Genetic diversity in natural and introduced island populations of koalas in Queensland
Kristen E. Lee A , Jennifer M. Seddon B , Stephen Johnston C , Sean I. FitzGibbon A , Frank Carrick A , Alistair Melzer D , Fred Bercovitch E and William Ellis A D F
+ Author Affiliations
- Author Affiliations
A Centre for Mined Land Rehabilitation, The University of Queensland, Brisbane, Qld 4072, Australia.
B School of Veterinary Science, The University of Queensland, Gatton, Qld 4343, Australia.
C School of Animal and Food Science, The University of Queensland, Gatton, Qld 4343, Australia.
D Central Queensland University, Centre for Environmental Management, Rockhampton, Qld 4700, Australia.
E Primate Research Institute and Wildlife Research Center, Kyoto University, 41-2 Kanrin Inuyama, Aichi 484-8506, Japan.
F Corresponding author. Email: w.ellis@uq.edu.au
Australian Journal of Zoology 60(5) 303-310 https://doi.org/10.1071/ZO12075
Submitted: 9 August 2012 Accepted: 16 January 2013 Published: 8 February 2013
Abstract
Island populations of animals are expected to show reduced genetic variation and increased incidence of inbreeding because of founder effects and the susceptibility of small populations to the effects of genetic drift. Koalas (Phascolarctos cinereus) occur naturally in a patchy distribution across much of the eastern Australian mainland and on a small number of islands near the Australian coast. We compared the genetic diversity of the naturally occurring population of koalas on North Stradbroke Island in south-east Queensland with other island populations including the introduced group on St Bees Island in central Queensland. The population on St Bees Island shows higher diversity (allelic richness 4.1, He = 0.67) than the North Stradbroke Island population (allelic richness 3.2, He = 0.55). Koalas on Brampton, Newry and Rabbit Islands possessed microsatellite alleles that were not identified from St Bees Island koalas, indicating that it is most unlikely that these populations were established by a sole secondary introduction from St Bees Island. Mitochondrial haplotypes on the central Queensland islands were more similar to a haplotype found at Springsure in central Queensland and the inland clades in south-east Queensland, rather than the coastal clade in south-east Queensland.
References
Allendorf, F. W., and Leary, R. F. (1986). Heterozygosity and fitness in natural populations of animals. In ‘Conservation Biology: The Science of Scarcity and Diversity’. (Ed. M. E. Soule.) pp. 57–76. (Sinauer: Sunderland, MA.)Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., and Bonhomme, F. (2004). GENETIX 4.03, logiciel ous Windows pour la genetique des populations Laboratoire Genome et Populations. Universite deMontpellier II. http://kimura.univ-montp2.fr/genetix/
Berck, L. (1995). ‘St. Bees Island: Its History, Life-styles and Tales.’ (Booralong: Brisbane.)
Cork, S. J., Clark, T. W., and Mazur, N. (2000). Conclusions and recommendations for koala conservation. Conservation Biology 14, 702–704.
Cristescu, R., Cahill, V., Handasyde, K., Carlyon, K., Whisson, D., Johnson, G., Herbert, C., Wilton, A. N., Carlsson, B. L. J., and Cooper, D. (2009). Inbreeding and testicular abnormalities in a bottlenecked population of koalas, Phascolarctos cinereus. Wildlife Research 36, 299–308.
| Inbreeding and testicular abnormalities in a bottlenecked population of koalas, Phascolarctos cinereus.Crossref | GoogleScholarGoogle Scholar |
Cristescu, R., Ellis, W., de Villiers, D., Lee, K. E., Woosnam-Merchez, O., Frere, C., Banks, P., Dique, D., Hodgkison, S., Carrick, H., Carter, D., Smith, P., and Carrick, F. (2012). North Stradbroke Island: an island ark for Queensland’s koala population? Proceedings of the Royal Society of Queensland 2012, 309–334.
