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

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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.

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References

  • Act E (1999) Environment Protection and Biodiversity Conservation Act 1999 (Cth)

  • 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 111:4922–4927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 41:1402–1413

    Article  Google Scholar 

  • Attenbrow V (1982) Archaeological Investigation of Deep Creek Shelter, Mangrove Creek Dam. Unpublished report to NSW National Parks and Wildlife Service

  • Barnosky AD, Koch PL, Feranec RS, Wing SL, Shabel AB (2004) Assessing the causes of late Pleistocene extinctions on the continents. Science 306:70–75

    Article  CAS  PubMed  Google Scholar 

  • Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345

    Article  CAS  PubMed  Google Scholar 

  • 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 98:4563–4568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326

    Article  PubMed  PubMed Central  Google Scholar 

  • Blois JL, McGuire JL, Hadly EA (2010) Small mammal diversity loss in response to late-Pleistocene climatic change. Nature 465:771–774

    Article  CAS  PubMed  Google Scholar 

  • Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83

    Article  CAS  PubMed  Google Scholar 

  • Bradshaw CJA (2012) Little left to lose: deforestation and forest degradation in Australia since European colonization. J Plant Ecol 5:109–120

    Article  Google Scholar 

  • Brook BW, Sodhi NS, Bradshaw CJA (2008) Synergies among extinction drivers under global change. Trends Ecol Evol 23:453–460

    Article  PubMed  Google Scholar 

  • Brooks SP, Gelman A (1998) General methods for monitoring convergence of iterative simulations. J Comput Gr Stat 7:434–455

    Google Scholar 

  • 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 10:20140619

    Article  PubMed  PubMed Central  Google Scholar 

  • Byrne M (2008) Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quatern Sci Rev 27:2576–2585

    Article  Google Scholar 

  • 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 186:983–995

    Article  PubMed  PubMed Central  Google Scholar 

  • Colhoun EA, Shimeld PW (2012) Late-Quaternary vegetation history of Tasmania from pollen records. Peopled Landsc 34:29

    Google Scholar 

  • Cooper A, Turney C, Hughen KA et al (2015) Abrupt warming events drove late pleistocene holarctic megafaunal turnover. Science 349:602–606

    Article  CAS  PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):1187–1189

    Article  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  CAS  PubMed  Google Scholar 

  • 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 11:1043–1049

    Article  Google Scholar 

  • Davis MB, Shaw RG (2001) Range shifts and adaptive responses to quaternary climate change. Science 292:673–679

    Article  CAS  PubMed  Google Scholar 

  • DECC (2008) Recovery plan for the brush-tailed rock-wallaby (Petrogale penicillata) (ed. Department of Environment and Climate Change S, New South Wales.), Sydney

    Google Scholar 

  • Diggle PJ, Gratton RJ (1984) Monte Carlo methods of inference for implicit statistical models. J R Stat Soc 193–227

  • Duncan RP, Blackburn TM, Worthy TH (2002) Prehistoric bird extinctions and human hunting. Proc R Soc Lond B 269:517–521

    Article  Google Scholar 

  • 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, Sydney

    Google Scholar 

  • 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, Barcelona

    Google Scholar 

  • 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 13:531–541

    Article  Google Scholar 

  • 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 10:2867–2876

    Article  CAS  PubMed  Google Scholar 

  • Ellegren H (2004) Microsatellites: Simple sequences with complex evolution. Nat Rev Genet 5:435–445

    Article  CAS  PubMed  Google Scholar 

  • 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 14:854–860

    Article  CAS  PubMed  Google Scholar 

  • Estoup A, Jarne P, Cornuet J (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604

    Article  CAS  PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frankham R (1995) Effective population size adult population size ratios in wildlife—a review. Genet Res 66:95–107

    Article  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 

  • 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):165–179

    Google Scholar 

  • Gollan K (1984) The Australian dingo: in the shadow of man. Vertebrate Zoogeography Evolu Aust, 921–927

  • Goossens B, Chikhi L, Ancrenaz M et al (2006) Genetic signature of anthropogenic population collapse in orang-utans. Plos Biology 4:e25

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 18:3346–3362

    Article  CAS  PubMed  Google Scholar 

  • 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 7:675–689

    Article  CAS  Google Scholar 

  • 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 15:2997–3007

    Article  CAS  PubMed  Google Scholar 

  • Hazlitt SL, Eldridge MDB, Goldizen AW (2010) Strong matrilineal structuring in the brush-tailed rock-wallaby confirmed by spatial patterns of mitochondrial DNA. Macropods 87–95

