Advertisement

Conservation Genetics

, Volume 18, Issue 5, pp 1077–1089 | Cite as

Genetic evidence of range-wide population declines in an Australian marsupial prior to European settlement

  • Anna Brüniche-Olsen
  • Stephanie L. Hazlitt
  • Mark D. B. Eldridge
Research Article

Abstract

Reconstruction of a species demographic history can be used to investigate impacts of environmental change through time. Australia’s mesic biome experienced massive changes during the Holocene, including climate fluctuations, increased human populations, and European settlement. Using microsatellite data from 202 brush-tailed rock-wallabies (Petrogale penicillata) sampled across the species current geographic range, we investigated gene flow and inferred the demographic history of the species to explore the historical impacts of environmental change on this once wide-ranging marsupial mammal. We found high levels of genetic diversity in all colonies, despite very restricted contemporary gene flow and no sign of historical gene flow. Demographic analyses showed that individual populations have low effective population sizes (N e < 200). We identified a major historical decline throughout the species range occurring 10,000–1000 years before present, spanning a period with increased El Niño Southern Oscillation activity, increased human population size and establishment of the dingo population. This major decline pre-dates the European settlement of Australia and so places the species most recent dramatic decline into context, suggesting that brushed-tailed rock-wallabies were inherently vulnerable to major changes to their environment.

Keywords

Marsupial Demographic history Gene flow Microsatellite Rock-wallaby 

Supplementary material

10592_2017_960_MOESM1_ESM.docx (708 kb)
Supplementary material 1 (DOCX 708 KB)

