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Microsatellite and mitochondrial DNA variation defines island genetic reservoirs for reintroductions of an endangered Australian marsupial, Perameles bougainville

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Abstract

Natural populations of the endangered western barred bandicoot (Perameles bougainville) now exist on only two islands in Shark Bay, Western Australia. Our aim was to investigate genetic diversity in natural, reintroduced, and captive populations of the bandicoots and to assess the extent of divergence between the populations. The contemporary isolation of the natural populations has resulted in heterogeneity of allele frequency between the islands, which has acted to maintain a higher combined diversity than would be expected from either population on its own. These findings highlight how remnant island populations can act as genetic reservoirs to maximize diversity for reintroductions into a species former range. Although diversity is high between island populations, diversity within populations, based on six microsatellite loci, are amongst the lowest ever recorded for populations of marsupials. The mtDNA sequence data indicate that the two remaining natural populations show only minor divergence from each other, with the five haplotypes separated by just single base pairs. The reintroduced population and captive colonies show evidence for the loss of diversity related to genetic drift operating on small isolated populations.

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References

  • Arrendal J, Walker CW, Sundqvist AK, Hellborg L, Vila C (2004) Genetic evaluation of an otter translocation program. Conserv Genet 5:79–88

    Article  CAS  Google Scholar 

  • Balloux F (2001) EASYPOP (version 1.7). A computer program for the simulation of population genetics. J Hered 92:301–302

    Article  PubMed  CAS  Google Scholar 

  • Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations?. Mol Ecol 13:3021–3031

    Article  PubMed  CAS  Google Scholar 

  • Beaumont M, Barratt EM, Gottelli D, Kitchener AC, Daniels MJ, Pritchard JK, Bruford MW (2001) Genetic diversity and introgression in the Scottish wildcat. Mol Ecol 10:319–336

    Article  PubMed  CAS  Google Scholar 

  • Blin N, Stafford DW (1976) General method for isolation of high molecular-weight DNA from eukaryotes. Nucleic Acids Res 3:2303–2308

    PubMed  CAS  Google Scholar 

  • Burbidge AA, McKenzie NL (1989) Patterns in the modern decline of Western Australia’s vertebrate fauna: causes and conservation implications. Biol Conserv 50:143–198

    Article  Google Scholar 

  • Churchill DM (1959) Late Quaternary eustatic changes in the Swan River District. J R Soc West Aust 42:53–55

    Google Scholar 

  • Cornuet JM, Luikart G (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • DeSalle R, Amato G (2004) The expansion of conservation genetics. Nat Rev Genet 5:702–712

    Article  PubMed  CAS  Google Scholar 

  • Dirienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human-populations. Proc Natl Acad Sci USA 91:3166–3170

    Article  CAS  Google Scholar 

  • Ebenhard T (1995) Conservation breeding as a tool for saving animal species from extinction. Trends Ecol Evol 10:438–443

    Article  Google Scholar 

  • Eldridge MDB, King JM, Loupis AK Spencer PBS, Taylor AC, Pope LC, Hall GP (1999) Unprecedented low levels of genetic variation and inbreeding depression in an island population of the black-footed rock-wallaby. Conserv Biol 13:531–541

    Article  Google Scholar 

  • 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 131:479–491

    PubMed  CAS  Google Scholar 

  • Excoffier LGL, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolution Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Fischer D Bachmann K (1998) Microsatellite enrichment in organisms with large genomes (Allium cepa L.). Biotechniques 24:796–802+

    Google Scholar 

  • Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327

    Article  PubMed  Google Scholar 

  • Frankham R (2005) Stress and adaptation in conservation genetics. J Evolution Biol 18:750–755

    Article  CAS  Google Scholar 

  • Frankham R, Manning H, Margan SH, Briscoe DA (2000) Does equalization of family sizes reduce genetic adaptation to captivity?. Anim Conserv 3:357–363

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Friend JA (1990) Status of bandicoots in Western Australia. In: Seebeck JH, Brown PR, Wallis RI, Kemper CM (eds) Bandicoots and bilbies. Surrey Beatty and Sons, Sydney, pp 73–84

    Google Scholar 

  • Friend JA, Beecham B (2004) Return to Dryandra: Western shield review – February 2003. Conserv Sci West Aust 5:174–193

    Google Scholar 

  • Friend JA, Burbidge AA (1995) Western barred bandicoot. In: Strahan R (ed) The mammals of Australia. Reed Books, Chatswood, NSW

    Google Scholar 

  • Fumagalli L, Pope LC, Taberlet P, Moritz C (1997) Versatile primers for the amplification of the mitochondrial DNA control region in marsupials. Mol Ecol 6:1199–1201

    Article  PubMed  CAS  Google Scholar 

  • Fumagalli L, Moritz C, Taberlet P, Friend JA (1999). Mitochondrial DNA sequence variation within the remnant populations of the endangered numbat (Marsupialia : Myrmecobiidae : Myrmecobius fasciatus). Mol Ecol 8:1545–1549

