Skip to main content

Advertisement

SpringerLink
Log in

Pedigree reconstruction using molecular data reveals an early warning sign of gene diversity loss in an island population of Tasmanian devils (Sarcophilus harrisii)

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

Abstract

Tasmanian devils have experienced an 85% population decline since the emergence of an infectious cancer. In response, a captive insurance population was established in 2006 with a subpopulation later introduced onto Maria Island, Tasmania. We aimed to (1) examine the genetic parameters of the Maria Island population as a stand-alone site and within its broader metapopulation context, (2) assess the efficacy of assisted colonisations, and (3) inform future translocations. This study reconstructs the pedigree of 86 island-born devils using 31 polymorphic microsatellite loci. Combined molecular and pedigree analysis was used to monitor change in population genetic parameters in 4 years since colonisation. Molecular analysis alone revealed no significant change in genetic diversity, while DNA-reconstructed pedigree analysis revealed a statistically significant increase in inbreeding due to skewed founder representation. Pedigree modelling predicted that gene diversity would only be maintained above the threshold of 95% for a further 2 years, dropping to 77.1% after 40 years. Modelling alternative supplementation strategies revealed introducing eight new founders every 3 years will enable the population to retain 95% gene diversity until 2056, provided the translocated animals breed; to ensure this we recommend introducing ten new females every 3 years. We highlight the value of combining pedigree analyses with molecular data, from both a single-site and metapopulation viewpoint, for analysing changes in genetic parameters within populations of conservation concern. The importance of post-release genetic monitoring in an established population is emphasised, given how quickly inbreeding can accumulate and gene diversity be lost.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allendorf FW, Luikart GH, Aitken SN (2012) Conservation and the genetics of populations. Wiley, Chicester

    Google Scholar 

  • Arthington AH (1991) Ecological and genetic impacts of introduced and translocated freshwater fishes in Australia. Can J Fish Aquat Sci 48:33–43. doi:10.1139/f91-302

    Article  Google Scholar 

  • Bradshaw CJA, Brook BW (2005) Disease and the devil: density-dependent epidemiological processes explain historical population fluctuations in the Tasmanian devil. Ecography 28:181–190. doi:10.1111/j.0906-7590.2005.04088.x

    Article  Google Scholar 

  • Cardoso MJ, Eldridge MDB, Oakwood M, Rankmore B, Sherwin WB, Firestone KB (2009) Effects of founder events on the genetic variation of translocated island populations: implications for conservation management of the northern quoll. Conserv Genet 10:1719–1733. doi:10.1007/s10592-008-9774-z

    Article  Google Scholar 

  • Cheng Y, Sanderson C, Jones M, Belov K (2012) Low MHC class II diversity in the Tasmanian devil (Sarcophilus harrisii). Immunogenetics 64:525–533. doi:10.1007/s00251-012-0614-4

    Article  CAS  PubMed  Google Scholar 

  • Clayton JA, Pavey CR, Vernes K, Tighe M (2014) Review and analysis of Australian macropod translocations 1969–2006. Mammal Rev 44:109–123. doi:10.1111/mam.12020

    Article  Google Scholar 

  • Coulon A (2010) GENHET: an easy-to-use R function to estimate individual heterozygosity. Mol Ecol Resour 10:167–169. doi:10.1111/j.1755-0998.2009.02731.x

    Article  CAS  PubMed  Google Scholar 

  • Cui J, Cheng Y, Belov K (2015) Diversity in the toll-like receptor genes of the Tasmanian devil (Sarcophilus harrisii). Immunogenetics 67:195–201. doi:10.1007/s00251-014-0823-0

    Article  CAS  PubMed  Google Scholar 

  • Earnhardt JM, Thompson SD, Schad K (2004) Strategic planning for captive populations: projecting changes in genetic diversity. Anim Conserv 7:9–16. doi:10.1017/S1367943003001161

    Article  Google Scholar 

  • Epstein B, Jones M, Hamede R, Hendricks S, McCallum H, Murchison EP, Schonfeld B, Wiench C, Hohenlohe P, Storfer A (2016) Rapid evolutionary response to a transmissible cancer in Tasmanian devils. Nat Commun 7:12684. doi:10.1038/ncomms12684

    Article  PubMed  PubMed Central  Google Scholar 

  • Ewing SR, Nager RG, Nicoll MA, Aumjaud A, Jones CG, Keller LF (2008) Inbreeding and loss of genetic variation in a reintroduced population of Mauritius kestrel. Conserv Biol 22:395–404