References

  1. Act E (1999) Environment Protection and Biodiversity Conservation Act 1999 (Cth)Google Scholar
  2. Allentoft ME, Heller R, Oskam CL et al (2014) Extinct New Zealand megafauna were not in decline before human colonization. Proc Natl Acad Sci USA 111:4922–4927CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ashcroft MB, Cavanagh M, Eldridge MD, Gollan JR (2014) Testing the ability of topoclimatic grids of extreme temperatures to explain the distribution of the endangered brush-tailed rock-wallaby (Petrogale penicillata). J Biogeogr 41:1402–1413CrossRefGoogle Scholar
  4. Attenbrow V (1982) Archaeological Investigation of Deep Creek Shelter, Mangrove Creek Dam. Unpublished report to NSW National Parks and Wildlife ServiceGoogle Scholar
  5. Barnosky AD, Koch PL, Feranec RS, Wing SL, Shabel AB (2004) Assessing the causes of late Pleistocene extinctions on the continents. Science 306:70–75CrossRefPubMedGoogle Scholar
  6. Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345CrossRefPubMedGoogle Scholar
  7. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568CrossRefPubMedPubMedCentralGoogle Scholar
  8. Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326CrossRefPubMedPubMedCentralGoogle Scholar
  9. Blois JL, McGuire JL, Hadly EA (2010) Small mammal diversity loss in response to late-Pleistocene climatic change. Nature 465:771–774CrossRefPubMedGoogle Scholar
  10. Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83CrossRefPubMedGoogle Scholar
  11. Bradshaw CJA (2012) Little left to lose: deforestation and forest degradation in Australia since European colonization. J Plant Ecol 5:109–120CrossRefGoogle Scholar
  12. Brook BW, Sodhi NS, Bradshaw CJA (2008) Synergies among extinction drivers under global change. Trends Ecol Evol 23:453–460CrossRefPubMedGoogle Scholar
  13. Brooks SP, Gelman A (1998) General methods for monitoring convergence of iterative simulations. J Comput Gr Stat 7:434–455Google Scholar
  14. Brüniche-Olsen A, Jones ME, Austin JJ, Burridge CP, Holland BR (2014) Extensive population decline in the Tasmanian devil predates European settlement and devil facial tumour disease. Biol Lett 10:20140619CrossRefPubMedPubMedCentralGoogle Scholar
  15. Byrne M (2008) Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quatern Sci Rev 27:2576–2585CrossRefGoogle Scholar
  16. Chikhi L, Sousa VC, Luisi P, Goossens B, Beaumont MA (2010) The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics 186:983–995CrossRefPubMedPubMedCentralGoogle Scholar
  17. Colhoun EA, Shimeld PW (2012) Late-Quaternary vegetation history of Tasmania from pollen records. Peopled Landsc 34:29Google Scholar
  18. Cooper A, Turney C, Hughen KA et al (2015) Abrupt warming events drove late pleistocene holarctic megafaunal turnover. Science 349:602–606CrossRefPubMedGoogle Scholar
  19. 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
  20. Cornuet J-M, Pudlo P, Veyssier J et al (2014) DIYABC v2. 0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics, 30(8):1187–1189CrossRefGoogle Scholar
  21. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295CrossRefPubMedGoogle Scholar
  22. Cristescu R, Sherwin W, Handasyde K, Cahill V, Cooper D (2010) Detecting bottlenecks using BOTTLENECK 1.2.02 in wild populations: the importance of the microsatellite structure. Conserv Genet 11:1043–1049CrossRefGoogle Scholar
  23. Davis MB, Shaw RG (2001) Range shifts and adaptive responses to quaternary climate change. Science 292:673–679CrossRefPubMedGoogle Scholar
  24. DECC (2008) Recovery plan for the brush-tailed rock-wallaby (Petrogale penicillata) (ed. Department of Environment and Climate Change S, New South Wales.), SydneyGoogle Scholar
  25. Diggle PJ, Gratton RJ (1984) Monte Carlo methods of inference for implicit statistical models. J R Stat Soc 193–227Google Scholar
  26. Duncan RP, Blackburn TM, Worthy TH (2002) Prehistoric bird extinctions and human hunting. Proc R Soc Lond B 269:517–521CrossRefGoogle Scholar
  27. Eldridge MDB, Close RL (2008) Brush-tailed rock-wallaby Petrogale penicillata. In: The mammals of Australia (Van Dyck S, Strahan R (eds)), pp. 382–384. New Holland, SydneyGoogle Scholar