    Article  PubMed  CAS  Google Scholar 

  • Goldstein DB, Pollock DD (1997) Launching microsatellites: a review of mutational processes and methods of phylogenetic inference. J Hered 88:335–342

    PubMed  CAS  Google Scholar 

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hedrick PW (2004) Recent developments in conservation genetics. Forest Ecol Manage 197:3–19

    Article  Google Scholar 

  • Hedrick P (2005) ‘Genetic restoration’: a more comprehensive perspective than ‘genetic rescue’. Trends Ecol Evol 20:109–109

    Article  PubMed  Google Scholar 

  • Hogg JT, Forbes SH, Steele BM, Luikart G (2006) Genetic rescue of an insular population of large mammals. Proc R Soc B-Biol Sci 273:1491–1499

    Article  Google Scholar 

  • Ingvarsson PK (2001) Restoration of genetic variation lost – the genetic rescue hypothesis. Trends Ecol Evol 16:62–63

    Article  PubMed  Google Scholar 

  • Jones ME, Paetkau D, Geffen E, Moritz C (2004) Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore. Mol Ecol 13:2197–2209

    Article  PubMed  CAS  Google Scholar 

  • Kendrick GW (1978) New species of fossil nonmarine molluscs from Western Australia and evidence of late Quaternary climate change in the Shark Bay district. Proc R Soc West Aust 60:49–60

    Google Scholar 

  • Le Page SL, Livermore RA, Cooper DW, Taylor AC (2000) Genetic analysis of a documented population bottleneck: introduced Bennett’s wallabies (Macropus rufogriseus rufogriseus) in New Zealand. Mol Ecol 9:753–763

    Article  PubMed  CAS  Google Scholar 

  • Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449

    Article  PubMed  CAS  Google Scholar 

  • Longmire JL, Maltbie M, Baker RJ (1997) Use of “lysis buffer” in DNA isolation and its implication for museum collections. Occasional Papers, Museum of Texas Tech University

  • Lynch M, O’Hely M (2001) Captive breeding and the genetic fitness of natural populations. Conserv Genet 2:363–378

    Article  Google Scholar 

  • Maehr DS, Crowley P, Cox JJ, Lacki MJ, Larkin JL, Hoctor TS, Harris LD, Hall PM (2006) Of cats and Haruspices: genetic intervention in the Florida panther. Response to Pimm et al. (2006). Anim Conserv 9:127–132

    Article  Google Scholar 

  • Mawson PR (2004) Captive breeding programs and their contribution to Western Shield: Western Shield review – February 2003. Conserv Sci West Aust 5:122–130

    Google Scholar 

  • Maxwell S, Burbidge AA, Morris K (1996) The 1996 Action Plan for Australian Marsupials and Monotremes in I. S. S. C. Australian Marsupial and Monotreme Specialist Group, editor

  • Mills HR,Moro D, Spencer PBS (2004) Conservation significance of island versus mainland populations: a case study of dibblers (Parantechinus apicalis) in Western Australia. Anim Conserv 7:387–395

    Article  Google Scholar 

  • Montalvo AM, Ellstrand NC (2000) Transplantation of the subshrub Lotus scoparius: testing the home-site advantage hypothesis. Conserv Biol 14:1034–1045

    Article  Google Scholar 

  • Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130:217–228

    Article  Google Scholar 

  • Moritz C, Heideman A, Geffen E, McRae P (1997) Genetic population structure of the Greater Bilby Macrotis lagotis, a marsupial in decline. Mol Ecol 6:925–936

    Article  PubMed  CAS  Google Scholar 

  • Morris K, Simms C, Himbeck K, Christensen P, Sercombe N, Ward B, Noakes N (2004) Project Eden – fauna recovery on Peron Peninsula, Shark Bay: Western Shield review – February 2003. Conserv Sci West Aust 5:202–234

    Google Scholar 

  • Moseby KE, O’Donnell E (2003) Reintroduction of the greater bilby, Macrotis lagotis (Reid) (Marsupialia: Thylacomyidae), to northern South Australia: survival, ecology and notes on reintroduction protocols. Wildlife Res 30:15–27

    Article  Google Scholar 

  • Nordstrom T, Nourizad K, Ronaghi M, Nyren P (2000) Method enabling pyrosequencing on double-stranded DNA. Anal Biochem 282:186–193

    Article  PubMed  CAS  Google Scholar 

  • Nunney L, Campbell KA (1993) Assessing minimum viable population-size: demography meets population-genetics. Trends Ecol Evol 8:234–239

    Article  Google Scholar 

  • O’Hara AJ, Warren KS, Swan RA, Simms C, Friend JA (2004) FC-17 Cutaneous papillomatosis and carcinomatosis in the highly endangered Western Barred Bandicoot. Veter Dermat 15:25–25

    Article  Google Scholar 

  • Ostermann SD, Deforge JR, Edge WD (2001) Captive breeding and reintroduction evaluation criteria: a case study of peninsular bighorn sheep. Conserv Biol 15:749–760

