Skip to main content

Advertisement

SpringerLink
Log in

Threatened populations of the Australian squirrel glider (Petaurus norfolcensis) show evidence of evolutionary distinctiveness on a Late Pleistocene timescale

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The squirrel glider Petaurus norfolcensis occurs across a broad Australian latitudinal range that includes gaps in distribution and potential biogeographic barriers, creating the potential for evolution of distinct entities within this species. Because of the species’ threatened status in the southern part of its range, we tested for the presence of geographically based independent evolutionary units among gliders sampled from southern, and northern coastal populations, using sequences of mitochondrial cytochrome b DNA (mtDNA) and a set of five nuclear microsatellites in 258 individuals. Our analyses suggest that an initial northward colonisation in the early- to mid-Pleistocene was followed by isolation by distance and, eventually, divergence between the sampled coastal and southern populations in the mid- to late-Pleistocene. We propose that the previously large and diverse southern populations have declined coincidentally with the replacement of wet forests by open sclerophyll woodlands during the preceding few million years. By contrast coastal populations further north appear to have been expanding and at present have an effective population size several times greater than southern populations. These results suggest that the two forms are on different evolutionary trajectories and should be treated separately for conservation purposes. It is highly desirable that loss of southern populations be prevented to maintain the unique genetic diversity accumulated over a considerable evolutionary timescale.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahern L, van der Ree R (2003) Squirrel Glider Petaurus norfolcensis. Action Statement No 166. Department of Sustainability and Environment

  • Ashton KG, Tracy MC, de Queiroz A (2000) Is Bergmann’s rule valid for mammals? Am Nat 156:390–415

    Article  Google Scholar 

  • Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    CAS  PubMed  Google Scholar 

  • Barrows TT, Stone JO, Fifield LK, Cresswell RG (2001) Late Pleistocene glaciation of the Kosciuszko Massif, Snowy Mountains, Australia. Q Res 55:179–189

    Article  CAS  Google Scholar 

  • Barrows TB, Stone JO, Fifield LK, Cresswell RG (2002) The timing of the Last Glacial Maximum in Australia. Q Sci Rev 21:159–173

    Article  Google Scholar 

  • Barrows TT, Stone JO, Fifield LK (2004) Exposure ages for Pleistocene periglacial deposits in Australia. Q Sci Rev 23:697–708

    Article  Google Scholar 

  • Bininda-Emonds ORP (2007) Fast genes and slow clades: comparative rates of molecular evolution in mammals. Evol Bioinform 3:59–85

    CAS  Google Scholar 

  • Bowler JM (1982) Aridity in the late tertiary and quaternary of Australia. In: Barker WR, Greenslade PJM (eds) Evolution of the flora and fauna of arid Australia. Peacock Publications, Frewville, pp 35–45

    Google Scholar 

  • Brown M, Kendal TA, Cooksley H, Saint KM, Taylor AC, Carthew SM, Cooper SJB (2004) Polymorphic microsatellite markers for the gliding marsupials Petaurus australis and Petaurus breviceps. Mol Ecol Notes 4:704–706

    Article  CAS  Google Scholar 

  • Brown M, Cooksley H, Carthew SM, Cooper SJB (2006) Conservation units and phylogeographic structure of an arboreal marsupial, the yellow-bellied glider (Petaurus australis). Aust J Zool 54:305–317

    Article  Google Scholar 

  • Claridge AW, van der Ree R (2004) Recovering endangered populations in fragmented landscapes: the squirrel glider Petaurus norfolcensis on the south-west slopes of New South Wales. In: Lunney D (ed) Conservation of Australia’s forest fauna, 2nd edn. Royal Zoological Society of New South Wales, Mosman, New South Wales, Australia, pp 678–687

    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  PubMed  Google Scholar 

  • Drummond A, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  Google Scholar 

  • Drummond AJ, Nicholls G, Rodrigo A, Solomon W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307–1320

    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  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed  Google Scholar 

  • Eyre TJ (2004) Distribution and conservation status of the possums and gliders of southern Queensland. In: Goldingay RL, Jackson SM (eds) The biology of Australian possums and gliders. Surrey Beatty and Sons, Chipping Norton, pp 1–25

    Google Scholar 

  • Frakes LA, McGowran B, Bowler JM (1987) Evolution of Australian environments. In: Dyne GR, Walton DW (eds) Fauna of Australia, vol 1A. Australian Government Publishing Service, Canberra

    Google Scholar 

  • Frankel OH, Soulé ME (1981) Conservation and evolution. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    CAS  PubMed  Google Scholar 

  • Gibbons P, Lindenmayer DB (2002) Tree hollows and wildlife conservation in Australia. CSIRO Publishing, Melbourne

    Google Scholar 

  • Hansen B, Harley D, Lindenmayer D, 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 

  • Hardy OJ, Vekemans X (2002) Spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hardy OJ, Charbonnel N, Freville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482