Eldridge, M. D. B., King, J. M., Loupis, A. K., Spencer, P. B. S., Taylor, A. C., Pope, L. C., and Hall, G. P. (1999). Unprecedented low levels of genetic variation and inbreeding depression in an island population of the black-footed rock wallaby. Conservation Biology 13, 531–541.
| Unprecedented low levels of genetic variation and inbreeding depression in an island population of the black-footed rock wallaby.Crossref | GoogleScholarGoogle Scholar |
Eldridge, M., Kinnear, J., Zenger, K., McKenzie, L., and Spencer, P. (2004). Genetic diversity in remnant mainland and “pristine” island populations of three endemic Australian macropodids (Marsupialia): Macropus eugenii, Lagorchestes hirsutus, Petrogale lateralis. Conservation Genetics 5, 325–338.
| Genetic diversity in remnant mainland and “pristine” island populations of three endemic Australian macropodids (Marsupialia): Macropus eugenii, Lagorchestes hirsutus, Petrogale lateralis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks1KnsbY%3D&md5=f8060e1211da0228eeeae80128d543c5CAS |
Ellis, W. A. H., Girjes, A. A., Carrick, F. N., and Melzer, A. (1993). Chlamydial infection in koalas under relatively little alienation pressure. Australian Veterinary Journal 70, 427–428.
| Chlamydial infection in koalas under relatively little alienation pressure.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7gslWqsA%3D%3D&md5=4da78ae18e59c1b7414c48eaff115218CAS |
Ellis, W., Melzer, A., Green, B., Newgrain, K., Hindell, M. A., and Carrick, F. N. (1995). Seasonal variation in water flux, field metabolic rate and food consumption of free-ranging koalas (Phascolarctos cinereus). Australian Journal of Zoology 43, 59–68.
| Seasonal variation in water flux, field metabolic rate and food consumption of free-ranging koalas (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar |
Ellis, W., Hale, P., and Carrick, F. (2002). Breeding dynamics of koalas in open woodlands. Wildlife Research 29, 19–25.
| Breeding dynamics of koalas in open woodlands.Crossref | GoogleScholarGoogle Scholar |
Ellis, W., Melzer, A., and Bercovitch, F. B. (2009). Spatiotemporal dynamics of habitat use by koalas: the checkerboard model. Behavioral Ecology and Sociobiology 63, 1181–1188.
| Spatiotemporal dynamics of habitat use by koalas: the checkerboard model.Crossref | GoogleScholarGoogle Scholar |
Fowler, E. V., Houlden, B. A., Hoeben, P., and Timms, P. (2000). Genetic diversity and gene flow among southeastern Queensland koalas (Phascolarctos cinereus). Molecular Ecology 9, 155–164.
| Genetic diversity and gene flow among southeastern Queensland koalas (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvF2ku7Y%3D&md5=77301a83d5a975e347b1e60dc450de06CAS |
Frankel, O. H., and Soule, M. E. (1981). ‘Conservation and Evolution.’ (Cambridge University Press: Cambridge.)
Frankham, R. (1997). Do island populations have less genetic variation than mainland populations? Heredity 78, 311–327.
| Do island populations have less genetic variation than mainland populations?Crossref | GoogleScholarGoogle Scholar |
Genever, M., Grindrod, J., and Barker, B. (2003). Holocene palynology of Whitehaven Swamp, Whitsunday Island, Queensland, and implications for the regional archaeological record. Palaeogeography, Palaeoclimatology, Palaeoecology 201, 141–156.
| Holocene palynology of Whitehaven Swamp, Whitsunday Island, Queensland, and implications for the regional archaeological record.Crossref | GoogleScholarGoogle Scholar |
Goudet, J. (2001). FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html
Houlden, B. A., England, P. R., Taylor, A. C., Greville, W. D., and Sherwin, W. B. (1996). Low genetic variability of the koala Phascolarctos cinereus in south-eastern Australia following a severe population bottleneck. Molecular Ecology 5, 269–281.
| 1:STN:280:DyaK283jvFKnsA%3D%3D&md5=c635b24e74265f770844d6639e7e71ceCAS |
Houlden, B. A., Costello, B. H., Sharkey, D., Fowler, E. V., Melzer, A., Ellis, W., Carrick, F., Baverstock, P. R., and Elphinstone, M. S. (1999). Phylogeographic differentiation in the mitochondrial control region in the koala, Phascolarctos cinereus (Goldfuss 1817). Molecular Ecology 8, 999–1011.
| Phylogeographic differentiation in the mitochondrial control region in the koala, Phascolarctos cinereus (Goldfuss 1817).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVOns7c%3D&md5=1a46632d5d055b9ad393a4f308b58acfCAS |
Jackson, S. (2007). ‘Koala: Origins of an Icon.’ (Allen & Unwin: Sydney.)
Kemp, J. (2009). Vegetation survey and mapping of St Bees Island. A report for the Queensland Parks and Wildlife Service. Queensland Herbarium, Brisbane.
