Skip to main content
Log in

Implications of introgression for wildlife translocations: the case of North American martens

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The evolutionary consequences of natural introgression provide a rare opportunity to retrospectively evaluate how the introduction of exotics or genetic rescue efforts may impact endemic faunas. Phylogeographic structure among mainland, endemic insular, and introduced North American marten (Martes americana and M. caurina) populations have been shaped by a complex history of natural, post-glacial population expansion followed by a series of anthropogenic introductions. In some cases, both natural colonization and translocations facilitated secondary contact, offering a series of replicated experiments that demonstrate how introgression, in these cases following isolation (insular and refugial), shapes genetic diversity. We test whether genetic exchange is occurring between North American marten species using mitochondrial genomes and ten nuclear loci. We present evidence of biased nuclear introgression from M. caurina into M. americana across two natural hybrid zones (insular and mainland) and found no remnant evidence of M. caurina on islands that received M. americana translocations, suggesting prior absence, potential extirpation, or genetic swamping of M. caurina from these islands. Our results highlight the importance of understanding phylogeographic variation prior to identifying source populations for wildlife translocations and caution the use of genetic rescue for North American marten populations. Although previously managed as a single species, these two species show substantial genetic divergence. When the two are placed into contact, they exhibit unidirectional, asymmetric introgression with potentially negative consequences for M. caurina, underscoring the value of mindful consideration of introgression in wildlife management.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson E (1948) Hybridization of the habitat. Evolution 2:1–9

    Article  Google Scholar 

  • Barton NH (2005) Fitness landscapes and the origin of species. Evolution 59:246–248

    Google Scholar 

  • Bouckaert R, Heled J, Kühnert D et al (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537. https://doi.org/10.1371/journal.pcbi.1003537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buerkle CA (2005) Maximum-likelihood estimation of a hybrid index based on molecular markers. Mol Ecol Notes 5:684–687

    Article  CAS  Google Scholar 

  • Carrara P, Ager TA, Baichtal JF (2007) Possible refugia in the Alexander Archipelago of southeastern Alaska during the late Wisconsin glaciation. Can J Earth Sci 44:229–244

    Article  Google Scholar 

  • Chesters D (2013) Collapsetypes.pl. https://sourceforge.net/projects/collapsetypes/files/

  • Colbeck G, Gibbs H, Marra P et al (2008) Phylogeography of a widespread North American migratory song bird (Setophaga ruticilla). J Hered 99:453–463

    Article  CAS  PubMed  Google Scholar 

  • Colella JP, Pierson BJ, Wilson RA, Talbot SL (2018) Sequence information from the mitogenome and ten nuclear genes from Martes species (Martes americana, M. caurina) of North America, 1972–2010: U.S. Geol Surv Data Release. https://doi.org/10.5066/P9V1L0SI

    Article  Google Scholar 

  • Cook JA, Dawson NG, MacDonald SO (2006) Conservation of highly fragmented systems: the northerntemperate Alexander Archipelago. Biol Conserv 133:1–15

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson N, Cook JA (2012) Behind the genes: diversification of North American Martens (Martes americana and M. caurina). 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 23–38

    Google Scholar 

  • Dawson NG, Colella JP, Small MP et al (2017) Historical biogeography sets the foundation for contemporary conservation of martens (genus Martes) in northwestern North America. J Mammal 98:715–730

    Article  Google Scholar 

  • Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York

    Google Scholar 

  • Drummond A, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite v3.5: a new series of programs to perform population genetics analysis under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675

    Article  Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gese E, Knowlton FF, Adams JR et al (2015) Managing hybridization of a recovering endangered species: the red wolf (Canis rufus) as a case study. Curr Zool 61:191–205

    Article  Google Scholar 

  • Gompert Z, Buerkle CA (2009) A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Mol Ecol 18:1207–1224

    Article  PubMed  Google Scholar 

  • Gompert Z, Buerkle CA (2010) Introgress: a software package for mapping components of isolation in hybrids. Mol Ecol Resour 10:378–384

    Article  CAS  PubMed  Google Scholar 

  • Grauer J, Gilbert J, Woodford J et al (2017) Unexpected genetic composition of a reintroduced carnivore population. Biol Conserv 215:246–253

    Article  Google Scholar 

  • Haig SM, Allendorf FW (2006) Hybrids and policy. In: Scott JM, Goble DD, Davis F (eds.) The endangered species act at thirty: conserving biodiversity in human-dominated landscapes, Island Press. Chicago, pp 150–163

    Google Scholar 

  • Hanski I (2005) The shrinking world: ecological consequences of habitat loss. International Ecology Institute, Oldendorf/Luhe

    Google Scholar 

  • Heaton TD, Grady F (2003) The late Wisconsin vertebrate history of Prince of Wales Island, Southeast Alaska. In: Schubert BW, Mead JI, Graham RW (eds.) Ice age cave faunas of North America, Indiana University Press, Bloomington, pp 17–53

    Google Scholar 

  • Heaton TH, Talbot SL, Shields GF (1996) An ice age refugium for large mammals in the Alexander Archipelago, Southeastern Alaska. Quat Res 46:186–192