    Article  PubMed  Google Scholar 

  • 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 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Frankham R (1998) Inbreeding and extinction: Island populations. Conserv Biol 12:665–675. doi:10.1111/j.1523-1739.1998.96456.x

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Gooley RM, Hogg CJ, Belov K, Grueber CE (2017) No evidence of inbreeding depression in a Tasmanian devil insurance population despite significant variation in inbreeding. Sci Rep 7:1830. doi:10.1038/s41598-017-02000-y

    Article  PubMed  PubMed Central  Google Scholar 

  • Griffith B, Scott JM, Carpenter JW, Reed C (1989) Translocation as a species conservation tool: status and strategy. Science 245:477–480

    Article  CAS  PubMed  Google Scholar 

  • Groombridge JJ, Raisin C, Bristol R, Richardson DS (2012) Genetic consequences of reintroductions and insights from population history. In: Ewen J, Armstrong D, Parker K, Seddon P (eds) Reintroduction biology: integrating science and management. Wiley-Blackwell, New Jersey, pp 395–440

    Chapter  Google Scholar 

  • Grueber CE, Jamieson IG (2008) Quantifying and managing the loss of genetic variation in a free-ranging population of takahe through the use of pedigrees. Conserv Genet 9:645–651. doi:10.1007/s10592-007-9390-3

    Article  Google Scholar 

  • Grueber CE, Knafler GJ, King TM, Senior AM, Grosser S, Robertson B, Weston KA, Brekke P, Harris CLW, Jamieson IG (2015a) Toll-like receptor diversity in 10 threatened bird species: relationship with microsatellite heterozygosity. Conserv Genet 16:595–611. doi:10.1007/s10592-014-0685-x

    Article  CAS  Google Scholar 

  • Grueber CE, Peel E, Gooley R, Belov K (2015b) Genomic insights into a contagious cancer in Tasmanian devils. Trends Genet 31:528–535. doi:10.1016/j.tig.2015.05.001

    Article  CAS  PubMed  Google Scholar 

  • Grueber CE, Reid-Wainscoat EE, Fox S, Belov K, Shier DM, Hogg CJ, Pemberton D (2017) Increasing generations in captivity is associated with increased vulnerability of Tasmanian devils to vehicle strike following release to the wild. Sci Rep 7:2161. doi:10.1038/s41598-017-02273-3

    Article  PubMed  PubMed Central  Google Scholar 

  • Guiler E (1970) Observations on the Tasmanian Devil, Sarcophilus harrisii (Marsupialia : Dasyuridae) II. Reproduction, breeding and growth of pouch young. Aust J Zool 18:63–70

    Article  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of hardy-weinberg proportion for multiple alleles. Biometrics 48:361–372. doi:10.2307/2532296

    Article  CAS  PubMed  Google Scholar 

  • Haig SM, Ballou JD (2002) Pedigree analyses in wild populations. In: McCullough D, Beissinger S (eds) Population viability analysis. University of Chicago Press, Chicago, pp 388–405

    Google Scholar 

  • Hawkins CE, Baars C, Hesterman H, Hocking GJ, Jones ME, Lazenby B, Mann D, Mooney N, Pemberton D, Pyecroft S, Restani M, Wiersma J (2006) Emerging disease and population decline of an island endemic, the Tasmanian devil (Sarcophilus harrisii). Biol Conserv 131:307–324. doi:10.1016/j.biocon.2006.04.010

    Article  Google Scholar 

  • Hesterman H, Jones SM, Schwarzenberger F (2008) Reproductive endocrinology of the largest dasyurids: Characterization of ovarian cycles by plasma and fecal steroid monitoring. Part I. The Tasmanian devil (Sarcophilus harrisii). Gen Comp Endocrinol 155:234–244

    Article  CAS  PubMed  Google Scholar 

  • Hogg CJ, Lee AV (2014) DPIPWE-ZAA Tasmanian devil insurance population captive management plan 2014–2018. Zoo and Aquarium Association Australasia, Sydney

    Google Scholar 

  • Hogg C, Srb C, Hockley J (2013) Annual Report for the DPIPWE-ZAA Tasmanian Devil Insurance Population. Zoo and Aquarium Association Australasia, Sydney, Australia

  • Hogg CJ, Ivy JA, Srb C, Hockley J, Lees C, Hibbard C, Jones M (2015) Influence of genetic provenance and birth origin on productivity of the Tasmanian devil insurance population. Conserv Genet 16:1465–1473. doi:10.1007/s10592-015-0754-9

