Conservation Genetics

, Volume 12, Issue 6, pp 1619–1631 | Cite as

Genetic consequences of isolation: island tammar wallaby (Macropus eugenii) populations and the conservation of threatened species

  • Emily J. MillerEmail author
  • Mark D. B. Eldridge
  • Keith D. Morris
  • Kyall R. Zenger
  • Catherine A. Herbert
Research Article


Isolation and restricted gene flow can lead to genetic deterioration in populations. Populations of many species are increasingly becoming fragmented due to human impacts and active management is required to prevent further extinctions. Islands provide an ideal location to protect species from many mainland threatening processes such as habitat loss and fragmentation, disease and competition/predation from introduced species. However their isolation and small population size renders them prone to loss of genetic diversity and to inbreeding. This study examined two endemic and one introduced population of tammar wallaby (Macropus eugenii) on three islands in the Houtman Abrolhos Archipelago, Western Australia: East Wallabi (EWI), West Wallabi (WWI) and North Islands (NI). Nine autosomal and four Y-linked microsatellite loci, and sequence data from the mitochondrial DNA (mtDNA) control region were used to examine the impact of long-term isolation (EWI and WWI) and small founder size (NI) on genetic diversity and inbreeding. This study found all three populations had low genetic diversity, high levels of effective inbreeding and increased frequency of morphological abnormalities. Isolation has also led to significant inter-population genetic differentiation. These results highlight the importance of incorporating genetic management strategies when utilising islands as refuges for declining mainland populations.


Conservation genetics Population structure Genetic differentiation Genetic diversity Inbreeding Microsatellite 



This research was funded by an ARC Linkage Grant (LP0560344) and forms part of the Koala and Kangaroo Contraception Program. Special thanks to Neil Thomas, Brent Johnson, Peter Orell from DEC (WA) for field assistance; John Fitzharding; The Rat Patrol; Lee Ann Rollins (UNSW) and Greg Eldridge. All experimental work carried out was approved by the Department of Environment and Conservation, Western Australia under the approval numbers 10/2005 and 40/2007.

Supplementary material

10592_2011_265_MOESM1_ESM.doc (136 kb)
Supplementary material 1 (DOC 136 kb)


