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Significant patterns of population genetic structure and limited gene flow in a threatened macropodid marsupial despite continuous habitat in southeast Queensland, Australia

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Abstract

Many endangered species worldwide are found in remnant populations, often within fragmented landscapes. However, when possible, an understanding of the natural extent of population structure and dispersal behaviour of threatened species would assist in their conservation and management. The brush-tailed rock-wallaby (Petrogale penicillata), a once abundant and widespread rock-wallaby species across southeastern Australia, has become nearly extinct across much of the southern part of its range. However, the northern part of the species’ range still sustains many small colonies closely distributed across suitable habitat, providing a rare opportunity to investigate the natural population dynamics of a listed threatened species. We used 12 microsatellite markers to investigate genetic diversity, population structure and gene flow among brush-tailed rock-wallaby colonies within and among two valley regions with continuous habitat in southeast Queensland. We documented high and significant levels of population genetic structure between rock-wallaby colonies embedded in continuous escarpment habitat and forest. We found a strong and significant pattern of isolation-by-distance among colonies indicating restricted gene flow over a small geographic scale ( <10 km) and conclude that gene flow is more likely limited by intrinsic factors rather than environmental factors. In addition, we provide evidence that genetic diversity was significantly lower in colonies located in a more isolated valley region compared to colonies located in a valley region surrounded by continuous habitat. These findings shed light on the processes that have resulted in the endangered status of rock-wallaby species in Australia and they have strong implications for the conservation and management of both the remaining ‘connected’8 brush-tailed rock-wallaby colonies in the northern parts of the species’8 range and the remnant endangered populations in the south.

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References

  • Browning TL, Taggart DA, Rummery C, Close RL, Eldridge MDB (2001) Multifaceted genetic analysis of the “Critically Endangered” brush-tailed rock-wallaby Petrogale penicillata in Victoria, Australia: Implications for management. Conserv. Genet. 2:145–156

    Article  CAS  Google Scholar 

  • Carter K, Goldizen AW (2003) Habitat choice and vigilance behaviour of brush-tailed rock-wallabies (Petrogale penicillata) within their nocturnal foraging ranges. Wildl. Res. 30:355–364

    Article  Google Scholar 

  • Cegelski CC, Waits LP, Anderson NJ (2003) Assessing population structure and gene flow in Montana wolverines (Gulo gulo) using assignment-based approaches. Mol. Ecol. 12:2907–2918

    Article  PubMed  CAS  Google Scholar 

  • Clancy TF, Close RL (1997) The Queensland rock-wallabies – an overview of their conservation status, threats and management. Aust. Mammal. 19:169–174

    Google Scholar 

  • Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000

    PubMed  CAS  Google Scholar 

  • Danley PD, Markert JA, Arnegard ME, Kocher TD (2000) Divergence with gene flow in the rock-dwelling cichlids of Lake Malawi. Evolution 54:1725–1737

    Article  PubMed  CAS  Google Scholar 

  • Department of Environment and Conservation NSW (2005) Draft Recovery Plan for the Brush-tailed Rock-wallaby Petrogale penicillata. DEC, Sydney

  • Dieckmann U, O’8Hara B, Weisser W (1999) The evolutionary ecology of dispersal. Trends Ecol. Evol. 14:88–90

    Article  Google Scholar 

  • Dovey L, Wong V, Bayne P (1997) An overview of the status and management of rock-wallabies (Petrogale) in New South Wales. Aust. Mammal. 19, 163–168

    Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree Argania spinosa (L) Skeels endemic to Morocco. Theor. Appl. Genet. 92:832–839

    Article  Google Scholar 

  • Eldridge MDB, Kinnear JE, Onus ML (2001) Source population of dispersing rock-wallabies (Petrogale lateralis) identified by assignment tests on multilocus genotypic data. Mol. Ecol. 10:2847–2876

    Google Scholar 

  • Eldridge MDB, Rummery C, Bray C, Zenger KR, Browning TL, Close RL (2004) Genetic analysis of a population crash in brush-tailed rock-wallabies (Petrogale penicillata) from Jenolan Caves, south-eastern Australia. Wildl. Res. 31:229–240