Lee, K. E., Seddon, J. M., Corley, S. W., Ellis, W. A. H., Johnston, S. D., de Villiers, D. L., Preece, H. J., and Carrick, F. N. (2010). Genetic variation and structuring in the threatened koala populations of southeast Queensland. Conservation Genetics 11, 2091–2103.
| Genetic variation and structuring in the threatened koala populations of southeast Queensland.Crossref | GoogleScholarGoogle Scholar |
Lee, K. E., Ellis, W. A. H., Carrick, F. N., Corley, S. W., Johnston, S. D., Baverstock, P. R., Nock, C. J., Rowe, K. C., and Seddon, J. M. (2012). Anthropogenic changes to the landscape resulted in colonization of koalas in north-east New South Wales, Australia. Austral Ecology , .
| Anthropogenic changes to the landscape resulted in colonization of koalas in north-east New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |
Lee, T., Zenger, K. R., Close, R. L., Jones, M., and Phalen, D. N. (2010). Defining spatial genetic structure and management units for vulnerable koala (Phascolarctos cinereus) populations in the Sydney region. Wildlife Research 37, 156–165.
| Defining spatial genetic structure and management units for vulnerable koala (Phascolarctos cinereus) populations in the Sydney region.Crossref | GoogleScholarGoogle Scholar |
Lee, T., Zenger, K. R., Close, R. L., and Phalen, D. N. (2012). Genetic analysis reveals a distinct and highly diverse koala (Phascolarctos cinereus) population in South Gippsland, Victoria, Australia. Australian Mammalogy 34, 68–74.
| Genetic analysis reveals a distinct and highly diverse koala (Phascolarctos cinereus) population in South Gippsland, Victoria, Australia.Crossref | GoogleScholarGoogle Scholar |
Lunney, D., Phillips, S., Callaghan, J., and Coburn, D. (1998). Determining the distribution of koala habitat across a shire as a basis for conservation: a case study from Port Stephens, New South Wales. Pacific Conservation Biology 4, 186–196.
Lunney, D., Matthews, A., Moon, C., and Ferrier, S. (2000). Incorporating habitat mapping into practical koala conservation on private lands. Conservation Biology 14, 669–680.
| Incorporating habitat mapping into practical koala conservation on private lands.Crossref | GoogleScholarGoogle Scholar |
Martin, R., and Handasyde, K. A. (1999). ‘The Koala: Natural History, Conservation and Management.’ (UNSW Press: Sydney.)
Masters, P., Duka, T., Berris, S., and Moss, G. (2004). Koalas on Kangaroo Island: from introduction to pest status in less than a century. Wildlife Research 31, 267–272.
| Koalas on Kangaroo Island: from introduction to pest status in less than a century.Crossref | GoogleScholarGoogle Scholar |
Melzer, A., and Ellis, W. A. (2009). Integrating research and conservation land management – a case study from koala research in St Bees Island National Park. Australasian Journal of Environmental Management 16, 236–241.
| Integrating research and conservation land management – a case study from koala research in St Bees Island National Park.Crossref | GoogleScholarGoogle Scholar |
Melzer, A., Carrick, F., Menkhorst, P., Lunney, D., and StJohn, B. (2000). Overview, critical assessment, and conservation implications of koala distribution and abundance. Conservation Biology 14, 619–628.
| Overview, critical assessment, and conservation implications of koala distribution and abundance.Crossref | GoogleScholarGoogle Scholar |
Melzer, A., Tucker, G., Hodgson, J., and Elliott, B. (2003). A note on predation on koalas Phascolarctos cinereus by raptors, including wedge-tailed eagles Aquila audax, in Queensland. Queensland Naturalist 41, 38–41.