  28. Eldridge MDB, Coulson GM (2015) Family Macropodidae (kangaroos and wallabies). In: Handbook of the mammals of the world (Wilson DE, Mittermeier RA (eds)). Lynx Edicions, BarcelonaGoogle Scholar
  29. Eldridge MDB, King JM, Loupis AK et al (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
  30. Eldridge MDB, Kinnear JE, Onus ML (2001) Source population of dispersing rock-wallabies (Petrogale lateralis) idengified by assignment tests on multilocus genotypic data. Mol Ecol 10:2867–2876CrossRefPubMedGoogle Scholar
  31. Ellegren H (2004) Microsatellites: Simple sequences with complex evolution. Nat Rev Genet 5:435–445CrossRefPubMedGoogle Scholar
  32. Ellegren H, Moore S, Robinson N et al (1997) Microsatellite evolution—A reciprocal study of repeat lengths at homologous loci in cattle and sheep. Mol Biol Evol 14:854–860CrossRefPubMedGoogle Scholar
  33. Estoup A, Jarne P, Cornuet J (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604CrossRefPubMedGoogle Scholar
  34. 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 131:479–491PubMedPubMedCentralGoogle Scholar
  35. Frankham R (1995) Effective population size adult population size ratios in wildlife—a review. Genet Res 66:95–107CrossRefGoogle Scholar
  36. Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675CrossRefGoogle Scholar
  37. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  38. Girod C, Vitalis R, Leblois R, Freville H (2011) Inferring population decline and expansion from microsatellite data: a simulation-based evaluation of the MSVAR method. Genetics 88(1):165–179Google Scholar
  39. Gollan K (1984) The Australian dingo: in the shadow of man. Vertebrate Zoogeography Evolu Aust, 921–927Google Scholar
  40. Goossens B, Chikhi L, Ancrenaz M et al (2006) Genetic signature of anthropogenic population collapse in orang-utans. Plos Biology 4:e25CrossRefPubMedPubMedCentralGoogle Scholar
  41. Hansen BD, Harley DKP, Lindenmayer DB, Taylor AC (2009) Population genetic analysis reveals a long-term decline of a threatened endemic Australian marsupial. Mol Ecol 18:3346–3362CrossRefPubMedGoogle Scholar
  42. Hazlitt S, Goldizen A, Eldridge MB (2006a) Significant patterns of population genetic structure and limited gene flow in a threatened macropodid marsupial despite continuous habitat in southeast Queensland, Australia. Conserv Genet 7:675–689CrossRefGoogle Scholar
  43. Hazlitt S, Sigg D, Eldridge M, Goldizen A (2006b) Restricted mating dispersal and strong breeding group structure in a mid-sized marsupial mammal (Petrogale penicillata). Mol Ecol 15:2997–3007CrossRefPubMedGoogle Scholar
  44. Hazlitt SL, Eldridge MDB, Goldizen AW (2010) Strong matrilineal structuring in the brush-tailed rock-wallaby confirmed by spatial patterns of mitochondrial DNA. Macropods 87–95Google Scholar
  45. Hazlitt SL, Goldizen AW, Nicholls JA, Eldridge MD (2014) Three divergent lineages within an Australian marsupial (Petrogale penicillata) suggest multiple major refugia for mesic taxa in southeast Australia. Ecol Evol 4:1102–1116CrossRefPubMedPubMedCentralGoogle Scholar
  46. Heller R, Lorenzen ED, Okello JBA, Masembe C, Siegismund HR (2008) Mid-Holocene decline in African buffalos inferred from Bayesian coalescent-based analyses of microsatellites and mitochondrial DNA. Mol Ecol 17:4845–4858CrossRefPubMedGoogle Scholar
  47. Hing S, Narayan E, Thompson RCA, Godfrey S (2014) A review of factors influencing the stress response in Australian marsupials. Conserv Physiol 2:cou027CrossRefPubMedPubMedCentralGoogle Scholar
  48. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  49. Jeffreys H (1998) The theory of probability. Oxford University Press, OxfordGoogle Scholar
  50. Johnson C (2006) Australia’s mammal extinctions: a 50000 year history. Cambridge University Press, CambridgeGoogle Scholar
  51. Johnson CN, Letnic M (2013) Introducing a new top predator, the dingo. Invas Biol Ecol Theor 414Google Scholar
