Conservation Genetics

, Volume 15, Issue 5, pp 1085–1094 | Cite as

Persistence of a potentially rare mammalian genus (Wyulda) provides evidence for areas of evolutionary refugia within the Kimberley, Australia

  • Sally Potter
  • Dan Rosauer
  • J. Sean Doody
  • Myfanwy J. Webb
  • Mark D. B. Eldridge
Research Article

Abstract

Understanding the evolutionary and ecological processes that have shaped current patterns of biodiversity is crucial in the planning and implementation of broad scale conservation management. The temporal and spatial pattern of diversity across a landscape can help identify areas that have acted as climatically stable refugia historically, or do so currently. This has important implications for conservation efforts that try to maximise the evolutionary potential of species, as well as maintaining existing biodiversity. Northern Australia has recently reported catastrophic species decline, particularly in mammals, due to a series of threats. Here we apply an integrative approach utilising molecular analyses and spatial modelling to determine whether disjunct populations of a potentially rare, endemic mammal, the scaly-tailed possum (Wyulda squamicaudata) exhibit differentiation associated with biogeographic barriers or a recent decline. Significant but low genetic differentiation between the east and west Kimberley populations was detected. Principal component analyses indicate potential climatic niche differences that could support recent localised adaptations. Climatic reconstructions back to the last glacial maximum (LGM) indicate areas of suitable habitat have substantially shifted through time for W. squamicaudata and suggest multiple areas of refugia across the Kimberley since the LGM. Further comparative research is required to establish a biogeographical framework that will assist in our understanding of processes that have shaped biodiversity in northern Australia and assist in conservation planning.

Keywords

Wyulda squamicaudata mtDNA Northern Australia Conservation Genetics Refugia 

Supplementary material

10592_2014_601_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 82 kb)