    Article  CAS  Google Scholar 

  • Heled J, Drummond AJ (2008) Bayesian inference of population size history from multiple loci. BMC Evol Biol 8:289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580

    Article  CAS  PubMed  Google Scholar 

  • Hey J (2005) On the number of New World founders: a population genetic portrait of the peopling of the Americas. PLoS Biol 3:965–975

    Article  CAS  Google Scholar 

  • Hey J (2010) Isolation with migration models for more than two populaions. Molec Biol Evol 27:905–920

    Article  CAS  PubMed  Google Scholar 

  • Hey J, Nielsen R (2007) Integration with the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Nat Acad Sci USA 104:2785–2790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoberg EP, Koehler AVA, Cook JA (2012) Complex host-parasite systems in Martes implications for conservation biology of endemic faunas. 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 39–57

    Google Scholar 

  • Hope AG, Ho SYW, Malaney JL et al (2014) Accounting for rate variation among lineages in comparative demographic analyses. Evolution 68–9:2689–2700

    Article  Google Scholar 

  • Hubbs CL (1955) Hybridization between fishes in nature. Syst Zool 4:1–20

    Article  Google Scholar 

  • Johnson CA, Fryxell JM, Thompson ID, Baker JA (2009) Mortality risk increases with natal dispersal distance in American martens. P R Soc Lond B 276:3361–3367. https://doi.org/10.1098/rspb.2008.1958

    Article  Google Scholar 

  • Jombart T (2008) Adegenet: a R package for multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jombart T, Collins C (2015) A tutorial for discriminant analysis of principal components (DAPC) using adegenet 2.0.0. http://adegenet.r-forge.r-project.org/files/tutorial-dapc-pdf

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. J Zool 85:1049–1064

    Google Scholar 

  • Kohn BE, Eckstein RG (1987) Status of marten in Wisconsin, 1985. Department of Natural Resources 143, Madison

    Google Scholar 

  • Krohn W (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 58–73

    Google Scholar 

  • Kurtén B, Anderson E (1980) Pleistocene mammals of North America. Columbia University Press, New York

    Google Scholar 

  • Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am Nat 142:911–927

    Article  PubMed  Google Scholar 

  • Lavretsky P, Peters J, Winker K et al (2016) Becoming pure: identifying generational classes of admixed individuals within lesser and greater scaup populations. Mol Ecol 25:661–674

    Article  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DNAsp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Linnell MA, Moriarty K, Green DS, Levi T (2018) Density and population viability of coastal marten: a rare and geographically isolated small carnivore. PeerJ 6:e4530

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu L, Yu L, Edwards SV (2010) A maximum pseudo-likelihood approach for estimating species trees under the coalescent model. BMC Evol Biol 10:302

    Article  PubMed  PubMed Central  Google Scholar 

  • Medrano J, Aasen E, Sharrow L (1990) DNA extraction from nucleated red blood cells. Biotechniques 8:43

    CAS  PubMed  Google Scholar 

  • Merriam CH (1890) Descriptions of twenty-six new species of North American mammals. N Am Fauna 1890:1–55

    Google Scholar 

  • Milián-García Y, Ramos-Targarona R, Pérez-Fleitas E et al (2015) Genetic evidence of hybridization between the critically endangered Cuban crocodile and the American crocodile: implications for population history and in situ/ex situ conservation. Heredity 114:272–280

    Article  CAS  PubMed  Google Scholar 

  • Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420

    Article  CAS  PubMed  Google Scholar 

  • Pauli J, Moss W, Manlick P et al (2015) Examining the uncertain origin and management role of martens on Prince of Wales Island, Alaska. Conserv Biol 29:1257–1267

    Article  PubMed  Google Scholar 

  • Powell RA, Lewis JC, Slough BG et al (2012) Evaluating translocations of martens, sables, and fishers: testing model predictions with field data. 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, p 536

    Google Scholar 

  • Rambaut A (2012) FigTree v1.4. http://tree.bio.ed.ac.uk/software/figtree/. Accessed Jan 2018

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://beast.community/tracer

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    Article  CAS  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP Version 1.2: population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Article  Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Rodriguez D, Forstner M, Moler P et al (2011) Effect of human-mediated migration and hybridization on the recovery of the American crocodile in Florida (USA). Conserv Genet 12:449–459

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Schilthuizen M, Giesbers MCWG, Beukeboon LW (2011) Haldane’s rule in the 21st century. Heredity 107:95–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sethuraman A, Hey J (2016) Parallel MCMC and inference of ancient demography under the Isolation with Migration (IM) model. Mol Ecol Resour 16:206–215

    Article  PubMed  Google Scholar 

  • Shull GH (1948) What is “heterosis”? Genetics 33:439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Slauson KM, Baldwin JA, Zielinski WJ (2012) Occupancy estimation and modeling in Martes research and monitoring. 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 343–368

    Google Scholar 

  • Small MP, Stone KD, Cook JA (2003) American marten (Martes americana) in the Pacific Northwest: population differentiation across a landscape fragmented in time and space. Mol Ecol 12:89–103

