Genetic legacies of translocation and relictual populations of American marten at the southeastern margin of their distribution

  • Cody M. AylwardEmail author
  • James D. Murdoch
  • C. William Kilpatrick
Research Article


American marten were extirpated from much of their native range in the northeastern United States as a result of land development and overharvesting before the mid-twentieth century. Based on occurrence records, recolonization in the late twentieth century was believed to have occurred via natural population expansion from two refugia: northern Maine and the eastern Adirondack Mountains of New York. Furthermore, a 1989–1991 reintroduction attempt in southern Vermont was originally declared unsuccessful, but marten have been rediscovered in southern Vermont since 2010. We used molecular techniques to resolve uncertain population histories and estimate contemporary levels of genetic variation and gene flow in marten populations in the northeastern United States. We sequenced a 320 bp segment of the control region (D-loop) of mtDNA in 112 individuals and amplified 10 microsatellite loci in 111 individuals. Five genetic clusters were identified in the northeastern United States based on the microsatellite data: (1) Maine, (2) New Hampshire, (3) eastern Adirondacks (New York), (4) western Adirondacks (New York), and (5) southern Vermont. Clustering and assignment tests suggest that individuals in southern Vermont are most likely to have originated in Maine—the primary source of the reintroduction. However, we were unable to rule out the possibility of a relict population in southern Vermont. Population expansion in New Hampshire appears to be the primary source of recolonization in northeastern Vermont. Additionally, dispersers from the reintroduction attempt may have spread to northeastern Vermont. Genetic diversity is lower in the entire northeastern United States than an interior population in Ontario, Canada. This study improves our understanding of population history in the northeastern United States. Relict populations of marten may have persisted through the nineteenth and twentieth centuries where they were believed to have been extirpated. Recognizing and conserving all of the distinct subsets of native genetic diversity in the region could promote long-term population health.


Genetic diversity Genetic structure Martes Peripheral populations Reintroduction Relictual populations 



We thank the Vermont Fish and Wildlife Department and University of Vermont for funding, and Chris Bernier (Vermont Fish and Wildlife Department), Kim Royar (Vermont Fish and Wildlife Department), Paul Jensen (New York Department of Environmental Conservation), Jillian Kilborn (New Hampshire Fish and Game Department), Alexej Sirén (University of Massachusetts Amherst), Cory Mosby (Maine Department of Inland Fisheries and Wildlife), and volunteer trappers from Maine for providing tissue samples for genetic analyses. Katherine O’Shea conducted preliminary microsatellite amplifications.

Supplementary material

10592_2018_1130_MOESM1_ESM.docx (3.6 mb)
Supplementary material 1 (DOCX 3675 KB)