  1. Abbott I (2000) Improving the conservation of threatened and rare mammal species through translocation to islands: case study Western Australia. Biol Conserv 93:195–201CrossRefGoogle Scholar
  2. Abbott I, Burbridge AA (1995) The occurrence of mammal species on the islands of Australia: a summary of existing knowledge. CALM Sci 1:259–324Google Scholar
  3. Alexander WB (1922) The vertebrate fauna of Houtman’s Abrohlos (Abrohlos Islands), Western Australia. J Linn Soc Zool 34:457–486CrossRefGoogle Scholar
  4. Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5:181–190CrossRefGoogle Scholar
  5. Boessenkool S, Taylor S, Tepolt C, Komdeur J, Jamieson I (2007) Large mainland populations of South Island robins retain greater genetic diversity than offshore island refuges. Conserv Genet 8:705–714CrossRefGoogle Scholar
  6. BOM (2008) National Tidal Centre. Bureau of Meterology.
  7. Cabe PR (1998) The effects of founding bottlenecks on the genetic variation in the European starling (Sturnus vulgaris) in North America. Heredity 80:519–525CrossRefGoogle Scholar
  8. Cooper DW, McKenzie LM (1997) Genetics of tammar wallabies. In: Saunders NR, Hinds LA (eds) Marsupial biology: recent research and new perspectives. UNSW Press, Sydney, pp 120–131Google Scholar
  9. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  10. Courtenay J, Friend T (2003) Gilbert’s potoroo recovery plan: July 2003–June 2008. Department of Environment and Conservation, Western AustraliaGoogle Scholar
  11. DeRose MA, Roff DA (1999) A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53:1288–1292CrossRefGoogle Scholar
  12. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449PubMedCrossRefGoogle Scholar
  13. EH D (2004) Translocation proposal: re-introduction of mainland SA tammar wallaby to Innes National Park. Department for Environment and Heritage Adelaide, South AustraliaGoogle Scholar
  14. 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 13:531–541CrossRefGoogle Scholar
  15. Eldridge MDB, Kinnear JE, Zenger KR, McKenzie LM, Spencer PBS (2004) Genetic diversity in remnant mainland and “pristine” island populations of three endemic Australian macropodids (Marsupialia): Macropus eugenii, Lagorchestes hirsutus and Petrogale lateralis. Conserv Genet 5:325–338CrossRefGoogle Scholar
  16. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  17. Excoffier L, Laval G, Schneider S (2005) ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  18. Ficetola GF, Bonin A, Miaud C (2008) Population genetics reveals origin and number of founders in a biological invasion. Mol Ecol 17:773–782PubMedCrossRefGoogle Scholar
  19. Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327PubMedCrossRefGoogle Scholar
  20. Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675CrossRefGoogle Scholar
  21. Frankham R (2009) Where are we in conservation genetics and where do we need to go? Conserv Genet (online first)Google Scholar
  22. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeGoogle Scholar
  23. Fumagalli L, Pope LC, Taberlet P, Moritz C (1997) Versatile primers for the amplification of the mitochondrial DNA control region in marsupials. Mol Ecol 6:1199–1201PubMedCrossRefGoogle Scholar
  24. GeoscienceAustralia (2005) Australian GovernmentGoogle Scholar
  25. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet J (1995) FSTAT v-1.2: a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  26. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by molecular clock of mitochondrial DNA. J Mol Evol 22:160–174PubMedCrossRefGoogle Scholar
  27. Hedrick PW (1995) Gene flow and genetic restoration: the Florida panther as a case study. Conserv Biol 9:996–1007CrossRefGoogle Scholar
  28. Hedrick PW (2001) Conservation genetics: where are we now? Trends Ecol Evol 16:629–636CrossRefGoogle Scholar
  29. Hedrick PW, Fredrickson RJ (2008) Captive breeding and the reintroduction of Mexican and red wolves. Mol Ecol 17:344–350PubMedCrossRefGoogle Scholar
  30. Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162CrossRefGoogle Scholar
  31. Hedrick PW, Gutierrez-Espeleta GA, Lee RN (2001) Founder effect in an island population of bighorn sheep. Mol Ecol 10:851–857PubMedCrossRefGoogle Scholar
  32. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinfomatics 17:754–755CrossRefGoogle Scholar
  33. IUCN (2006) 2006 IUCN Red List of threatened species.