    Article  CAS  PubMed  Google Scholar 

  • Sonsthagen SA, Talbot SL, White CM (2004) Gene flow and genetic characterization of northern goshawks breeding in Utah. The Condor 106:826–836

    Article  Google Scholar 

  • Soulé ME (1987) Where do we go from here? In: Viable populations for conservation. Cambridge University Press, Cambridge, pp 175–183

    Chapter  Google Scholar 

  • Stamatakis A (2014) RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–11313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stephens M, Smith N, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stewart FE, Volpe JP, Taylor JS et al (2017) Distinguishing reintroduction from recolonization with genetic testing. Biol Conserv 214:242–249

    Article  Google Scholar 

  • Stone KD, Cook JA (2002) Molecular evolution of Holarctic martens (genus Martes, Mammalia: Carnivora: Mustelidae). Mol Phylogenet Evol 24:169–179

    Article  CAS  PubMed  Google Scholar 

  • Stone KD, Flynn RW, Cook JA (2002) Post-glacial colonization of northwestern North America by the forest-associated American marten (Martes americana, Mammalia: Carnivora: Mustelidae). Mol Ecol 11:2049–2063

    Article  CAS  PubMed  Google Scholar 

  • Swenson NG, Howard DJ (2005) Clustering of contact zones, hybrid zones, and phylogeographic breaks in North America. Am Nat 166:581–591

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teeter K, Payseur B, Harris L et al (2008) Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res 18:67–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas M, Roemer G, Donlan J et al (2013) Ecology: Gene tweaking for conservation. Nature 501:485–486

    Article  PubMed  Google Scholar 

  • Todesco M, Pascual MA, Owens GL et al (2016) Hybridization and extinction. Evol Appl 9:892–908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turton W (1806) A general system of nature, through the three grand kingdoms of animals, vegetables, and minerals. Lackington and Allen, London, United Kingdom. Natl Union Catalog 605:388

    Google Scholar 

  • USDA (U. S. Department of Agriculture) (2007a) Kuiu timber sale area record of decision. Tongass National Forest Report R10-MB-620. Tongass National Forest, Ketchikan, Alaska. https://www.fs.usda.gov/nfs/11558/www/nepa/3332_FSPLT1_017178.pdf

  • USDA (U. S. Department of Agriculture) (2007b) Kuiu timber sale area final environmental impact statement. Tongass National Forest Report R10-MB-604. Tongass National Forest, Ketchikan, Alaska. https://play.google.com/books/reader?id=AYs2AQAAMAAJ&printsec=frontcover&output=reader&hl=en&pg=GBS.PP1

  • vonHoldt BM, Cahill J, Fan Z, Gronau I, Robinson J, Pollinger JP, Shapiro B, Wall J, Wayne RK (2016) Whole-genome sequence analysis shows that two endemic species of North American wolf are admixtures of the coyote and gray wolf. Sci Adv 2:e1501714

    Article  PubMed  PubMed Central  Google Scholar 

  • Williams BW, Gilbert JH, Zollner PA (2007) Historical Perspective on the Reintroduction of the Fisher and American Marten in Wisconsin and Michigan. US Department of Agriculture, Forest Service, Northern Research Station, Newtown Square

    Book  Google Scholar 

  • Wisely SM, Santymire RM, Livieri TM, Meuting SA, Howard J (2008) Genotypic and phenotypic consequences of reintroduction history in the black-footed ferret (Mustela nigripes). Conserv Genet 9:389–399

    Article  Google Scholar 

  • Woerner AE, Cox MP, Hammer MF (2007) Recombination-filtered genomic datasets by information maximization. Bioinformatics 23:1851–1853

    Article  CAS  PubMed  Google Scholar 

  • Wright PL (1953) Intergradation between Martes americana and Martes caurina in Western Montana. J Mammal 34:74–86

    Article  Google Scholar 

Download references

Acknowledgements

We thank Sarah Sonsthagen for streamlining MiSeq protocols at the U.S. Geological Survey, Alaska Science Center; Haven Shaginoff and Aaron Cde Baca for lab assistance; Travis Burkhard for computational support; Barbara Deshler for independent reviews; Alaska and British Columbia trappers, Nikolai Dokuchaev, Natalie Dawson, Melissa Fleming, and Anson Koehler for coordinating specimen acquisition; and our funding sources, including: the American Society of Mammalogists Grant-in-Aid, the UNM Biology Graduate Student Association, U.S. Geological Survey, and NSF-DEB 1258010 for support. This research used resources provided by the Center for Advanced Research Computing (CARC) at the University of New Mexico and the Core Science Analytics, Synthesis, and Libraries (CSASL) Advanced Research Computing (ARC) group at the U.S. Geological Survey. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U. S. Government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jocelyn P. Colella.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 13 KB)

Supplementary material 2 (DOCX 4486 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Colella, J.P., Wilson, R.E., Talbot, S.L. et al. Implications of introgression for wildlife translocations: the case of North American martens. Conserv Genet 20, 153–166 (2019). https://doi.org/10.1007/s10592-018-1120-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-018-1120-5

Keywords

Navigation