References

  1. Alexander WB (1919) A new species of marsupial of the subfamily Phalangerinae. J R Soc West Aust 4:31–36Google Scholar
  2. Amante C, Eakins BW (2009) ETOPO1 1 arc-minute global relief model: procedures, data sources and analysis. NOAA Technical Memorandum NESDIS NGDC-24. http://www.ngdc.noaa.gov/mgg/global/global.html. Accessed 26 April 2012
  3. Blacket MJ, Adams M, Cooper SJB, Krajewski C, Westerman M (2001) Systematics and evolution of the Dasyurid marsupial genus Sminthopsis: I. The Macroura species group. J Mamm Evol 8:149–170Google Scholar
  4. Bouckaert R, Heled J, Kǖhnert D, Vaughan TG, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2013). BEAST2: a software platform for Bayesian evolutionary analysis. http://beast2.cs.auckland.ac.nz. Accessed 16 April 2013
  5. Bowman DMJS, Brown GK, Braby MF, Brown JR, Cook LG, Crisp MD, Ford F, Haberle S, Hughes J, Isagi Y, Joseph L, McBride J, Nelson G, Ladiges PY (2010) Biogeography of the Australian monsoon tropics. J Biogeogr 37:201–216CrossRefGoogle Scholar
  6. Burbidge AA, Webb MJ (2008) Scaly-tailed possum, Wyulda squamicaudata. In: Van Dyck S, Strahan R (eds) The mammals of Australia, 3rd edn. Reed New Holland, Sydney, pp 277–278Google Scholar
  7. Byrne M, Yeates DK, Joseph L, Kearney M, Bowler J, Williams MAJ, Cooper S, Donnellan SC, Keogh JS, Leys R, Melville J, Murphy DJ, Porch N, Wyrwoll K-H (2008) Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Mol Ecol 17:4398–4417PubMedCrossRefGoogle Scholar
  8. Byrne M, Steane DA, Joseph L, Yeates DK, Jordan GJ, Crayn D, Aplin K, Cantrill DJ, Cook LG, Crisp MD, Keogh JS, Melville J, Moritz C, Porch N, Sniderman JMK, Sunnucks P, Weston PH (2011) Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. J Biogeogr 38:1635–1656CrossRefGoogle Scholar
  9. Cadotte MC, Dinnage R, Tilman D (2012) Phylogenetic diversity promotes ecosystem stability. Ecology 93:223–233CrossRefGoogle Scholar
  10. Cassens I, Mardulyn P, Milinkovitch MC (2005) Evaluating intraspecific “network” construction methods using simulated sequence data: do existing algorithms outperform the global maximum parsimony approach? Syst Biol 54:363–372PubMedCrossRefGoogle Scholar
  11. Catullo RA, Lanfear R, Doughty P, Keogh JS (2013) The biogeographical boundaries of northern Australia: evidence from ecological niche models and a multi-locus phylogeny of Uperoleia toadlets (Anura: Myobatrachidae). J Biogeogr 41:659–672CrossRefGoogle Scholar
  12. Cracraft J (1991) Patterns of diversification within continental biotas: hierarchical congruence among areas of endemism of Australian vertebrates. Aust Syst Bot 4:211–227CrossRefGoogle Scholar
  13. Department of Environment and Conservation Western Australia (2013) Threatened and priority fauna rankings. Department of Environment and Conservation Western Australia, SydneyGoogle Scholar
  14. Doody JS, Rhind D, Castellano CM, Bass M (2012) Rediscovery of the scaly-tailed possum (Wyulda squamicaudata) in the eastern Kimberley. Aust Mamm 34:260–262CrossRefGoogle Scholar
  15. Doughty P (2011) An emerging frog diversity hotspot in the northwest Kimberley of Western Australia: another new frog species from the high rainfall zone. Rec West Aust Mus 26:209–216Google Scholar
  16. Eldridge MDB, Potter S, Cooper SJB (2012) Biogeographic barriers in north-western Australia: an overview and standardization of nomenclature. Aust J Zool 59:270–272CrossRefGoogle Scholar
  17. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50Google Scholar
  18. Fitzsimons J, Legge S, Traill B, Woinarski J (2010) Into oblivion: the disappearing mammals of northern Australia. The Nature Conservancy, Melbourne. http://wildaustralia.org/science/oblivion-disappearing-mammals-northern-australia. Accessed 3 Sep 2011
  19. Flannery T, Archer M, Maynes G (1987) The phylogenetic relationships of living phalangerids (Phalangeroidea: Marsupialia) with a suggested new taxonomy. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty & the Royal Zoological Society of New South Wales, Sydney, pp 477–506Google Scholar
  20. Flannery T (1994) Possums of the world. A monograph of the Phalangeroidea. GEO Productions, SydneyGoogle Scholar
  21. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedPubMedCentralGoogle Scholar
  22. Fuchs R, Herold M, Verburg PH, Clevers JGPW (2013) A high-resolution and harmonized model approach for reconstructing and analysing historic land changes in Europe. Biogeosciences 10:1543–1559CrossRefGoogle Scholar