    Article  Google Scholar 

  • Hogg CJ, Lee AV, Srb C, Hibbard C (2016) Metapopulation management of an endangered species with limited genetic diversity in the presence of disease: the Tasmanian devil Sarcophilus harrisii. Int Zoo Yearb 51:1–17. doi:10.1111/izy.12144

    Google Scholar 

  • Hughes R (1982) Reproduction in the Tasmanian devil Sarcophilus harrisii (Dasyuridae, Marsupialia). In: Archer M (ed) Carnivorous marsupials, vol 1. Royal Zoological Society of New South Wales, Sydney, pp 49–63

    Google Scholar 

  • Jamieson IG, Wallis GP, Briskie JV (2006) Inbreeding and endangered species management: Is New Zealand out of step with the rest of the world? Conserv Biol 20:38–47. doi:10.1111/j.1523-1739.2005.00282.x

    Article  PubMed  Google Scholar 

  • Johnson WE, Onorato DP, Roelke ME, Land ED, Cunningham M, Belden RC, McBride R, Jansen D, Lotz M, Shindle D, Howard J, Wildt DE, Penfold LM, Hostetler JA, Oli MK, O'Brien SJ (2010) Genetic restoration of the Florida panther. Science 329:1641–1645. doi:10.1126/science.1192891

    Article  CAS  PubMed  Google Scholar 

  • Jones M, McCallum H (2007) Environmental risk assessment - impact of the introduction of Tasmanian devils to Maria island on the natural values of the island

  • Jones M (1995) Tasmanian devil Sarcophilus harrisii. In: Van Dyck S, Strahan R (eds) The Mammals of Australia. New Holland Publishers, Sydney, pp 82–84

    Google Scholar 

  • Jones ME, Paetkau D, Geffen E, Moritz C (2003) Microsatellites for the Tasmanian devil (Sarcophilus laniarius). Mol Ecol Notes 3:277–279. doi:10.1046/j.1471-8286.2003.00425.x

    Article  CAS  Google Scholar 

  • Jones ME, Paetkau D, Geffen ELI, Moritz C (2004) Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore. Mol Ecol 13:2197–2209. doi:10.1111/j.1365-294X.2004.02239.x

    Article  CAS  PubMed  Google Scholar 

  • Jones ME, Cockburn A, Hamede R, Hawkins C, Hesterman H, Lachish S, Mann D, McCallum H, Pemberton D (2008) Life-history change in disease-ravaged Tasmanian devil populations. Proc Natl Acad Sci U S A 105:10023–10027. doi:10.1073/pnas.0711236105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106. doi:10.1111/j.1365-294X.2007.03089.x

    Article  PubMed  Google Scholar 

  • Lacy RC (1989) Analysis of founder representation in pedigrees: Founder equivalents and founder genome equivalents. Zoo Biol 8:111–123. doi:10.1002/zoo.1430080203

    Article  Google Scholar 

  • Lacy RC, Ballou JD, Pollak JP (2012) PMx: software package for demographic and genetic analysis and management of pedigreed populations: PMx software for pedigree analysis. Methods Ecol Evol 3:433–437. doi:10.1111/j.2041-210X.2011.00148.x

    Article  Google Scholar 

  • Lees C, Andrew P, Sharman A, Byers O (2013) Saving the devil: one species, one plan. WAZA Magazine 14:37–40

    Google Scholar 

  • Leus K, Traylor-Holzer K, Lacy RC (2011) Genetic and demographic population management in zoos and aquariums: recent developments, future challenges and opportunities for scientific research. Int Zoo Yearb 45:213–225. doi:10.1111/j.1748-1090.2011.00138.x

    Article  Google Scholar 

  • Liu N, Chen L, Wang S, Oh C, Zhao H (2005) Comparison of single-nucleotide polymorphisms and microsatellites in inference of population structure. BMC Genet 6 Suppl 1:S26. doi:10.1186/1471-2156-6-S1-S26

  • MacCluer JW, VandeBerg JL, Read B, Ryder OA (1986) Pedigree analysis by computer simulation. Zoo Biol 5:147–160. doi:10.1002/zoo.1430050209

    Article  Google Scholar 

  • Mallick S (2003) Translocation of Tasmanian devils Sarcophilus harrisii (now laniarius) to Tasmanian offshore islands - a proposed measure to quarantine an infection-free population from devil facial tumour (DFT) disease: selection of potential islands and preliminary cost/benefit assessment

