The impact of isolation and bottlenecks on genetic diversity in the Pearson Island population of the black-footed rock-wallaby (Petrogale lateralis pearsoni; Marsupialia: Macropodidae)
Michelle Jones Lennon A B , David A. Taggart C D , Peter D. Temple-Smith A E and Mark D. B. Eldridge F G H
+ Author Affiliations
- Author Affiliations
A Department of Zoology, University of Melbourne, Parkville, Vic. 3010, Australia.
B Current address: Department of Primary Industries, 1 Spring Street, Melbourne, Vic. 3000, Australia.
C Department of Anatomical Sciences and Department of Earth and Environmental Science, University of Adelaide, Adelaide, SA 5005, Australia.
D Conservation Ark, Royal Zoological Society of South Australia, Frome Road, Adelaide, SA 5000, Australia.
E Department of Obstetrics and Gynaecology, Southern Clinical School, Monash University, Clayton, Vic. 3168, Australia.
F Evolutionary Biology, Australian Museum, 6 College Street, Sydney, NSW 2010, Australia.
G Department of Biological Sciences, Macquarie University, NSW 2109, Australia.
H Corresponding author. Email: mark.eldridge@austmus.gov.au
Australian Mammalogy 33(2) 152-161 https://doi.org/10.1071/AM11011
Submitted: 18 March 2011 Accepted: 1 July 2011 Published: 12 September 2011
Abstract
A morphologically distinct subspecies of black-footed rock-wallaby (Petrogale lateralis pearsoni), is naturally found only on North Pearson Island (~160 ha) in the Investigator Group, SA, where it was isolated by rising sea levels ~10 500 years ago. Subsequent translocations have seen additional populations established on Middle-South Pearson Island (~53 ha) in 1960 and Wedge Island (96 ha) in 1975. We have used 10 hypervariable microsatellite loci to examine the levels of genetic diversity in the endemic (n = 38) and translocated (n = 45–77) P. l. pearsoni populations compared with mainland P. lateralis populations (n = 19–52). Results show that all sampled P. l. pearsoni populations have very low levels of genetic diversity (A = 1.5–1.9; HE = 0.02–0.13) compared with mainland populations (A = 3.5–12.7; HE = 0.54–0.87). Intriguingly, more diversity was detected in the translocated Middle-South Pearson population than in its source population from North Pearson Island. In contrast, the Wedge Island population was almost monomorphic. Overall, the severe loss of genetic diversity (up to 98%) in P. l. pearsoni populations appears to result from random genetic drift on a small isolated population, exacerbated by some subsequent one-off translocation events. Although additional supplementary translocations are recommended to enhance genetic diversity, populations of P. l. pearsoni are likely to remain inherently vulnerable to extinction and therefore of special conservation concern.
References
Barlow, S. (1999). Reintroduction of the yellow-footed rock-wallaby, Petrogale xanthopus xanthopus to Aroona Sanctuary, Northern Flinders Ranges, South Australia: an overview. Thylacinus 23, 12–16.Briskie, J. V., and Mackingtosh, M. (2004). Hatching failure increases with severity of population bottlenecks in birds. Proceedings of the National Academy of Sciences of the United States of America 101, 558–561.
| Hatching failure increases with severity of population bottlenecks in birds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsFGntw%3D%3D&md5=2a690bedf3ec15a4b6593f0c9f1150b4CAS |
Calaby, J. H., and Grigg, G. (1989). Changes in macropod communities and populations in the last 200 years, and the future. In ‘Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 813–820. (Surrey Beatty: Sydney.)
Copley, P. B. (1994). Translocation of native vertebrates in South Australia: a review. In ‘Reintroduction Biology of Australian and New Zealand Fauna’. (Ed. M. Serena.) pp. 35–42. (Surrey Beatty: Sydney.)
Copley, P. B., and Alexander, P. J. (1997). Overview of the status of rock-wallabies in South Australia. Australian Mammalogy 19, 153–162.