  23. Fujita MK, McGuire JA, Donnellan SC, Moritz C (2010) Diversification and persistence at the arid-monsoonal interface: Australia-wide biogeography of the Bynoe’s gecko (Heteronotia binoei; Geckkonidae). Evolution 64:2293–2314PubMedGoogle Scholar
  24. Fumagalli L, Pope LC, Taberlet P, Moritz C (1997) Versatile primers for the amplification of the mitochondrial DNA control region in marsupials. Mol Ecol 6:1199–1201Google Scholar
  25. Geneious version (6.0.5) created by Biomatters. http://www.geneious.com/. Accessed 12 Dec 2012
  26. Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174PubMedCrossRefGoogle Scholar
  27. Houlder DJ, Hutchinson MF, Nix HA, McMahon JP (2000) ANUCLIM User Guide, Version 5.1. Centre for Resource and Environmental Studies, Australian National University, CanberraGoogle Scholar
  28. Huelsenbeck JP, Ronquist F (2005) Bayesian analysis of molecular evolution using MrBayes. In: Nielsen R (ed) Statistical methods in molecular evolution. Springer, New York, pp 183–232CrossRefGoogle Scholar
  29. Humphreys WF, How RA, Bradley J, Kemper CM, Kitchener DJ (1984) The biology of Wyulda squamicaudata, Alexander 1919. In: Smith AP, Hume ID (eds) Possums and gliders. Surrey Beatty, Sydney, pp 162–169Google Scholar
  30. Jennings WB, Edwards SV (2005) Speciational history of Australian grass finches (Poephila) inferred from thirty gene trees. Evolution 59:2033–2047PubMedGoogle Scholar
  31. Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut AGT, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr 21:393–404CrossRefGoogle Scholar
  32. Kerle JA (2001) Possums: the brushtails, ringtails, and greater glider. University of New South Wales Press Ltd., SydneyGoogle Scholar
  33. Klein C, Wilson K, Watts M, Stein J, Berry S, Carwardine J, Stafford Smith J, Mackey B, Possingham H (2009) Incorporating ecological and evolutionary processes into continental-scale conservation planning. Ecol Appl 19:206–217PubMedCrossRefGoogle Scholar
  34. Köhler F (2010) Uncovering local endemism in the Kimberley, Western Australia: description of new species of the genus Amplirhagada Iredale, 1933 (Pulmonata: camaenidae). Rec Aust Mus 62:217–284CrossRefGoogle Scholar
  35. Köhler F (2011) Descriptions of new species of the diverse and endemic land snail Amplirhagada Iredale, 1933 from the rainforest patches across the Kimberley, Western Australia (Pulmonata: camaenidae). Rec Aust Mus 63:167–202CrossRefGoogle Scholar
  36. Legge S, Murphy S, Heathcote J, Flaxman E, Augusteyn J, Crossman M (2008) The short-term effects of an extensive and high-intensity fire on vertebrates in the tropical savannas of the central Kimberley, northern Australia. Wildl Res 35:33–43CrossRefGoogle Scholar
  37. Legge S, Kennedy MS, Lloyd R, Murphy SA, Fisher A (2011) Rapid recovery of mammal fauna in the central Kimberley, northern Australia, following the removal of introduced herbivores. Austral Ecol 36:791–799CrossRefGoogle Scholar
  38. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  39. Mackey BG, Watson JEM, Hope G, Gilmore S (2008) Climate change, biodiversity conservation, and the role of protected areas: an Australian perspective. Biodiversity 9:11–18CrossRefGoogle Scholar
  40. McKnight M (2008) Wyulda squamicaudata. In: IUCN 2013. IUCN red list of threatened species. Version 2013.1. http://www.iucnredlist.org. Accessed 2 Sep 2013
  41. Melville J, Ritchie EG, Chapple SNJ, Glor RE, Schulte JA (2011) Evolutionary origins and diversification of dragon lizards in Australia’s tropical savannas. Mol Phylogenet Evol 58:257–270PubMedCrossRefGoogle Scholar
  42. Meredith RW, Westerman M, Springer MS (2008) A phylogeny and timescale for the living genera of kangaroos and kin (Macropodiformes: marsupialia) based on nuclear DNA sequences. Aust J Zool 56:395–410CrossRefGoogle Scholar
  43. Moritz C, Ens EJ, Potter S, Catullo R (2013) The Australian monsoonal tropics: an opportunity to protect unique biodiversity and secure benefits for aboriginal communities. Pac Conserv Biol 19:343–355Google Scholar
  44. Oliver PM, Adams M, Doughty P (2010) Molecular evidence for ten species and Oligo-Miocene vicariance within a nominal Australian gecko species (Crenadactylus ocellatus, Diplodactylidae). BMC Evol Biol 10:386–396PubMedCrossRefPubMedCentralGoogle Scholar