  1. Aylward CM, Murdoch JD, Donovan TM, Kilpatrick CW, Bernier C, Katz J (2018) Estimating distribution and connectivity of recolonizing American marten in the northeastern United States using expert elicitation techniques. Anim Conserv. CrossRefGoogle Scholar
  2. Brooks RT (1996) Assessment of two camera-based systems for monitoring arboreal wildlife. Wildl Soc Bull 24:298–300Google Scholar
  3. Broquet T, Johnson C, Petit E, Thompson I, Burel F, Fryxell JM (2006) Dispersal and genetic structure in the American marten, Martes americana. Mol Ecol 15:1689–1697CrossRefPubMedGoogle Scholar
  4. Brussard PF (1984) Geographic patterns and environmental gradients: the central-marginal model in Drosophila revisited. Ann Rev Ecol Syst 15:25–64CrossRefGoogle Scholar
  5. Carroll C (2007) Interacting effects of climate change, landscape conversion, and harvest on carnivore populations at the range margin: Marten and Lynx in the northern Appalachians. Conserv Biol 21:1092–1104CrossRefPubMedGoogle Scholar
  6. Channell R, Lomolino MV (2000) Dynamic biogeography and conservation of endangered species. Nature 403:84–86CrossRefPubMedGoogle Scholar
  7. Chen C, Durand E, Forbes F, François O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7:747–756CrossRefGoogle Scholar
  8. Clark TW, Anderson E, Douglas C, Strickland M (1987) Martes americana. Mamm Species 289:1–8CrossRefGoogle Scholar
  9. Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinform 9:539CrossRefGoogle Scholar
  10. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  11. Daniel A, Hanson T (2001) Remote, rocky, barren, bushy, wild-woody wilderness: the natural history of the northeast. In: McGrory-Klyza C (ed) Wilderness comes home: rewilding the northeast. University Press of New England, Hanover, pp 27–46Google Scholar
  12. Davis MH (1983) Post-release movements of introduced marten. J Wildl Manag 47:59–66CrossRefGoogle Scholar
  13. Davis CS, Strobeck C (1998) Isolation, variability, and cross-species amplification of polymorphic microsatellite loci in the family Mustelidae. Mol Ecol 7:1776–1778CrossRefPubMedGoogle Scholar
  14. Distefano JJ, Royar KJ, Pence DM, Denoncour JE (1990) Marten recovery plan for Vermont. Vermont Fish and Wildlife Department, WaterburyGoogle Scholar
  15. Drew RE, Hallett JG, Aubry KB, Cullings KW, Koepf SM, Zielinski WJ (2003) Conservation genetics of the fisher (Martes pennanti) based on mitochondrial DNA sequencing. Mol Ecol 12:51–62CrossRefPubMedGoogle Scholar
  16. Durand E, Jay F, Gaggiotti OE, François O (2009) Spatial inference of admixture proportions and secondary contact zones. Mol Biol Evol 26:1963–1973CrossRefGoogle Scholar
  17. 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
  18. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  19. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864CrossRefPubMedGoogle Scholar
  20. 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 10:564–567CrossRefPubMedGoogle Scholar
  21. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedPubMedCentralGoogle Scholar
  22. Fleming MA, Ostrander EA, Cook JA (1999) Microsatellite markers for American mink (Mustela vison) and ermine (Mustela erminea). Mol Ecol 8:1352–1354CrossRefPubMedGoogle Scholar
  23. Foster DR, Donahue B, Kittredge DB, Motzkin G, Hall B, Turner BL, Chilton E (2008) New England’s forest landscape: ecological legacies and conservation patterns shaped by agrarian history. In: Redman CL, Foster DR (eds) Agrarian landscapes in transition. Oxford University Press, New York, pp 44–88Google Scholar
  24. Fuller R (1987) Proposed endangered and threatened mammals. In: Laughlin S (ed), The endangered and threatened species of plants and animals in Vermont. Vermont Fish and Wildlife Department, Waterbury, pp. 42–54Google Scholar
  25. Godin AJ (1977) Wild mammals of New England. Johns Hopkins University Press, BaltimoreGoogle Scholar
  26. Goudet (2015) Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol Ecol Resour 5:184–186CrossRefGoogle Scholar
  27. Grauer JA, Gilber JH, Woodford JE, Eklund D, Anderson S, Pauli JN (2017) Unexpected genetic composition of a reintroduced carnivore population. Biol Conserv 215:246–253CrossRefGoogle Scholar
  28. Griekspoor A, Groothuis T (2006) A high-tech infusion for science. In: 4Peaks. 10 Dec 2012Google Scholar
  29. Guillot G, Mortier F, Estoup A (2005) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715CrossRefGoogle Scholar
  30. Hagmeier EM (1956) Distribution of marten and fisher in North America. Can Field-Nat 70:149–168Google Scholar
  31. Hapeman P, Latch EK, Fike JA, Rhodes OE, Kilpatrick CW (2011) Landscape genetics of fishers (Martes pennanti) in the Northeast: dispersal barriers and historical influences. J Hered 102:251–259CrossRefPubMedGoogle Scholar
  32. Hapeman P, Latch EK, Rhodes OE, Kilpatrick CW (2014) When recent and evolutionary histories meet: deciphering temporal events from contemporary patterns of mtDNA from fishers (Martes pennanti) in north-eastern North America. J Zool Syst Evol Res 52:331–337CrossRefGoogle Scholar
  33. Kelly JR, Fuller TK, Kanter JJ (2009) Records of recovering American marten, Martes americana, in New Hampshire. Can Field-Nat 123:1–6CrossRefGoogle Scholar
  34. Koen EL, Bowman J, Garroway CJ, Mills SC, Wilson PJ (2012) Landscape resistance and American marten gene flow. Landscape Ecol 27:29–43CrossRefGoogle Scholar
  35. Krohn WB (2012) Distribution changes of American martens and fishers in eastern North America, 1699–2001. In: Aubry KB, Zielinski WJ, Raphael MG, Proulx G, Buskirk SW (eds) Biology and conservation of martens sables and fishers, a new synthesis. Cornell University Press, Ithaca, pp 58–73Google Scholar