Cornuet, J.-M., and Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.
| 1:STN:280:DyaK2s7jt1Kgsw%3D%3D&md5=7127dca5de1e5cc3791c51c165621977CAS |
Dortch, C. E., and Morse, K. (1984). Prehistoric stone artefacts on some offshore islands in Western Australia. Australian Archaeology 19, 31–47.
Eldridge, M. D. B. (2008). Rock-wallabies: Petrogale. In ‘The Mammals of Australia‘. 3rd edn. (Eds S. Van Dyck and R. Strahan.) pp. 361–362. (Reed New Holland: Sydney.)
Eldridge, M. D. B. (2010). Population and conservation genetics of marsupials. In ‘Marsupial Genetics and Genomics’. (Eds J. E. Deakin, P. D. Waters and J. A. M. Graves.) pp. 461–497. (Springer: Dordrecht.)
Eldridge, M. D. B., and Close, R. L. (1997). Chromosomes and evolution in rock-wallabies, Petrogale (Marsupialia: Macropodidae). Australian Mammalogy 19, 123–135.
Eldridge, M. D. B., and Pearson, D. J. (2008). Black-footed rock-wallaby Petrogale lateralis. In ‘The Mammals of Australia’. 3rd edn. (Eds S. Van Dyck and R. Strahan.) pp. 376–380. (New Holland: Sydney.)
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. D. B., Kinnear, J. E., and Onus, M. L. (2001a). Source population of dispersing rock-wallabies (Petrogale lateralis) identified by assignment tests on multilocus genotypic data. Molecular Ecology 10, 2867–2876.
| 1:STN:280:DC%2BD387nslOlug%3D%3D&md5=23e9b929268691cd34f2d8230a44ff19CAS |
Eldridge, M. D. B., Wilson, A. C., Metcalfe, C. J., Dollin, A. E., Bell, J. N., Johnson, P. M., Johnston, P. G., and Close, R. L. (2001b). Taxonomy of rock-wallabies, Petrogale (Marsupialia: Macropodidae). III. Molecular data confirms the species status of the purple-necked rock-wallaby Petrogale purpureicollis Le Souef 1924. Australian Journal of Zoology 49, 323–343.
| Taxonomy of rock-wallabies, Petrogale (Marsupialia: Macropodidae). III. Molecular data confirms the species status of the purple-necked rock-wallaby Petrogale purpureicollis Le Souef 1924.Crossref | GoogleScholarGoogle Scholar |
Eldridge, M. D. B., Piggott, M. P., and Hazlitt, S. L. (2010). Population genetic studies of the Macropodoidea: a review. In ‘Macropods: the Biology of Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. M. Coulson and M. D. B. Eldridge.) pp. 35–51. (CSIRO Publishing: Melbourne.)
Finlayson, G. R., Finlayson, S. T., and Dickman, C. R. (2010). Returning the rat-kangaroos: translocation attempts in the family Potoroidae (superfamily Macropodoidea) and recommendations for conservation. In ‘Macropods: the Biology of Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. M. Coulson and M. D. B. Eldridge.) pp. 245–262. (CSIRO Publishing: Melbourne.)
Frankel, O. H. (1981). Evolution in jeopardy: the role of nature reserves. In ‘Evolution and Speciation. Essasys in Honour of M. J. D. White’. (Eds W. R. Atchley and L. D. Woodruff.) pp. 415–424. (Cambridge University Press: New York.)
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 |
Frankham, R. (1998). Inbreeding and extinction: island populations. Conservation Biology 12, 665–675.
| Inbreeding and extinction: island populations.Crossref | GoogleScholarGoogle Scholar |
Frankham, R., Lees, K., Montgomery, M. E., England, P. A., Lowe, E. H., and Briscoe, D. A. (1999). Do population size bottlenecks reduce evolutionary potential? Animal Conservation 2, 255–260.
| Do population size bottlenecks reduce evolutionary potential?Crossref | GoogleScholarGoogle Scholar |
Frankham, R., Ballou, J. D., and Briscoe, D. A. (2010). ‘Introduction to Conservation Genetics.’ 2nd edn. (Cambridge University Press: Cambridge.)