  52. Johnson CN, Wroe S (2003) Causes of extinction of vertebrates during the Holocene of mainland Australia: arrival of the dingo, or human impact? Holocene 13:941–948CrossRefGoogle Scholar
  53. Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795CrossRefGoogle Scholar
  54. Kumar S, Subramanian S (2002) Mutation rates in mammalian genomes. Proc Nat Acad Sci USA 99:803–808CrossRefPubMedPubMedCentralGoogle Scholar
  55. Lennon MJ, Taggart DA, Temple-Smith PD, Eldridge MDB (2011) The impact of isolation and bottlenecks on genetic diversity in the Pearson Island population of the black-footed rock-wallaby (Petrogale lateralis pearsoni; Marsupialia: Macropodidae). Aust Mammal 33:152–161CrossRefGoogle Scholar
  56. Letnic M, Dickman CR (2006) Boom means bust: interactions between the El Niño/Southern Oscillation (ENSO), rainfall and the processes threatening mammal species in arid Australia. Biodivers Conserv 15:3847–3880CrossRefGoogle Scholar
  57. Lorenzen ED, Nogues-Bravo D, Orlando L et al (2011) Species-specific responses of late quaternary megafauna to climate and humans. Nature 479:359–364CrossRefPubMedPubMedCentralGoogle Scholar
  58. Lourandos H (1997) Continent of hunter-gatherers: new perspectives in Australian prehistory. Cambridge University Press, CambridgeGoogle Scholar
  59. Lunney D, Law B, Rummery C (1996) Contrast between the visible abundance of the brush-tailed rock-wallaby, Petrogale penicillata, and its rarity in fox and dog scats in the gorges east of Armidale, New South Wales. Wildl Res 23:373–379CrossRefGoogle Scholar
  60. Lunney D, Law B, Rummery C (1997) An ecological interpretation of the historical decline of the brush-tailed rock-wallaby P. penicillata in New South Wales. Aust Mammal 19:281–296Google Scholar
  61. Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  62. Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for Microsatellite Loci. Genetics 142:1061–1064PubMedPubMedCentralGoogle Scholar
  63. Mitchell KJ, Pratt RC, Watson LN et al (2014) Molecular phylogeny, biogeography, and habitat preference evolution of marsupials. Mol Biol Evol 31:2322–2330CrossRefPubMedGoogle Scholar
  64. Nogués-Bravo D, Rodríguez J, Hortal J, Batra P, Araújo MB (2008) Climate change, humans, and the extinction of the woolly mammoth. Plos Biol 6:e79CrossRefPubMedPubMedCentralGoogle Scholar
  65. O’Connell JF, Allen J (1998) When did humans first arrive in greater Australia and why is it important to know? Evol Anthropol 6, 132–146.CrossRefGoogle Scholar
  66. Peery MZ, Kirby R, Reid BN et al (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418CrossRefPubMedGoogle Scholar
  67. Petherick L, Bostock H, Cohen TJ et al (2013) Climatic records over the past 30 ka from temperate Australia—a synthesis from the Oz-INTIMATE workgroup. Quatern Sci Rev 74:58–77CrossRefGoogle Scholar
  68. Piggott MP, Banks SC, Stone N, Banffy C, Taylor AC (2006a) Estimating population size of endangered brush-tailed rock-wallaby (Petrogale penicillata) colonies using faecal DNA. Mol Ecol 15:81–91CrossRefPubMedGoogle Scholar
  69. Piggott MP, Banks SC, Taylor AC (2006b) Population structure of brush-tailed rock-wallaby (Petrogale penicillata) colonies inferred from analysis of faecal DNA. Mol Ecol 15:93–105CrossRefPubMedGoogle Scholar
  70. Potter S, Cooper SJ, Metcalfe CJ, Taggart DA, Eldridge MD (2012a) Phylogenetic relationships of rock-wallabies, Petrogale (Marsupialia: Macropodidae) and their biogeographic history within Australia. Mol Phylogenet Evol 62:640–652CrossRefPubMedGoogle Scholar
  71. Potter S, Eldridge MD, Taggart DA, Cooper SJ (2012b) Multiple biogeographical barriers identified across the monsoon tropics of northern Australia: phylogeographic analysis of the brachyotis group of rock-wallabies. Mol Ecol 21:2254–2269CrossRefPubMedGoogle Scholar
  72. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  73. Rambaut A, Drummond A (2012) Tracer v1. 5.. http://beast.bio.ed.ac.uk/Tracer.
  74. Rasmussen M, Guo X, Wang Y et al (2011) An aboriginal Australian genome reveals separate human dispersals into Asia. Science 334:94–98CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rees ABH, Cwynar LC, Fletcher M-S (2015) Southern westerly winds submit to the enso regime: a multiproxy paleohydrology record from Lake Dobson, Tasmania. Quatern Sci Rev 126:254–263CrossRefGoogle Scholar