    CAS  PubMed  Google Scholar 

  • Heatwole H (1987) Major components and distributions of the terrestrial fauna. In: Dyne GR, Walton DW (eds) Fauna of Australia, vol 1A. Australian Government Publishing Service, Canberra

    Google Scholar 

  • Hestbeck SB (1982) Population regulation in cyclic mammals: the social fence hypothesis. Oikos 39:157–163

    Article  Google Scholar 

  • Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790

    Article  CAS  PubMed  Google Scholar 

  • Houlden BA, Costello BH, Sharkey D, Fowler EV, Melzer A, Ellis W, Carrick F, Baverstock PR, Elphinstone MS (1999) Phylogeographic differentiation in the mitochondrial control region in the koala, Phascolarctos cinereus (Goldfuss 1817). Mol Ecol 8:999–1011

    Article  CAS  PubMed  Google Scholar 

  • Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144

    Article  CAS  PubMed  Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13

    Article  PubMed  Google Scholar 

  • Joseph L, Moritz C (1994) Mitochondrial DNA phylogeography of birds in eastern Australian rainforests: first fragments. Aust J Zool 42:385–403

    Article  CAS  Google Scholar 

  • Joseph L, Moritz C, Hugall A (1993) A mitochondrial perspective on the historical biogeography of mideastern Queensland rainforest birds. Mem Queensl Mus 34:201–214

    Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200

    Article  CAS  PubMed  Google Scholar 

  • Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on the coalescent. Genetics 149:429–434

    CAS  PubMed  Google Scholar 

  • Lee AK, Cockburn A (1985) Evolutionary ecology of marsupials. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Lessa EP, Cook JA, Patton JL (2003) Genetic footprints of demographic expansion in North America, but not Amazonia, during the Late Quaternary. Proc Natl Acad Sci USA 100:10331–10334

    Article  CAS  PubMed  Google Scholar 

  • Mace GM (2004) The role of taxonomy in species conservation. Philos Trans R Soc Lond B 359:711–719

    Article  Google Scholar 

  • Malekian M, Cooper SJB, Norman JA, Christidis L, Carthew SM (2009) Molecular systematics and evolutionary origins of the genus Petaurus (Marsupialia: Petauridae) in Australia and New Guinea. Mol Phylogenet Evol 54:122–135

    Article  PubMed  Google Scholar 

  • Markgraf V, McGlone M, Hope G (1995) Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems—a southern perspective. Trends Ecol Evol 10:143–147

    Article  Google Scholar 

  • McGlashan DJ, Hughes JM (2002) Extensive genetic divergence among populations of the Australian freshwater fish, Pseudomugil signifer (Pseudomugilidae), at different hierarchical scales. Mar Freshw Res 53:1–11

    Article  Google Scholar 

  • McKechnie SW, Blacket MJ, Song SV, Rako L, Carroll X, Johnson TK, Jensen LT, Lee SF, Wee CW, Hoffmann AA (2010) A clinally varying promoter polymorphism associated with adaptive variation in wing size in Drosophila. Mol Ecol 19:775–784

    Article  CAS  PubMed  Google Scholar 

  • Menkhorst PW, Weavers BW, Alexander JSA (1988) Distribution, habitat and conservation status of the squirrel glider Petaurus norfolcensis (Petauridae, Marsupialia) in Victoria. Aust Wildl Res 15:59–71

    Article  Google Scholar 

  • Millis AL (2000) Isolation and characterization of microsatellite loci in marsupial gliders (Petaurus norfolcensis, P. breviceps and P. gracilis). Mol Ecol 9:1661–1686

    Article  Google Scholar 

  • Moritz C (1994) Defining “evolutionary significant units” for conservation. Trends Ecol Evol 9:373–375

    Article  Google Scholar 

  • Nabholz B, Mauffrey JF, Bazin E, Galtier N, Glemin S (2008) Determination of mitochondrial genetic diversity in mammals. Genetics 178:351–361

    Article  PubMed  Google Scholar 

  • Nicholls JA, Austin JJ (2005) Phylogeography of an east Australian wet-forest bird, the satin bowerbird (Ptilonorhynchus violaceus), derived from mtDNA, and its relationship to morphology. Mol Ecol 14:1485–1496

    Article  CAS  PubMed  Google Scholar 

  • Pope L, Storch D, Adams M, Moritz C, Gordon G (2001) A phylogeny for the genus Isoodon and a range extension for I. obesulus peninsulae based on mtDNA control region and morphology. Aust J Zool 49:411–434

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Wen W (2003) Documentation for Structure Software, Version 2. Department of Human Genetics, University of Chicago, USA

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Quin DG, Smith AP, Norton TW (1996) Eco-geographic variation in size and sexual dimorphism in sugar gliders and squirrel gliders (Marsupialia: Petauridae). Aust J Zool 44:19–45