    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

    Article  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Ralls K, Ballou J (1986) Captive breeding programs for populations with a small number of founders. Trends Ecol Evol 1:19–22

    Article  Google Scholar 

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

    Google Scholar 

  • Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Richards JD (2005) Western barred bandicoot, burrowing bettong and banded hare-wallaby recovery plan. In W. A. D. o. C. a. L. Management, editor

  • Richards JD, Short J (2003) Reintroduction and establishment of the western barred bandicoot Perameles bougainville (Marsupialia: Peramelidae) at Shark Bay, Western Australia. Biol Conserv 109:181–195

    Article  Google Scholar 

  • Robert A, Couvet FSD (2004) Influence of the rate of introduction on the fitness of restored populations. Conserv Genet 5:673–682

    Article  Google Scholar 

  • Serena M (ed) (1995) Reintroduction biology of Australian and New Zealand fauna. Surrey Beatty & Sons, Chipping Norton

    Google Scholar 

  • Short J, Turner B, Majors C, Leone J (1997) The fluctuating abundance of endangered mammals on Bernier and Dorre Islands, Western Australia – conservation implications. Aust Mammal 20:53–71

    Google Scholar 

  • Short J, Richards JD, Turner B (1998) Ecology of the western barred bandicoot (Perameles bougainville) (Marsupialia : Peramelidae) on Dorre and Bernier Islands, Western Australia. Wildlife Res 25:567–586

    Article  Google Scholar 

  • Sigg DP (2006) Reduced genetic diversity and significant genetic differentiation after translocation: Comparison of the remnant and translocated populations of bridled nailtail wallabies (Onychogalea fraenata). Conserv Genet 7:577–589

    Article  Google Scholar 

  • Slatkin M (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Smith S, Morin PA (2005) Optimal storage conditions for highly dilute DNA samples: A role for trehalose as a preserving agent. J Forensic Sci 50:1101–1108

    Article  PubMed  CAS  Google Scholar 

  • Taylor AC, Cooper DW (1998) A set of tammar wallaby (Macropus eugenii) microsatellites tested for genetic linkage. Mol Ecol 7:925–926

    Article  PubMed  CAS  Google Scholar 

  • Taylor AC, Sherwin WB, Wayne RK (1994) Genetic-variation of microsatellite loci in a bottlenecked species – the northern hairy-nosed wombat Lasiorhinus krefftii. Mol Ecol 3:277–290

    Article  PubMed  CAS  Google Scholar 

  • Theodorou K, Couvet D (2004) Introduction of captive breeders to the wild: harmful or beneficial?. Conserv Genet 5:1–12

    Article  Google Scholar 

  • Todd CR, Jenkins S, Bearlin AR (2002) Lessons about extinction and translocation: models for eastern barred bandicoots (Perameles gunnii) at Woodlands Historic Park, Victoria, Australia. Biol Conserv 106:211–223

    Article  Google Scholar 

  • Tordoff HB, Redig PT (2001) Role of genetic background in the success of reintroduced Peregrine Falcons. Conserv Biol 15:528–532

    Article  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Wang JL, Ryman N (2001) Genetic effects of multiple generations of supportive breeding. Conserv Biol 15:1619–1631

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Zenger KR, Johnston PG (2001) Isolation and characterization of microsatellite loci in the southern brown bandicoot (Isoodon obesulus), and their applicability to other marsupial species. Mol Ecol Notes 1:149–151

    Article  CAS  Google Scholar 

  • Zenger KR, Eldridge MDB, Johnston PG (2005) Phylogenetics, population structure and genetic diversity of the endangered southern brown bandicoot (Isoodon obesulus) in south-eastern Australia. Conserv Genet 6:193–204

    Article  CAS  Google Scholar 

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Acknowledgements

Our thanks go to Neil Thomas and Nicole Noakes from the Western Australian Department of Environment and Conservation; Jacqui Richards from the Australian Wildlife Conservancy; and Mark Bennett and Lucy Woolford from Murdoch University for supplying samples and background information for this study. Tony Friend from the Western Australian Department of Environment and Conservation provided many useful suggestions for the design of the project and provided many of the samples from the captive colony he initiated at Dryandra. Many thanks also to Jeff Short for helpful comments on an earlier draft of the manuscript.

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  1. Centre for Riverine Landscapes, Molecular Ecology Lab, Faculty of Environmental Sciences, Griffith University, 170 Kessels Rd, Nathan, QLD, 4111, Australia

    Steve Smith & Jane Hughes

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  1. Steve Smith
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Correspondence to Steve Smith.

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Smith, S., Hughes, J. Microsatellite and mitochondrial DNA variation defines island genetic reservoirs for reintroductions of an endangered Australian marsupial, Perameles bougainville . Conserv Genet 9, 547–557 (2008). https://doi.org/10.1007/s10592-007-9368-1

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