  • 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 4:1102–1116

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 17:4845–4858

    Article  CAS  PubMed  Google Scholar 

  • Hing S, Narayan E, Thompson RCA, Godfrey S (2014) A review of factors influencing the stress response in Australian marsupials. Conserv Physiol 2:cou027

    Article  PubMed  PubMed Central  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Jeffreys H (1998) The theory of probability. Oxford University Press, Oxford

  • Johnson C (2006) Australia’s mammal extinctions: a 50000 year history. Cambridge University Press, Cambridge

  • Johnson CN, Letnic M (2013) Introducing a new top predator, the dingo. Invas Biol Ecol Theor 414

  • Johnson CN, Wroe S (2003) Causes of extinction of vertebrates during the Holocene of mainland Australia: arrival of the dingo, or human impact? Holocene 13:941–948

    Article  Google Scholar 

  • Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795

    Article  Google Scholar 

  • Kumar S, Subramanian S (2002) Mutation rates in mammalian genomes. Proc Nat Acad Sci USA 99:803–808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 33:152–161

    Article  Google Scholar 

  • 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 15:3847–3880

    Article  Google Scholar 

  • Lorenzen ED, Nogues-Bravo D, Orlando L et al (2011) Species-specific responses of late quaternary megafauna to climate and humans. Nature 479:359–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lourandos H (1997) Continent of hunter-gatherers: new perspectives in Australian prehistory. Cambridge University Press, Cambridge

  • 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 23:373–379

    Article  Google Scholar 

  • 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 19:281–296

    Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for Microsatellite Loci. Genetics 142:1061–1064

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchell KJ, Pratt RC, Watson LN et al (2014) Molecular phylogeny, biogeography, and habitat preference evolution of marsupials. Mol Biol Evol 31:2322–2330

    Article  CAS  PubMed  Google Scholar 

  • 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:e79

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Peery MZ, Kirby R, Reid BN et al (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

    Article  PubMed  Google Scholar 

  • 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 74:58–77

    Article  Google Scholar 

  • 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 15:81–91

    Article  CAS  PubMed  Google Scholar 

  • 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 15:93–105

    Article  CAS  PubMed  Google Scholar 

  • 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 62:640–652

    Article  PubMed  Google Scholar 

  • 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 21:2254–2269

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut A, Drummond A (2012) Tracer v1. 5.. http://beast.bio.ed.ac.uk/Tracer.

  • Rasmussen M, Guo X, Wang Y et al (2011) An aboriginal Australian genome reveals separate human dispersals into Asia. Science 334:94–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 126:254–263

    Article  Google Scholar 

  • Rubin DB (1984) Bayesianly justifiable and relevant frequency calculations for the applied statistician. Ann Stat 12:1151–1172

    Article  Google Scholar 

  • 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:e43524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandel B, Arge L, Dalsgaard B et al (2011) The influence of late Quaternary climate-change velocity on species endemism. Science 334:660–664

    Article  CAS  PubMed  Google Scholar 

  • Short J (1982) Habitat requirements of the brush-tailed rock-wallaby, Petrogale penicillata, in New South Wales. Wildl Res 9:239–246

    Article  Google Scholar 

  • Short J, Milkovits G (1990) Distribution and status of the brush-tailed rock-wallaby in south-eastern Australia. Wildl Res 17:169–179

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith BJ (2007) BOA: An R package for MCMC output convergence assessment and posterior inference. J Stat Softw 21:1–37

    Article  Google Scholar 

  • 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, Townsville

    Google Scholar 

  • 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 4:523–525

    Article  CAS  PubMed  Google Scholar 

  • 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 45:199–210

    Article  Google Scholar 

  • Stiller M, Baryshnikov G, Bocherens H et al (2010) Withering away—25,000 years of genetic decline preceded cave bear extinction. Mol Biol Evol 27:975–978

    Article  CAS  PubMed  Google Scholar 

  • 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 56:154–166

    Article  CAS  Google Scholar 

  • Taggart D, Menkhorst P, Lunney D (2008) Petrogale penicillata. The IUCN Red List of Threatened Species. http://www.iucnredlist.org

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

    Article  CAS  PubMed  Google Scholar 

  • 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 58:104–112

    Article  Google Scholar 

  • 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 12:424–440

    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  Google Scholar 

  • Wakeley J, Aliacar N (2001) Gene genealogies in a metapopulation. Genetics 159:893–905

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walther G-R, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  CAS  PubMed  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  PubMed Central  Google Scholar 

  • 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 112:4531–4540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Brüniche-Olsen, A., Hazlitt, S.L. & Eldridge, M.D.B. Genetic evidence of range-wide population declines in an Australian marsupial prior to European settlement. Conserv Genet 18, 1077–1089 (2017). https://doi.org/10.1007/s10592-017-0960-8

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