  34. Jamieson IG (2007) Has the debate over genetics and extinction of island endemics truly been resolved? Anim Conserv 10:139–144CrossRefGoogle Scholar
  35. Johnson MS (1988) Founder effects and geographic variation in the land snail Theba pisana. Heredity 61:133–142CrossRefGoogle Scholar
  36. Jones ME, Paetkau D, Geffen E, Moritz C (2004) Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore. Mol Ecol 13:2197–2209PubMedCrossRefGoogle Scholar
  37. Kinnear JE, Sumner NR, Onus ML (2002) The red fox in Australia—an exotic predator turned biocontrol agent. Biol Conserv 108:335–359CrossRefGoogle Scholar
  38. Land DE, Shindle D, Cunningham M, Lotz M, Ferree B (2004) Florida panther genetic restoration and management: annual performance report 2003–2004. Florida Fish and Wildlife Conservation Commission, FloridaGoogle Scholar
  39. MacDonald AJ, Sankovic N, Sarre SD, Fitzsimmons NN, Wakefield MJ, Graves JAM, Zenger KR (2006) Y chromosome microsatellite markers identified from the tammar wallaby (Macropus eugenii) and their amplification in three other macropod species. Mol Ecol Notes 6:1202–1204CrossRefGoogle Scholar
  40. Madsen T, Shine R, Olsson M, Wittzell H (1999) Conservation biology: restoration of an inbred adder population. Nature 402:34–35CrossRefGoogle Scholar
  41. Main AR (1961) The occurence of Macropodidae on islands and its climatic and ecological implications. J R Soc West Aust 44:84–89Google Scholar
  42. McKenzie NL, Burbidge AA, Baynes A (2006) Australian mammal map updates. Western Australian Department of Conservation and Land Management. Department of Conservation and Land Management, Western AustraliaGoogle Scholar
  43. Miller EJ, Eldridge MDB, Herbert CA (2010) Dominance, body size and internal relatedness influence male reproductive success in eastern grey kangaroos (Macropus giganteus). Reprod Fertil Dev 22:539–549PubMedCrossRefGoogle Scholar
  44. 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 7:387–395CrossRefGoogle Scholar
  45. Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trends Ecol Evol 9:373–375PubMedCrossRefGoogle Scholar
  46. Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130:217–228CrossRefGoogle Scholar
  47. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  48. 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
  49. Peltier WR (2004) Global glacial isostasy and the surface of the ice-age Earth: the ICE-5G (VM2) model and GRACE. Annu Rev Earth Planet Sci 32:111–149CrossRefGoogle Scholar
  50. Pimm SL, Dollar L, Bass OL Jr (2006) The genetic rescue of the Florida panther. Anim Conserv 9:115–122CrossRefGoogle Scholar
  51. 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 90:502–503CrossRefGoogle Scholar
  52. Poole WE, Wood JT, Simms NG (1991) Distribution of the tammar, Macropus eugenii, and the relationships of populations as determined by cranial morphometrics. Wildl Res 18:625–639CrossRefGoogle Scholar
  53. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  54. Possingham H, Jarman P, Kearns A (2003) Independent review of Western Shield. Department of Conservation and Land Management, PerthGoogle Scholar
  55. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  56. Ramstad KM, Woody CA, Sgae GK, Allendorf FW (2004) Founding events influence genetic population structure of sockeye salmon (Oncorhynchus nerka) in Lake Clark, Alaska. Mol Ecol 13:277–290PubMedCrossRefGoogle Scholar
  57. Rankmore BR, Griffiths AD, Woinarski JCZ, Ganambarr BL, Taylor R, Brennan K, Firestone K, Cardoso M (2008) Island translocation of the northern quoll Dasyurus hallucatus as a conservation response to the spread of the cane toad Chaunus (Bufo) marinus in the Northern Territory, Australia. Australian Government National Heritage Trust, Northern Territory GovernmentGoogle Scholar
  58. Raymond M, Rousset F (2003) GenePop 3.4., an updated version of GenePop V.1.2 (1995): population genetics software for exact tests and ecumenicism. J Heredi 86:248–249Google Scholar
  59. Rice WR (1989) Analysing tables for statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  60. Robinson NA, Murray ND, Sherwin WB (1993) VNTR loci reveal differentiation between and structure within populations of the eastern barred bandicoot Perameles gunnii. Mol Ecol 2:195–207CrossRefGoogle Scholar
  61. Robinson AC, Canty PD, Mooney T, Ruddock P (1996) South Australia’s offshore islands. Department of Environment and Conservation, AdelaideGoogle Scholar