  45. Oliver PM, Doughty P, Palmer R (2012) Hidden biodiversity in rare northern Australian vertebrates: the case of the clawless geckos (Crenadactylus, Diplodactylidae) of the Kimberley. Wildl Res 39:429–435CrossRefGoogle Scholar
  46. Osborne MJ, Christidis L (2001) Molecular phylogenetics of Australo-Papuan possums and gliders (family Petauridae). Mol Phylogenet Evol 20:211–224PubMedCrossRefGoogle Scholar
  47. Osborne MJ, Christidis L (2002) Molecular relationships of the cuscuses, brushtail and scaly-tailed possums (Phalangerinae). Aust J Zool 50:135–149CrossRefGoogle Scholar
  48. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  49. Potter S, Eldridge MDB, Taggart DA, Cooper SJB (2012) Multiple biogeographic barriers identified across the monsoon tropics of northern Australia: phylogeographic analysis of the brachyotis group of rock-wallabies. Mol Ecol 21:2254–2269PubMedCrossRefGoogle Scholar
  50. Rambaut A, Drummond AJ (2009) Tracer v1.5, http://beast.bio.ed.ac.uk/Tracer. Accessed 17 April 2013
  51. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100PubMedCrossRefGoogle Scholar
  52. Ronquist F, Huelsenbeck JP (2003) MrBayes3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  53. Rosauer D, Laffan SW, Crisp MD, Donnellan SC, Cook LG (2009) Phylogenetic endemism: a new approach for identifying geographical concentrations of evolutionary history. Mol Ecol 18:4061–4072PubMedCrossRefGoogle Scholar
  54. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  55. Runcie MJ (1999) Movements, dens and feeding behaviour of the tropical scaly-tailed possum (Wyulda squamicaudata). Wildl Res 26:367–373CrossRefGoogle Scholar
  56. Russell-Smith J, Lucas DE, Brock J, Bowman DMJS (1993) Allosyncarpia-dominated rain forest in monsoonal northern Australia. J Veg Sci 4:67–82CrossRefGoogle Scholar
  57. Singarayer JS, Valdes PJ (2010) High-latitude climate sensitivity to ice-sheet forcing over the last 120 kyr. Quat Sci Rev 29:43–55CrossRefGoogle Scholar
  58. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedCrossRefGoogle Scholar
  59. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 57:758–771PubMedCrossRefGoogle Scholar
  60. 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 13:510–524PubMedCrossRefGoogle Scholar
  61. Swofford D (2002) PAUP*. 4.0b, 10th edn. Sinauer Associates Inc., SunderlandGoogle Scholar
  62. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  63. Toon A, Hughes JM, Joseph L (2010) Multilocus analysis of honeyeaters (Aves: meliphagidae) highlights spatio-temporal heterogeneity in the influence of biogeographic barriers in the Australian monsoonal zone. Mol Ecol 19:2980–2994PubMedCrossRefGoogle Scholar
  64. VanDerWal J, Falconi L, Januchowski S, Shoo LP, Storlie C (2012) SDMTools: species distribution modelling tools: tools for processing data associated with species distribution modelling exercises. R package version 1.1–13. http://cran.r-project.org/package=SDMTools. Accessed 1 June 2010
  65. Wheeler D, Hope R, Cooper SJB, Dolman G, Webb GC, Bottema CDK, Gooley AA, Goodman M, Holland RAB (2001a) An orphaned mammalian [beta]-globin gene of ancient evolutionary origin. Proc Natl Acad Sci USA 98:1101–1106PubMedCrossRefPubMedCentralGoogle Scholar
  66. Wheeler D, Hope R, Cooper SJB, Gooley AA, Holland RAB (2001b) An orphaned mammalian b-globin gene of ancient evolutionary origin. Proc Natl Acad Sci USA 98:1101–1106PubMedCrossRefPubMedCentralGoogle Scholar
  67. Woinarski JCZ, Mackey B, Nix H, Traill B (2007) The nature of northern Australia: natural values, ecological processes and future prospects. ANU E Press, CanberraGoogle Scholar
  68. Woinarski JCZ, Legge S, Fitzsimons JA, Traill BJ, Burbidge AA, Fisher A, Firth RSC, Gordon IJ, Griffiths AD, Johnson CN, McKenzie NL, Palmer C, Radford I, Rankmore B, Ritchie EG, Ward S, Ziembicki M (2011) The disappearing mammal fauna of northern Australia: context, cause and response. Conserv Lett 4:192–201CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Sally Potter
    • 1
    • 2
  • Dan Rosauer
    • 1
  • J. Sean Doody
    • 3
  • Myfanwy J. Webb
    • 4
  • Mark D. B. Eldridge
    • 2
  1. 1.Research School of BiologyAustralian National UniversityCanberraAustralia
  2. 2.Australian Museum Research InstituteAustralian MuseumSydneyAustralia
  3. 3.School of Environmental and Life SciencesThe University of NewcastleCallaghanAustralia
  4. 4.MacMasters BeachAustralia

Personalised recommendations