Genetic variation and structuring in the threatened koala populations of Southeast Queensland

Abstract

Habitat fragmentation can act to cause reproductive isolation between conspecifics and undermine species’ persistence, though most studies have reported the genetic condition of populations that have already declined to a very small size. We examined genetic diversity within the vulnerable, declining koala (Phascolarctos cinereus) population in Southeast Queensland, Australia to determine the genetic impact of ongoing threatening processes. Five hundred and twelve koalas from ten Southeast Queensland Local Government Areas on the mainland and one island were genotyped at six polymorphic microsatellite loci. Based on Bayesian cluster analysis incorporating spatial data, the regional koala population was subdivided into six clusters, with location of major roads and rivers appearing to be consistent with being barriers to gene flow. The distribution of mtDNA control region haplotypes identified distinct coastal and inland clades suggesting that historically there was gene flow between koalas along the coast (though little interchange between coastal and inland animals). In contrast, koalas from the Koala Coast (Brisbane City, Logan City and Redland Shire) were shown by microsatellite analysis to be genetically distinct from adjacent areas. It is likely, therefore, that more recent reductions in population size and restricted gene flow through urbanisation have contributed to the genetic differentiation of koalas in the Koala Coast region.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Aguilar A, Jessup DA, Estes J, Garza JC (2008) The distribution of nuclear genetic variation and historical demography of sea otters. Anim Conserv 11:35–45

    Article  Google Scholar 

  2. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) genetix 4.03, logiciel ous Windows pour la genetique des populations. Laboratoire Genome et Populations. Universite deMontpellier II, Montpellier

  3. Carrick FN (1996) A review of disease in Koalas. In: Gordon G (ed) Koalas–research for management—proceedings of the Brisbane Koala symposium. World Koala Research Incorporated, Brisbane, pp 37–41

    Google Scholar 

  4. Carrick FN (2004) Koala coast protection plan. Report prepared for the premier of Queensland. The University of Queensland Koala Study Program on behalf of the Koala Conservation Council Inc., p 24

  5. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate genealogies. Mol Ecol 9(10):1657–1660

    CAS  Article  PubMed  Google Scholar 

  6. Cristescu R, Cahill V, Sherwin WB, Handasyde K, Carlyon K, Whisson D, Herbert CA, Carlsson BLJ, Wilton AN, Cooper DW (2009) Inbreeding and testicular abnormalities in a bottlenecked population of koalas (Phascolarctos cinereus). Wildlife Res 36:1–10

    Article  Google Scholar 

  7. Dique DS, Preece HJ, Thompson J, de Villiers DL (2004) Determining the distribution and abundance of a regional koala population in South-east Queensland for conservation management. Wildlife Res 31:109–117

    Article  Google Scholar 

  8. Dixon JD, Oli MK, Wooten MC, Eason TH, McCown JW, Cunningham MW (2007) Genetic consequences of habitat fragmentation and loss: the case of the Florida black bear (Ursus americanus floridanus). Conserv Genet 8:455–464

    Article  Google Scholar 

  9. 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(3):531–541

    Article  Google Scholar 

  10. Ellis WAH, Girjes AA, Carrick FN, Melzer A (1993) Chlamydial infection in koalas under relatively little alienation pressure. Aust Vet J 70:427–428

    CAS  Article  PubMed  Google Scholar 

  11. Ellis WA, Hale PT, Carrick FN (2002) Breeding dynamics of koalas in open woodlands. Wildlife Res 29:19–25

    Article  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  13. Fowler EV, Houlden BA, Hoeben P, Timms P (2000) Genetic diversity and gene flow among Southeastern Queensland koalas (Phascolarctos cinereus). Mol Ecol 9:155–164

    CAS  Article  PubMed  Google Scholar 

  14. Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327

    Article  PubMed  Google Scholar 

  15. Frankham R, Ballou J, Briscoe D (2002) Introduction to conservation genetics. Cambridge University Press, New York, p 640

    Google Scholar 

  16. Girjes A, Hugall A, Timms P, Lavin M (1988) Two distinct forms of Chlamydia psittaci associated with disease and infertility in Phascolarctos cinereus (koala). Infect Immun 56(8):1897–1900

    CAS  PubMed  Google Scholar 

  17. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html

  18. Guillot G, Mortier F, Estoup A (2005) geneland: a computer package for landscape genetics. Mol Ecol 5:712–715

    CAS  Article  Google Scholar 

  19. Hazlitt SL, Goldizen AW, Eldridge MDB (2006) 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

    CAS  Article  Google Scholar 

  20. Houlden BA, England P, Sherwin WB (1996a) Paternity exclusion in koalas (Phascolarctos cinereus) using hypervariable microsatellites. JHered 87:149–152

    CAS  Google Scholar 

  21. Houlden BA, England PR, Taylor AC, Greville WD, Sherwin WB (1996b) Low genetic variability of the Koala Phascolarctos cinereus in south-eastern Australia following a severe population bottleneck. Mol Ecol 5:269–281

    CAS  PubMed  Google Scholar 

  22. 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 of the Koala. Mol Ecol 8:999–1011

    CAS  Article  PubMed  Google Scholar 

  23. IUCN (1987) Translocation of living organisms. http://www.iucnsscrsg.org/download/IUCNPositionStatement.pdf. Accessed on 13 Jan 2009