Franklin, I. R. (1980). Evolutionary change in small populations. In ‘Conservation Biology: An Evolutionary Ecological Perspective’. (Eds M. E. Soulé and B. A. Wilcox.) pp. 139–145. (Sinauer Associates Inc.: Sunderland, USA.)
Gemmell, N. J., and Akiyama, S. (1996). An efficient method for the extraction of DNA from vertebrate tissue. Trends in Genetics 13, 337–338.
Goudet, J. (1995). FSTAT (Version 1.2): A computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.
Hazlitt, S. L., Eldridge, M. D. B., and Goldizen, A. W. (2010). Strong matrilineal structuring in the brush-tailed rock-wallaby confirmed by spatial patterns of mitochondrial DNA. In ‘Macropods: the Biology of Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. M. Coulson and M. D. B. Eldridge.) pp. 87–95. (CSIRO Publishing: Melbourne.)
Heber, S., and Briskie, J. V. (2010). Population bottlenecks and increased hatching failure in endangered birds. Conservation Biology 24, 1674–1678.
| Population bottlenecks and increased hatching failure in endangered birds.Crossref | GoogleScholarGoogle Scholar |
Hinten, G., Harriss, F., Rossetto, M., and Baverstock, P. R. (2003). Genetic variation and island biogeography: microsatellite and mitochondrial DNA variation in island populations of the Australian bush rat, Rattus fuscipes greyii. Conservation Genetics 4, 759–778.
| Genetic variation and island biogeography: microsatellite and mitochondrial DNA variation in island populations of the Australian bush rat, Rattus fuscipes greyii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptlyrs7Y%3D&md5=da1e3ae76a888f73a418792a33e4beb0CAS |
Jamieson, I. G. (2011). Founder effects, inbreeding, and the loss of genetic diversity in four avian reintroduction programs. Conservation Biology 25, 115–123.
| Founder effects, inbreeding, and the loss of genetic diversity in four avian reintroduction programs.Crossref | GoogleScholarGoogle Scholar |
Johnson, P. M., Nolan, B. J., and Schaper, D. N. (2003). Introduction of the Proserpine rock-wallaby Petrogale persephone from mainland Queensland to nearby Hayman Island. Australian Mammalogy 25, 61–71.
Johnson, W. E., Onorato, D. P., Roelke, M. E., Land, E. D., Cunningham, M., Belden, R. C., McBride, R., Jansen, D., Lotz, M., Shindle, D., Howard, J., Wildt, D. E., Penfold, L. M., Hostetler, J. A., Oli, M. K., and O’Brien, S. J. (2010). Genetic restoration of the Florida panther. Science 329, 1641–1645.
| Genetic restoration of the Florida panther.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFOqsrrI&md5=1ecafc9e65342c43fbe595127e8c4a08CAS |
Kinnear, J. E., Onus, M. L., and Bromilow, R. N. (1988). Fox control and rock-wallaby population dynamics. Australian Wildlife Research 15, 435–450.
| Fox control and rock-wallaby population dynamics.Crossref | GoogleScholarGoogle Scholar |
Kinnear, J. E., Onus, M. L., and Sumner, N. R. (1998). Fox control and rock-wallaby population dynamics. II. An update. Wildlife Research 25, 81–88.
| Fox control and rock-wallaby population dynamics. II. An update.Crossref | GoogleScholarGoogle Scholar |
Langford, D. C., and Burbidge, A. A. (2001). Translocation of mala (Lagorchestes hirsutus) from the Tanami Desert, Northern Territory to Trimouille Island, Western Australia. Australian Mammalogy 23, 37–46.