    Article  Google Scholar 

  • Rambaut A (2006) FigTree. http://tree.bio.ed.ac.uk/software/figtree

  • Rambaut A, Drummond AJ (2007) Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    CAS  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumenicism. Heredity 86:248–249

    Google Scholar 

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

    Article  Google Scholar 

  • Rozas J, Sánchez DelBarrio JC, Messeguer X, Rozas R (2003) Dnasp, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10

    Article  Google Scholar 

  • Strahan R (1995) The mammals of Australia. Reed Books, Sydney

    Google Scholar 

  • Strasburg JL, Rieseberg LH (2010) How robust are “isolation with migration” analyses to violations of the im model? A simulation study. Mol Biol Evol 27:297–310

    Article  CAS  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

    CAS  PubMed  Google Scholar 

  • Sunnucks P, Wilson ACC, Beheregaray LB, Zenger K, French J, Taylor AC (2000) SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. Mol Ecol 9:1699–1710

    Article  CAS  PubMed  Google Scholar 

  • Symula R, Keogh JS, Cannatella DC (2008) Ancient phylogeographic divergence in southeastern Australia among populations of the widespread common froglet, Crinia signifera. Mol Phylogenet Evol 47:569–580

    Article  CAS  PubMed  Google Scholar 

  • Taylor AC, Foulkes J (2004) Molecules and morphology: a taxonomic analysis of the common brushtail possum Trichosurus vulpecula, with an emphasis on the central Australian form. In: Goldingay R, Jackson SM (eds) The biology of Australian possums and gliders. Southern Cross University Press, Lismore

    Google Scholar 

  • van der Ree R (2002) The population ecology of the squirrel glider (Petaurus norfolcensis) within a network of remnant linear habitats. Wildl Res 29:329–340

    Article  Google Scholar 

  • van der Ree R, Suckling GC (2008) The squirrel glider. In: van Dyck S, Strahan R (eds) Mammals of Australia. New Holland Publishers, Sydney, pp 235–236

    Google Scholar 

  • van der Ree R, Harper MJ, Crane M (2006) Longevity in wild populations of the squirrel glider Petaurus norfolcensis. Aust Mammal 28:239–242

    Google Scholar 

  • Van Dyck S, Strahan R (eds) (2008) The mammals of Australia, 3rd edn. New Holland Publishers, Sydney

    Google Scholar 

  • Waples RS (1991) Pacific Salmon, Oncorhynchus spp. and the definition of ‘species’ under the endangered species act. Mar Fish Rev 53:11–22

    Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276

    Article  CAS  PubMed  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    CAS  PubMed  Google Scholar 

  • Zhang D-X, Hewitt GM (1996) Nuclear integrations: challenges for mitochondrial DNA markers. Trends Ecol Evol 11:247–251

    Article  Google Scholar 

Download references

Acknowledgments

We thank Tina Ball (Environmental Protection Agency, QLD), David Sharpe (Southern Cross University), Steve Cooper and Mansooreh Malekian (South Australian Museum), Leo Joseph and Robert Palmer (Australian National Wildlife Collection), Steve Van Dyck and Heather Janetzki (Queensland Museum), Ray Thomas (Helmeted Honeyeater Project) and members of other landcare groups, for making genetic samples available to us. This manuscript has been greatly improved from discussions with Paul Sunnucks and his comments on the draft, and by the comments of two anonymous reviewers. Part of this work was carried out using the resources of the Computational Biology Service Unit from Cornell University, which is partially funded by Microsoft Corporation. Fiona Caryl produced the map for Fig. 1. We thank the Monash University School of Biological Sciences, Norman Wettenhall Foundation, Brisbane City Council, former versions of the NSW Department of Environment and Climate Change, the Victorian Department of Sustainability and Environment, The Baker Foundation and the M.A. Ingram Trust, for funding.

Author information

Author notes

  1. Faith M. Walker

    Present address: Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, 86011, USA

Authors and Affiliations

  1. School of Biological Sciences, Australian Centre for Biodiversity, Monash University, Clayton, VIC, 3800, Australia

    Alexandra Pavlova, Faith M. Walker, Silvana Cesarini & Andrea C. Taylor

  2. Australian Research Centre for Urban Ecology, Royal Botanic Gardens Melbourne, School of Botany, University of Melbourne, Melbourne, VIC, 3010, Australia

    Rodney van der Ree

Authors
  1. Alexandra Pavlova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Faith M. Walker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rodney van der Ree
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Silvana Cesarini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrea C. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexandra Pavlova.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pavlova, A., Walker, F.M., van der Ree, R. et al. Threatened populations of the Australian squirrel glider (Petaurus norfolcensis) show evidence of evolutionary distinctiveness on a Late Pleistocene timescale. Conserv Genet 11, 2393–2407 (2010). https://doi.org/10.1007/s10592-010-0125-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-010-0125-5

Keywords

Search

Navigation