  • Marshall T, Slate J, Kruuk L, Pemberton J (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  CAS  PubMed  Google Scholar 

  • McCallum H, Tompkins DM, Jones ME, Lachish S, Mervanek S, Lazenby B, Hocking G, Wiersma J, Hawkins CE (2007) Distribution and impacts of Tasmanian devil facial tumor disease. EcoHealth 4:318–325. doi:10.1007/s10393-007-0118-0

    Article  Google Scholar 

  • Miller W, Miller J, Hayes VM, Ratan A, Petersen DC, Wittekindt NE, Walenz B, Knight J, Qi J, Zhao F, Wang Q, Bedoya-Reina OC, Katiyar M, Tomsho LP, Kasson LM, Hardie RA, Woodbridge P, Tindall EA, Bertelsen MF, Dixon D, Pyecroft S, Helgen KM, Lesk AM, Pringle TH, Patterson N, Zhang Y, Kreiss A, Woods GA, Jones ME, Schuster SC (2011) Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil). Proc Natl Acad Sci USA 108:12348–12353. doi:10.1073/pnas.1102838108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris K, Austin JJ, Belov K (2013) Low major histocompatibility complex diversity in the Tasmanian devil predates European settlement and may explain susceptibility to disease epidemics. Biol Lett 9:20120900. doi:10.1098/rsbl.2012.0900

    Article  PubMed  PubMed Central  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ottewell K, Dunlop J, Thomas N, Morris K, Coates D, Byrne M (2014) Evaluating success of translocations in maintaining genetic diversity in a threatened mammal. Biol Conserv 171:209–219

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel: Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel: Population genetic software for teaching and research - an update. Bioinformatics 28:2537–2539. doi:10.1093/bioinformatics/bts460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pemberton D (1990) Social organisation and behaviour of the Tasmanian devil, Sarcophilus harrisii. Dissertation. University of Tasmania, Hobart

  • Pemberton JM (2008) Wild pedigrees: the way forward. Proc R Soc Biol 275:613–621. doi:10.1098/rspb.2007.1531

    Article  CAS  Google Scholar 

  • Pemberton D, Gales S, Bauer B, Gales R, Lazenby B, Medlock K (2008) The diet of the Tasmanian devil, Sarcophilus harrisii, as determined from analysis of scat and stomach contents. Pap Proc R Soc Tasmania 2:13–22

    Google Scholar 

  • Puckett EE, Kristensen TV, Wilton CM, Lyda SB, Noyce KV, Holahan PM, Leslie DM, Beringer J, Belant JL, White D, Eggert LS (2014) Influence of drift and admixture on population structure of American black bears (Ursus americanus) in the Central Interior Highlands, USA, 50 years after translocation. Mol Ecol 23:2414–2427. doi:10.1111/mec.12748

    Article  PubMed  Google Scholar 

  • R Development Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org. Accessed May 2016

  • Robinson SP, Simmons LW, Kennington WJ (2013) Estimating relatedness and inbreeding using molecular markers and pedigrees: the effect of demographic history. Mol Ecol 22:5779–5792. doi:10.1111/mec.12529

    Article  CAS  PubMed  Google Scholar 

  • Rogers T, Fox S, Pemberton D, Wise P (2016) Sympathy for the devil: captive-management style did not influence survival, body-mass change or diet of Tasmanian devils 1 year after wild release. Wildl Res 43:544–552. doi:10.1071/wr15221

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Santure AW, Stapley J, Ball AD, Birkhead TR, Burke T, Slate JON (2010) On the use of large marker panels to estimate inbreeding and relatedness: empirical and simulation studies of a pedigreed zebra finch population typed at 771 SNPs. Mol Ecol 19:1439–1451. doi:10.1111/j.1365-294X.2010.04554.x

    Article  PubMed  Google Scholar 

  • Seddon PJ, Moro D, Mitchell NJ, Chauvenet A, Mawson P (2015) Proactive conservation or planned invasion? Past, current and future use of assisted colonisation. In: Armstrong D, Hayward M, Moro D, Seddon P (eds) Advances in reintroduction biology of Australian and New Zealand Fauna. CSIRO Publishing, Melbourne, pp 105–126

    Google Scholar 

  • Sigg DP, Goldizen AW, Pople AR (2005) The importance of mating system in translocation programs: reproductive success of released male bridled nailtail wallabies. Biol Conserv 123:289–300