Mills, H., Moro, D., and Spencer, P. (2004). Conservation significance of island versus mainland populations: a case study of dibblers (Parantechinus apicalis) in Western Australia. Animal Conservation 7, 387–395.
| Conservation significance of island versus mainland populations: a case study of dibblers (Parantechinus apicalis) in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Nei, M (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.
| 1:STN:280:DC%2BC3crpt1Kqtg%3D%3D&md5=da465cc5ae44d5269c3173231ed79f4eCAS |
O’Brien, S. J., and Evermann, J. F. (1988). Interactive influence of infectious disease and genetic diversity in natural populations. Trends in Ecology & Evolution 3, 254–259.
| Interactive influence of infectious disease and genetic diversity in natural populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7gvFehuw%3D%3D&md5=813246c9e49614b46ecdbe9be158c44fCAS |
O’Brien, S. J., Roelke, M. E., Marker, L., Newman, A., Winkler, C. A., Meltzer, D., Colly, L., Evermann, J. F., Bush, M., and Wildt, D. E. (1985). Genetic basis for species vulnerability in the cheetah. Science 227, 1428–1434.
| Genetic basis for species vulnerability in the cheetah.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M7kt1Wmtg%3D%3D&md5=9e7921b80a9649c7ecc0d9ac833f2f24CAS |
Peakall, R., and Smouse, P. (2006). GENALEX6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
| GENALEX6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Penn, A. M., Sherwin, W. B., Gordon, G., Lunney, D., Melzer, A., and Lacy, R. C. (2000). Demographic forecasting in koala conservation. Conservation Biology 14, 629–638.
| Demographic forecasting in koala conservation.Crossref | GoogleScholarGoogle Scholar |
Phillips, S. S. (2000). Population trends and the koala conservation debate. Conservation Biology 14, 650–659.
| Population trends and the koala conservation debate.Crossref | GoogleScholarGoogle Scholar |
Raymond, M., and Rousset, F. (1995). GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. The Journal of Heredity 86, 248–249.
Robinson, A. C., and Bergin, T. J. (1978). The koala in South Australia. In ‘The Koala: Taronga Symposium on Koala Biology, Management and Medicine’. (Ed. T. Bergin.) pp. 132–143. (Zoological Parks Board of NSW: Sydney.)
Seymour, A. M., Montgomery, M. E., Costello, B. H., Ihle, S., Johnsson, G., St John, B., Taggart, D., and Houlden, B. A. (2001). High effective inbreeding coefficients correlate with morphological abnormalities in populations of South Australian koalas (Phascolarctos cinereus). Animal Conservation 4, 211–219.
| High effective inbreeding coefficients correlate with morphological abnormalities in populations of South Australian koalas (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar |
Sherwin, W. B., Timms, P., Wilcken, J., and Houlden, B. A. (2000). Analysis and conservation implications of koala genetics. Conservation Biology 14, 639–649.
| Analysis and conservation implications of koala genetics.Crossref | GoogleScholarGoogle Scholar |
Sloss, C., Murray-Wallace, C., and Jones, B. (2007). Holocene sea-level change on the southeast coast of Australia: a review. The Holocene 17, 999–1014.
| Holocene sea-level change on the southeast coast of Australia: a review.Crossref | GoogleScholarGoogle Scholar |
Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.
| MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrsL8%3D&md5=84a0ff55abf979eff10629c4167bfb20CAS |
Taylor, A. C., Graves, J. M., Murray, N. D., O’Brien, S. J., Yuhki, N, and Sherwin, B. (1997). Conservation genetics of the koala (Phascolarctos cinereus), low mitochondrial DNA variation amongst southern Australian populations. Genetical Research 69, 25–33.
| Conservation genetics of the koala (Phascolarctos cinereus), low mitochondrial DNA variation amongst southern Australian populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjvVOksLo%3D&md5=d1605d35679c388e55939a5775cb363cCAS |
Templeton, A. R., and Read, B (1984). Factors eliminating inbreeding depression in a captive herd of Speke’s Gazelle (Gazella spekei). Zoo Biology 3, 177–199.
van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. F. (2003). Micro-Checker Version 2.2.3. University of Hull. http://www.microchecker.hull.ac.uk/
Weir, B. S., and Cockerham, C. C.. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.
| Estimating F-statistics for the analysis of population structure.Crossref | GoogleScholarGoogle Scholar |
Whisson, D. A., Holland, G. J., and Carlyon, K. (2012). Translocation of overabundant species: implications for translocated individuals. Journal of Wildlife Management 76, 1661–1669.
| Translocation of overabundant species: implications for translocated individuals.Crossref | GoogleScholarGoogle Scholar |
Woodward, W., Ellis, W. A., Carrick, F. N., Tanizaki, M., Bowen, D., and Smith, P. (2008). Koalas on North Stradbroke Island: diet, tree use and reconstructed landscapes. Wildlife Research 35, 606–611.
| Koalas on North Stradbroke Island: diet, tree use and reconstructed landscapes.Crossref | GoogleScholarGoogle Scholar |