    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 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1993) PHYLIP. University of Washington, Seattlefs, WA

    Google Scholar 

  • Frankham R, J.D. B, Briscoe DA (2002) Introduction to Conservation Genetics. Cambridge University Press, Cambridge

    Google Scholar 

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

    Google Scholar 

  • Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim. Behav. 28:1140–1162

    Article  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  PubMed  CAS  Google Scholar 

  • Hanski I (2001) Population dynamic consequences of dispersal in local populations and in metapopulations. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) Dispersal. Oxford University Press, New York, pp 283–298

    Google Scholar 

  • Hazlitt SL, Eldridge MDB, Goldizen AW (2004) Fine-scale spatial genetic correlation analyses reveal strong female philopatry within a brush-tailed rock-wallaby colony in southeast Queensland. Mol. Ecol. 13:3621–3632

    Article  PubMed  CAS  Google Scholar 

  • Hoffman JI, Amos W (2005) Microsatellite genoty** errors: detection approaches, common sources and consequences for paternal exclusion. Mol. Ecol. 14:599–612

    Article  PubMed  CAS  Google Scholar 

  • Hood GM (2003) PopTools version 2.6.2. Available on the internet. URL http://www.cse.csiro.au/poptools/

  • Jarman PJ, Bayne P (1997) Behavioural ecology of Petrogale pencillata in relation to conservation. Aust. Mammal. 19:219–228

    Google Scholar 

  • Kraaijeveld-Smit FJL, Lindenmayer DB, Taylor AC (2002) Dispersal patterns and population structure in a small marsupial, Antechinus agilis, from two forests analysed using microsatellite markers. Aust. J. Zool. 50:325–338

    Article  Google Scholar 

  • Laws RJ, Goldizen AW (2003) Nocturnal home ranges and social interactions of the brush-tailed rock-wallaby Petrogale penicillata at Hurdle Creek, Queensland. Aust. Mammal. 25:169–176

    Google Scholar 

  • Lim TL, Giles JR (1987) Studies on the yellow-footed rock-wallaby, Petrogale xanthropus Gray (Marsupalia: Macropodidae) III. Distribution and management in Western New South Wales. Aust. Wildl. Res. 14:147–161

    Article  Google Scholar 

  • Lowe A, Harris S, Ashton P (2004) Ecological Genetics: Design, Analysis, and Application. Blackwell Science Ltd., Oxford

    Google Scholar 

  • Lunney D, Law B, Rummery C (1997) An ecological interpretation of the historical decline of the Brush-tailed Rock-wallaby Petrogale penicillata in New South Wales. Aust. Mammal. 19:281–296

    Google Scholar 

  • Manel S, Berthier P, Luikart G (2002) Detecting wildlife poaching: identifying the origin of individuals with Bayesian assignment tests and multilocus genotypes. Conserv. Biol. 16:650–659

    Article  Google Scholar 

  • Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol. Evol. 20:136–142

    Article  PubMed  Google Scholar 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics 3. Genic homozygosity in populations which experience periodic bottlenecks. Genetics 111:691–703

    PubMed  CAS  Google Scholar 

  • McCallum HI (1997) Rock-wallaby biology and management: synthesis and directions for future research. Aust. Mammal. 19:319–324

    Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) Bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol. Ecol. 4:347–354

    PubMed  CAS  Google Scholar 

  • Page RD (1996) TreeView: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357–358

    PubMed  CAS  Google Scholar 

  • Pearse DE, Crandall KA (2004) Beyond F ST: Analysis of population genetic data for conservation. Conserv. Genet. 5:585–602

    Article  CAS  Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: A software for genetic assignment and first-generation migrant detection. J. Hered. 95:536–539

    Article  PubMed  CAS  Google Scholar 

  • Poole WE, Catling PC (1974) Reproduction in two species of grey kangaroos, Macropus giganteus (Shaw) and Macropus fuliginosus (Desmarest) 1. Sexual maturity and estrus. Aust. J. Zool. 22:277–302