  62. Roelke ME, Martenson J, O’Brien SJ (1993) The consequences of demographic reduction and genetic depletion in the endangered Florida panther. Curr Biol 3:340–350PubMedCrossRefGoogle Scholar
  63. Seymour AM, Montgomery ME, Costello BH, Ihle S, Johnsson G, St John B, Taggart D, Houlden BA (2001) High effective inbreeding coefficients correlate with morphological abnormalities in populations of South Australian koalas (Phascolarctos cinereus). Anim Conserv 4:211–219CrossRefGoogle Scholar
  64. Sinclair EA (2001) Phylogeographic variation in the quokka, Setonix brachyurus (Marsupialia: Macropodidae): implications for conservation. Anim Conserv 4:325–333CrossRefGoogle Scholar
  65. Soulé ME (1976) Allozyme variation, its determinants in space and time. In: Ayala FJ (ed) Molecular evolution. Sinauer Associates, Sunderland, pp 151–169Google Scholar
  66. Spielman D, Brook BW, Briscoe DA, Frankham R (2004) Does inbreeding and loss of genetic diversity decrease disease resistance? Conserv Genet 5:439–488CrossRefGoogle Scholar
  67. Stanley F, Morris K, Holmes T, Moore J (2010) Giant steps: industry and conservation make history through Gorgon. Landscope 25:10–16Google Scholar
  68. Storr GM (1960) The physiography, vegetation and vertebrate fauna of North Island, Houtman Abrohlos. J R Soc West Aust 43:59–62Google Scholar
  69. Storr GM (1965) The physiography, vegetation and vertebrate fauna of the Wallabi Group, Houtman Abrohlos. J R Soc West Aust 48:1–14Google Scholar
  70. Sunnucks P, Hales D (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphidae). Mol Ecol 13:510–524Google Scholar
  71. Sunquist ME, Sunquist F (2001) Changing landscapes: consequences for carnivores. In: Gittleman JL, Funk SM, Macdonald D, Wayne RK (eds) Carnivore conservation. Cambridge University Press, Cambridge, pp 399–418Google Scholar
  72. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, SunderlandGoogle Scholar
  73. Tarr CL, Conant S, Fleisher RC (1998) Founder events and variation at microsatellite loci in an insular passerine bird, the Laysan finch (Telespiza cantans). Mol Ecol 7:719–731CrossRefGoogle Scholar
  74. Taylor AC, Cooper DW (1998) A set of tammar wallaby (Macropus eugenii) microsatellites tested for genetic linkage. Mol Ecol 7:925–931PubMedCrossRefGoogle Scholar
  75. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  76. Waples RS (1991) Pacific salmon, Oncorhynchus spp., and the definition of “species” under the endangered species act. Mar Fish Rev 53:11Google Scholar
  77. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  78. Williamson-Natesan E (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562CrossRefGoogle Scholar
  79. Wright M, Stott P (1999) The Kangaroo Island Tammar wallaby: assessing ecologically sustainable commercial harvesting. A report for the Rural Industries Research and Development Corporation, University of Adelaide, SA, CanberraGoogle Scholar
  80. Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418PubMedCrossRefGoogle Scholar
  81. Zenger KR, Cooper DW (2001) Characterisation of 14 macropod microsatellite genetic markers. Anim Genet 32:160–167CrossRefGoogle Scholar
  82. Zenger KR, Eldridge MDB, Pope LC, Cooper DW (2003a) Characterisation and cross-species utility of microsatellite markers within kangaroos, wallabies and rat kangaroos (Macropodoidea: Marsupialia). Aust J Zool 51:587–596CrossRefGoogle Scholar
  83. Zenger KR, Richardson BJ, Vachot-Griffin AM (2003b) A rapid population expansion retains genetic diversity within European rabbits in Australia. Mol Ecol 12:789–794PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Emily J. Miller
    • 1
    • 2
    Email author
  • Mark D. B. Eldridge
    • 4
  • Keith D. Morris
    • 5
  • Kyall R. Zenger
    • 6
  • Catherine A. Herbert
    • 1
    • 3
  1. 1.School of Biological, Earth and Environmental SciencesUniversity of New South WalesKensingtonAustralia
  2. 2.School of Biological SciencesThe University of SydneySydneyAustralia
  3. 3.Faculty of Veterinary ScienceUniversity of SydneyCamperdownAustralia
  4. 4.Department of Molecular BiologyAustralian MuseumSydneyAustralia
  5. 5.Department of Environment and ConservationWestern Australian Wildlife Research CentreWannerooAustralia
  6. 6.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia

Personalised recommendations