    Article  Google Scholar 

  • Srb C (2015) Tasmanian devil studbook. Healesville Sanctuary on behalf of the Zoo and Aquarium Association, Healesville

    Google Scholar 

  • Swan KD, McPherson JM, Seddon PJ, Moehrenschlager A (2016) Managing marine biodiversity: the rising diversity and prevalence of marine conservation translocations. Conserv Lett 9:239–251

    Article  Google Scholar 

  • Taylor SS, Sardell RJ, Reid JM, Bucher T, Taylor NG, Arcese P, Keller LF (2010) Inbreeding coefficient and heterozygosity-fitness correlations in unhatched and hatched song sparrow nestmates. Mol Ecol 19:4454–4461. doi:10.1111/j.1365-294X.2010.04824.x

    Article  PubMed  Google Scholar 

  • Thalmann S, Peck S, Wise P, Potts JM, Clarke J, Richley J (2016) Translocation of a top-order carnivore: tracking the initial survival, spatial movement, home-range establishment and habitat use of Tasmanian devils on Maria island. Aust Mammal 38:68–79

    Article  Google Scholar 

  • Warton D, Hui F (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  PubMed  Google Scholar 

  • Weeks AR, Sgro CM, Young AG, Frankham R, Mitchell NJ, Miller KA, Byrne M, Coates DJ, Eldridge MDB, Sunnucks P, Breed MF, James EA, Hoffman AA (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evol Appl 4:709–725. doi:10.1111/j.1752-4571.2011.00192.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Wise P, Lee AV, Peck S, Clarke J, Thalmann S, Hockley J, Schaap D, Pemberton D (2016) The conservation introduction of Tasmanian devils to Maria island National Park: A response to devil facial tumour disease (DFTD). In: Soorae PS (ed) Global Re-introduction Perspectives: 2016. Case studies from around the globe. IUCN/SSC Re-introduction Specialist Group and Abu Dhabi, UAE: Environment Agency Abu Dhabi. Gland, Switzerland, pp 166–171

    Google Scholar 

  • Wright B, Morris K, Grueber CE, Willet CE, Gooley RM, Hogg CJ, O'Meally D, Hamede R, Jones ME, Wade C, Belov K (2015) Development of a SNP-based assay for measuring genetic diversity in the Tasmanian devil insurance population. BMC Genomics 16:791

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the Save the Tasmanian Devil Program, in particular Phil Wise and Drew Lee, for providing essential DNA samples and field observation data for the Maria Island devil population. Thank you to Drew Lee for providing a map of Maria Island used in Fig. 1. Thanks also to the studbook keeper (C. Srb) for her maintenance of the Tasmanian devil studbook and species management from the Zoo and Aquarium Association Australasia. We thank two anonymous reviewers for their comments that improved this manuscript.

Funding

Funding for this study was provided via an ARC Linkage grant to KB, CJH and CEG (LP140100508).

Author information

Author notes

    Authors and Affiliations

    1. School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, 2006, Australia

      Elspeth A. McLennan, Rebecca M. Gooley, Katherine Belov, Carolyn J. Hogg & Catherine E. Grueber

    2. Save the Tasmanian Devil Program, DPIPWE, Hobart, TAS, 7001, Australia

      Phil Wise

    3. Zoo and Aquarium Association Australasia, Mosman, NSW, 2088, Australia

      Carolyn J. Hogg

    4. San Diego Zoo Global, P. O. Box 120551, San Diego, CA, 92112, USA

      Catherine E. Grueber

    Authors
    1. Elspeth A. McLennan
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Rebecca M. Gooley
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Phil Wise
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Katherine Belov
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Carolyn J. Hogg
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Catherine E. Grueber
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Catherine E. Grueber.

    Ethics declarations

    Conflict of interest

    The authors declare that they have no conflict of interest.

    Ethical approval

    All Tasmanian devils sampled as part of the monitoring for the Maria Island population were done so under permit and the standard operating procedure of the Tasmanian Department of Primary Industries, Population, Water and the Environment.

    Additional information

    Carolyn J. Hogg and Catherine E. Grueber have contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 28 KB)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    McLennan, E.A., Gooley, R.M., Wise, P. et al. Pedigree reconstruction using molecular data reveals an early warning sign of gene diversity loss in an island population of Tasmanian devils (Sarcophilus harrisii). Conserv Genet 19, 439–450 (2018). https://doi.org/10.1007/s10592-017-1017-8

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10592-017-1017-8

    Keywords

    Search

    Navigation