholar 

  • St. Clair RC, Gregory PT (1990) Factors affecting the northern range limit of painted turtles (Chrysemys picta): winter acidosis or freezing? Copeia 1990:1083–1089

  • Storey KB, Storey JM, Brooks SPJ, Churchill TA, Brooks RJ (1988) Hatchling turtles survive freezing during winter hibernation. Proc Natl Acad Sci USA 85:8350–8354

    Article  PubMed  CAS  Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

    Article  PubMed  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:597–601

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Turtle Conservation Fund (2002) A global action plan for conservation of tortoises and freshwater turtles. Strategy and funding prospectus 2002–2007. Conservation International and Chelonian Research Foundation, Washington, DC

    Google Scholar 

  • Tryon BW (1990) Bog turtles (Clemmys muhlenbergii) in the south—a question of survival. Bull Chicago Herpetol Soc 25:57–66

    Google Scholar 

  • Tryon BW, Herman DW (1990) Status, conservation, and management of the bog turtle, Clemmys muhlenbergii, in the southeastern United States. In: Beaman K, Caporaso F, McKeown S, Graff M (eds), Proceedings of the first international symposium on turtles and tortoises: conservation and captive husbandry. Chapman University, Orange California, pp 36–53

    Google Scholar 

  • United States Fish and Wildlife Service (2001) Bog turtle (Clemmys muhlenbergii), northern population, recovery plan. Hadley, Massachussetts

    Google Scholar 

  • Vellend M, Waterway MJ (1999) Geographic patterns in the genetic diversity of a northern sedge, Carex rariflora. Can J Bot 7:269–278

    Article  Google Scholar 

  • Walker D, Avise JC (1998) Principles of phylogeography as illustrated by freshwater and terrestrial turtles in the southeastern United States. Ann Rev Ecol Syst 29:23–58

    Article  Google Scholar 

  • Walker D, Moler PE, Buhlmann KA, Avise JC (1998) Phylogenetic uniformity in mitochondrial DNA of the snapping turtle (Chelydra serpentina). Anim Conserv 1:55–60

    Article  Google Scholar 

  • Weisrock DW, Janzen FJ (2000) Comparative molecular phylogeography of North American Softshell Turtles (Apalone spinifera): implications for regional and wide-scale historical evolutionary forces. Mol Phylogenet Evol 14:152–164

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Tim King and Robyn Johnson for tissues and DNA extracts from bog turtle populations in MA, PA, NC, and VA; Ann Somers and Project Bog Turtle for samples from NC and VA; Alison Whitlock and Michael Klemens for samples from MA; and Robert Zappalorti for samples from PA. The Royal Ontario Museum provided the tissue of G. insculpta. Diane Lynch (USFWS) kindly facilitated the necessary permits. Alvin Breisch, Jesse Jaycox, John Sullivan, and Andrew Nelson provided support and assistance in the field for sampling of New York populations. Field and lab studies were supported by grants and contracts from SUNY-Oswego, the New York State Department of Environmental Conservation, and the Linnaeus Fund of the Chelonian Research Foundation (to PAR); remaining laboratory work was funded by NSF grant DEB-9907798 (to KZ). Labwork was performed in the Evolutionary Genetics Core Facility at Cornell University. We thank ␣J. Austin, F. Janzen, and two anonymous reviewers for comments on earlier versions of the manuscript.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, State University of New York, Oswego, 213 Piez Hall, Oswego, NY, 13126, USA

    Peter A. Rosenbaum

  2. Department of Ecology and Evolutionary Biology, Cornell University, E145 Corson Hall, Ithaca, NY, 14850, USA

    Jeanne M. Robertson & Kelly R. Zamudio

Authors
  1. Peter A. Rosenbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeanne M. Robertson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kelly R. Zamudio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kelly R. Zamudio.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rosenbaum, P.A., Robertson, J.M. & Zamudio, K.R. Unexpectedly low genetic divergences among populations of the threatened bog turtle (Glyptemys muhlenbergii). Conserv Genet 8, 331–342 (2007). https://doi.org/10.1007/s10592-006-9172-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-006-9172-3

Keywords

Search

Navigation