  36. Kyle CJ, Strobeck C (2003) Genetic homogeneity of Canadian mainland marten populations underscores the distinctiveness of Newfoundland pine martens (Martes americana atrata). Can J Zool 66:57–66CrossRefGoogle Scholar
  37. Kyle CJ, Davis CS, Strobeck C (2000) Microsatellite analysis of North American pine marten (Martes americana) populations from the Yukon and Northwest Territories. Can J Zool 78:1150–1157CrossRefGoogle Scholar
  38. Lambeck RJ (1997) Focal species: a multi-species umbrella for nature conservation. Conserv Biol 11:849–856CrossRefGoogle Scholar
  39. Landguth EL, Cushman SA, Schwartz MK, McKelvey KS, Murphy M, Luikart G (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191CrossRefGoogle Scholar
  40. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  41. Lesica P, Allendorf FW (1995) When are peripheral populations valuable for conservation? Conserv Biol 9:753–760CrossRefGoogle Scholar
  42. Moruzzi TL, Royar KJ, Grove C, Brooks RT, Bernier C, Thompson FL, DeGraaf RM, Fuller TK (2003) Assessing an American marten, Martes americana, reintroduction in Vermont. Can Field-Nat 117:190–195CrossRefGoogle Scholar
  43. Mowry RA, Schneider TM, Latch EK, Gompper ME, Beringer J, Eggert LS (2015) Genetics and the successful reintroduction of the Missouri river otter. Anim Conserv 18:196–206CrossRefGoogle Scholar
  44. O’Brien P, Bernier C, Hapeman P (2018) A new record of an American marten (Martes americana) population in southern Vermont. Small Carniv Conserv 56:68–75Google Scholar
  45. Paradis E (2010) Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420CrossRefPubMedGoogle Scholar
  46. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669CrossRefGoogle Scholar
  47. 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
  48. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  49. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a program for detecting recent effective population size reductions from allele data frequencies. J Hered 90:502–503CrossRefGoogle Scholar
  50. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539CrossRefPubMedGoogle Scholar
  51. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  52. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  53. Rice WER (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefPubMedGoogle Scholar
  54. Royar KJ (1992) Monitoring reintroduced marten populations in Vermont. Vermont Fish and Wildlife Department, WaterburyGoogle Scholar
  55. 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 152:1079–1089PubMedPubMedCentralGoogle Scholar
  56. Schwartz M (2005) Guidelines on the use of molecular genetics in reintroduction programs. In: The EU LIFE-nature projects to guidelines for the reintroduction of threatened species. Caramanico Terme, Italy, pp 51–58Google Scholar
  57. Seddon PJ, Armstrong DP, Maloney RF (2007) Developing the science of reintroduction biology. Conserv Biol 21:303–312CrossRefPubMedGoogle Scholar
  58. Shields GF, Kocher TD (1991) Phylogenetic relationships of north American ursids based on analyses of mitochondrial DNA. Evolution 45:218–221CrossRefPubMedGoogle Scholar
  59. Silver H (1957) A history of New Hampshire game and furbearers. New Hampshire fish and game, survey report number 6. Concord, New HampshireGoogle Scholar
  60. Slough BG (1989) Movements and habitat use by transplanted marten in the Yukon Territory. J Wildl Manag 53:991–997CrossRefGoogle Scholar
  61. Soutiere E, Coulter MW (1975) Interim report: reintroduction of Marten to the White Mountain National Forest, New HampshireGoogle Scholar
  62. Stewart FEC, Volpe JP, Taylor JS, Bowman J, Thomas PJ, Pybus M, Fisher JT (2017) Distinguishing reintroduction from recolonization with genetic testing. Biol Conserv 214:242–249CrossRefGoogle Scholar
  63. Trombulak S, Royar KJ (2001) Restoring the wild: Species recovery and reintroductions. In: McGrory-Klyza C (ed) Wilderness comes home: rewilding the northeast. University Press of New England, Hanover, pp 157–181Google Scholar
  64. Tucker JM, Schwartz MK, Truex R, Wisely SM, Allendorf FW (2014) Sampling affects the detection of genetic subdivision and conservation implications for fisher in the Sierra Nevada. Conserv Genet 15:123–136CrossRefGoogle Scholar
  65. Vincent IR, Farid A, Otieno CJ (2003) Variability of thirteen microsatellite markers in American mink (Mustela vison). Can J Anim Sci 83:597–599CrossRefGoogle Scholar
  66. Walker CW, Vilà C, Landa A, Linden M, Ellegren H (2001) Genetic variation and population structure in Scandinavian wolverine (Gulo gulo) populations. Mol Ecol 10:53–63CrossRefPubMedGoogle Scholar
  67. Williams BW, Scribner KT (2010) Effects of multiple founder populations on spatial genetic structure of reintroduced American martens. Mol Ecol 19:227–240CrossRefPubMedGoogle Scholar
  68. Wolf CM, Griffith B, Reed C, Temple SA (1996) Avian and mammalian translocations: update and reanalysis of 1987 survey data. Conserv Biol 10:1142–1154CrossRefGoogle Scholar
  69. Woods JG, Paetkau D, Lewis D, McLellan BN, Proctor M, Strobeck C (1999) Genetic tagging of free-ranging black and brown bears. Wildl Soc Bull 27:616–627Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Cody M. Aylward
    • 1
    • 2
    Email author
  • James D. Murdoch
    • 1
  • C. William Kilpatrick
    • 3
  1. 1.Wildlife and Fisheries Biology Program, Rubenstein School of Environment and Natural ResourcesUniversity of Vermont, George D. Aiken CenterBurlingtonUSA
  2. 2.Department of Fish, Wildlife and Conservation BiologyUniversity of California, DavisDavisUSA
  3. 3.Department of BiologyUniversity of VermontBurlingtonUSA

Personalised recommendations