    Article  PubMed  CAS  Google Scholar 

  • Pope LC, Sharp A, Moritz C (1996) Population structure of the yellow-footed rock-wallaby Petrogale xanthopus (Gray, 1854) inferred from mtDNA sequences and microsatellite loci. Mol. Ecol. 5:629–640

    PubMed  CAS  Google Scholar 

  • Pope LC, Estoup A, Moritz C (2000) Phylogeography and population structure of an ecotonal marsupial, Bettongia tropica, determined using mtDNA and microsatellites. Mol. Ecol. 9:2041–2053

    Article  PubMed  CAS  Google Scholar 

  • Pope LC, Blair D, Johnson CN (2005) Dispersal and population structure of the rufous bettong,Aepyprymnus rufescens (Marsupialia : Potoroidae). Austral. Ecol. 30:572–580

    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 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rossiter SJ, Jones G, Ransome RD, Barrattt EM (2000) Genetic variation and population structure in the endangered greater horseshoe bat Rhinolophus ferrumequinum. Mol. Ecol. 9:1131–1135

    Article  PubMed  CAS  Google Scholar 

  • Sharp A (1997) Insights into the dispersal patterns of yellow-footed rock-wallabies, Petrogale xanthopus. Aust. Mammal. 19:229–238

    Google Scholar 

  • Short J (1990) Distribution and status of the brush-tailed rock-wallaby in south-eastern Australia. Aust. Wildl. Res. 17:169–180

    Article  Google Scholar 

  • Short J, Smith A (1994) Mammal decline and recovery in Australia. J. Mammal. 75:288–297

    Article  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 

  • Smith JNM, Hellmann JJ (2002) Population persistence in fragmented landscapes. Trends Ecol. Evol. 17:397–399

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the Principles and Practice of Statistics in Biological Research. W.H. Freeman & Co., New York

    Google Scholar 

  • Strahan R (eds) (1995) The Mammals of Australia. Reed Books, Australia

    Google Scholar 

  • Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol. Evol. 15:199–203

    Article  PubMed  Google Scholar 

  • Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol. Biol. Evol. 13:510–524

    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

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Yeh FC, Yang R-C, Boyle TJB, Ye Z-H, Mao JX (1997) POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada. Available at URL http://www.ualberta.ca/∼ ∼fyeh/

  • Zenger KR, Eldridge MDB, Cooper DW (2003) Intraspecific variation, sex-biased dispersal and phylogeography of the eastern grey kangaroo (Macropus giganteus). Heredity 91:153–162

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank all the private land owners for access to their properties and we are indebted to D. Sigg, J. Carter, K. Carter, R. Laws, N. Wynd, T. Barnes and numerous volunteers for help with trap** and field work over the course of this study. We are grateful to Queensland Parks and Wildlife Service and the Toowoomba City Council, including R. Laws, G. Maags, G. Lundi-Jenkins, P. Johnson, R. Hobson, M. Ready and N. Hyslop for in-kind support and samples. In particular, we wish to thank J. Rayner for help with fieldwork and for his local knowledge of rock-wallabies. We are indebted to the School of Integrative Biology Molecular Zoology and Gene Flow Labs for help with the molecular work, and D. Sigg, J. Nicholls, W. Telfer, P. Macqueen and two anonymous reviewers for constructive criticisms on earlier drafts of this manuscript. This study was approved by the University of Queensland Animal Ethics Committee and the Queensland Parks and Wildlife Service (Scientific Purposes Permit # W4/002560/00/SAA). This research was funded by the Australian Research Council, the National Geographic Society, the Norman Wettenhall Foundation, the University of Queensland and the Australian Commonwealth.

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Correspondence to Stephanie L. Hazlitt.

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Hazlitt, S.L., Goldizen, A.W. & Eldridge, M.D.B. 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 (2006). https://doi.org/10.1007/s10592-005-9101-x

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