  24. Lacy RC (1988) A report on population genetics in conservation. Conserv Biol 2:245–247

    Article  Google Scholar 

  25. Lawson VJ, Carrick FN (1998) Morphology of the thyroid in coastal and non-coastal populations of the Koala (Phascolarctos cinereus) in Queensland. Gen Comp Endocr 110:295–306

    CAS  Article  PubMed  Google Scholar 

  26. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  27. Moritz C, Geffen HE, McRae P (1997) Genetic population structure of the Greater Bilby Macrotis lagotis, a marsupial in decline. Mol Ecol 6:925–936

    CAS  Article  PubMed  Google Scholar 

  28. Nattrass AEO, Fiedler KB (1996) Koala rescue–the perception and the reality. In: Gordon G (ed) Koalas–research for management–proceedings of the Brisbane Koala symposium. World Koala Research Incorporated, Brisbane, pp 129–136

    Google Scholar 

  29. Nei M (1987) Molecular evolutionary genetics. New York, Columbia University Press

    Google Scholar 

  30. Noël S, Ouellet M, Galois P, Lapointe F (2007) Impact of urban fragmentation on the genetic structure of the eastern red-backed salamander. Conserv Genet 8:599–606

    Article  Google Scholar 

  31. Noss RF, Copperrider AY (1994) Saving nature’s legacy. Island Press, Washington

    Google Scholar 

  32. O’Brien SJ, Evermann JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 3:254–259

    Article  Google Scholar 

  33. O’Brien SJ, Roelke ME, Marker L et al (1985) Genetic basis for species vulnerability in the Cheetah. Science 227:1428–1434

    Article  PubMed  Google Scholar 

  34. Peakall R, Smouse P (2006) GENALEX6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  35. Phillips B (1990) Koalas. The little Australians we’d all hate to lose. AGPS Press, Canberra

    Google Scholar 

  36. Preece H (2007) Monitoring and modelling threats to koala populations in rapidly urbanising landscapes: Koala Coast, South East Queensland, Australia. PhD Thesis. The University of Queensland

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

    CAS  PubMed  Google Scholar 

  38. Queensland Government (2006) Nature conservation (Koala) conservation plan 2006 and management program 2006–2016. Queensland Environmental Protection Agency, Brisbane

    Google Scholar 

  39. Queensland Government (2007) Report on Koala Coast Koala surveys 2005–2006. Queensland Environmental Protection Agency, Brisbane

    Google Scholar 

  40. Queensland Government (2009) Decline of the Koala Coast Koala population: population status in 2008. Department of Environment and Resource Management, Brisbane

    Google Scholar 

  41. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  42. Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452

    Article  Google Scholar 

  43. Segelbacher G, Hoglund J, Storch I (2003) From connectivity to isolation: genetic consequences of population fragmentation in Capercaillie across Europe. Mol Ecol 12:1773–1780

    CAS  Article  PubMed  Google Scholar 

  44. Sherwin WB, Timms P, Wilcken J, Houlden B (2000) Analysis and implications of koala genetics. Conserv Biol 14(3):639–649

    Article  Google Scholar 

  45. Simberloff D (1994) Habitat fragmentation and extinction by birds. Ibis 137:105–111

    Article  Google Scholar 

  46. Sloss CR, Murray-Wallace CV, Jones BJ (2006) Holocene sea-level change on the southeast coast of Australia: a review. The Holocene 17(7):999–1014

    Article  Google Scholar 

  47. Thompson J (2006) The comparative ecology and population dynamics of koalas in the Koala Coast region of South-East Queensland. PhD Thesis. The University of Queensland

  48. Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and extinction debt. Nature 371:65–66

    Article  Google Scholar 

  49. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley PF (2003) Micro-checker version 2.2.3 University of Hull. Available from http://www.microchecker.hull.ac.uk/. Accessed on 18 Oct 2007

  50. Vos CC, Antonisse-De Jong AG, Goedhart PW, Smulders MJM (2001) Genetic similarity as a measure for connectivity between fragmented populations of the moor frog (Rana arvalis). Heredity 86:598–608

    CAS  Article  PubMed  Google Scholar 

  51. Weigler B, Girjes A, White N et al (1988) Aspects of the epidemiology of Chlamydia psittaci infection in a population of Koalas (Phascolarctos cinereus) in southeastern Queensland, Australia. J Wildlife Dis 24(2):282–291

    CAS  Google Scholar 

  52. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370

    Article  Google Scholar 

Download references

Acknowledgments

This project was funded by an Australian Research Council Linkage Grant, LP0455785. Thanks to Camryn Allen for providing samples from Burbank and Greg Simmons for sharing Gold Coast samples collected by Steve Phillips. David Pavlacky provided assistance with ArcGIS and Simon Blomberg assisted with performing statistical analyses. Thanks to staff of Queensland Parks and Wildlife Service Moggill Koala Hospital and Australian Wildlife Hospital for collecting samples. Thanks to Cynthia Riginos and the genetics discussion group and two anonymous reviewers for helpful feedback and suggestions.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Kristen E. Lee.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lee, K.E., Seddon, J.M., Corley, S.W. et al. Genetic variation and structuring in the threatened koala populations of Southeast Queensland. Conserv Genet 11, 2091–2103 (2010). https://doi.org/10.1007/s10592-009-9987-9

Download citation

Keywords

  • Koalas
  • Habitat fragmentation
  • Mitochondrial DNA
  • Microsatellites
  • Genetic isolation
  • Island population