  76. Rubin DB (1984) Bayesianly justifiable and relevant frequency calculations for the applied statistician. Ann Stat 12:1151–1172CrossRefGoogle Scholar
  77. Salmona J, Salamolard M, Fouillot D et al (2012) Signature of a pre-human population decline in the critically endangered Reunion Island endemic forest bird Coracina newtoni. PloS ONE 7:e43524CrossRefPubMedPubMedCentralGoogle Scholar
  78. Sandel B, Arge L, Dalsgaard B et al (2011) The influence of late Quaternary climate-change velocity on species endemism. Science 334:660–664CrossRefPubMedGoogle Scholar
  79. Short J (1982) Habitat requirements of the brush-tailed rock-wallaby, Petrogale penicillata, in New South Wales. Wildl Res 9:239–246CrossRefGoogle Scholar
  80. Short J, Milkovits G (1990) Distribution and status of the brush-tailed rock-wallaby in south-eastern Australia. Wildl Res 17:169–179CrossRefGoogle Scholar
  81. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedPubMedCentralGoogle Scholar
  82. Smith BJ (2007) BOA: An R package for MCMC output convergence assessment and posterior inference. J Stat Softw 21:1–37CrossRefGoogle Scholar
  83. Spencer PBS (1996) Coping with a naturally fragmented environment: a genetic and ecological study of the allied rock-wallaby, Petrogale assimilis. James Cook University of North Queensland, TownsvilleGoogle Scholar
  84. Spencer PBS, Odorico DM, Jones SJ, Marsh HD, Miller DJ (1995) Highly variable microsatellites in isolated colonies of the rock-wallaby (Petrogale assimilis). Mol Ecol 4:523–525CrossRefPubMedGoogle Scholar
  85. Spencer PBS, Adams M, Marsh H, Miller DJ, Eldridge MDB (1997) High levels of genetic variability in an isolated colony of rock-wallabies (Petrogale assimilis): evidence from three classes of molecular markers. Aust J Zool 45:199–210CrossRefGoogle Scholar
  86. Stiller M, Baryshnikov G, Bocherens H et al (2010) Withering away—25,000 years of genetic decline preceded cave bear extinction. Mol Biol Evol 27:975–978CrossRefPubMedGoogle Scholar
  87. Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evol Int J org Evol 56:154–166CrossRefGoogle Scholar
  88. Taggart D, Menkhorst P, Lunney D (2008) Petrogale penicillata. The IUCN Red List of Threatened Species. http://www.iucnredlist.org
  89. Taylor A, Cooper D (1998) A set of tammar wallaby (Macropus eugenii) microsatellites tested for genetic linkage. Mol Ecol 7:925CrossRefPubMedGoogle Scholar
  90. Telfer WR, Eldridge MDB (2010) High levels of mitochondrial DNA divergence within short-eared rock-wallaby (Petrogale brachyotis) populations in northern Australia. Aust J Zool 58:104–112CrossRefGoogle Scholar
  91. Thuiller W, Broennimann O, Hughes G et al (2006) Vulnerability of African mammals to anthropogenic climate change under conservative land transformation assumptions. Global Change Biol 12:424–440CrossRefGoogle Scholar
  92. 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 4:535–538CrossRefGoogle Scholar
  93. Wakeley J, Aliacar N (2001) Gene genealogies in a metapopulation. Genetics 159:893–905PubMedPubMedCentralGoogle Scholar
  94. Walther G-R, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefPubMedGoogle Scholar
  95. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedPubMedCentralGoogle Scholar
  96. Woinarski JCZ, Burbidge AA, Harrison PL (2015) Ongoing unraveling of a continental fauna: Decline and extinction of Australian mammals since European settlement. Proc Nat Acad Sci USA 112:4531–4540CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Anna Brüniche-Olsen
    • 1
    • 2
  • Stephanie L. Hazlitt
    • 3
  • Mark D. B. Eldridge
    • 4
  1. 1.School of Biological SciencesUniversity of TasmaniaHobartAustralia
  2. 2.Department of Forestry & Natural ResourcesPurdue UniversityWest LafayetteUSA
  3. 3.British Columbia Ministry of EnvironmentVictoriaCanada
  4. 4.Australian Museum Research InstituteAustralian MuseumSydneyAustralia

Personalised recommendations