Luikart, G., Allendorf, F. W., Cornuet, J.-M., and Sherwin, W. B. (1998). Distortion of allele frequency distributions provide a test for recent population bottlenecks. The Journal of Heredity 89, 238–247.
| Distortion of allele frequency distributions provide a test for recent population bottlenecks.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czitVKhsA%3D%3D&md5=93c75588848704a5d3a7e312d255c168CAS |
Main, A. R. (1961). The occurrence of Macropodidae on islands and its climatic and ecological implications. Journal of the Royal Society of Western Australia 44, 84–89.
Maruyama, T., and Fuerst, P. A. (1985). Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111, 675–689.
| 1:STN:280:DyaL28%2FjtFeiug%3D%3D&md5=100fc8c9e27abccaa1fba0ab59945714CAS |
Mason, R. A., Browning, T. L., and Eldridge, M. D. B. (2011). Reduced MHC class II diversity in island compared to mainland populations of the black-footed rock-wallaby (Petrogale lateralis lateralis). Conservation Genetics 12, 91–103.
| Reduced MHC class II diversity in island compared to mainland populations of the black-footed rock-wallaby (Petrogale lateralis lateralis).Crossref | GoogleScholarGoogle Scholar |
Maxwell, S., Burbidge, A. A., and Morris, K. (Eds) (1996). ‘The 1996 Action Plan for Australian Marsupials and Monotremes.’ (Wildlife Australia: Canberra.)
McCallum, H. I. (1997). Rock-wallaby biology and management: synthesis and directions for future research. Australian Mammalogy 19, 319–324.
Nei, M., Maruyama, T., and Chakraborty, R. (1975). The bottleneck effect and genetic variability in populations. Evolution 29, 1–10.
| The bottleneck effect and genetic variability in populations.Crossref | GoogleScholarGoogle Scholar |
Pearson, D. J., and Kinnear, J. E. (1997). A review of the distribution, status and conservation of rock-wallabies in Western Australia. Australian Mammalogy 19, 137–152.
Piry, S., Luikart, G., and Cornuet, J.-M. (1999). BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. The Journal of Heredity 90, 502–503.
| BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data.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.
Rice, W. (1989). Analysing tables of statistical tests. Evolution 43, 223–225.
| Analysing tables of statistical tests.Crossref | GoogleScholarGoogle Scholar |
Richards, J. D., and Short, J. (2003). Reintroduction and establishment of the western barred bandicoot Perameles bougainville (Marsupialia: Peramelidae) at Shark Bay, Western Australia. Biological Conservation 109, 181–195.
| Reintroduction and establishment of the western barred bandicoot Perameles bougainville (Marsupialia: Peramelidae) at Shark Bay, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Robinson, A. C. (1980). Notes on the mammals and reptiles of Pearson, Dorothee and Greenly Islands, South Australia. Transactions of the Royal Society of South Australia 104, 93–99.
Robinson, A. C. (1989). Island management in South Australia. In ‘Australia and New Zealand Islands: Nature and Conservation Values and Management’. (Ed. A. A. Burbidge.) pp. 163–181. (Department of Conservation and Land Management: Perth.)
Robinson, A. C., Canty, P. D., Mooney, T., and Rudduck, P. (1996). ‘South Australia’s Offshore Islands.’ (Department of Environment and Natural Resources, South Australia: Adelaide.)
Saccheri, I., Kuussaari, M., Kankare, M., Vikman, P., Fortelius, W., and Hanski, I. (1998). Inbreeding and extinction in a butterfly metapopulation. Nature 392, 491–494.
| Inbreeding and extinction in a butterfly metapopulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisFemsrw%3D&md5=7f271891d1ccbfbcb76c524616e45d5cCAS |
Schmitt, L. H. (1975). Genetic evidence for the existence of two separate populations of Rattus fuscipes greyii on Pearson Island, South Australia. Transactions of the Royal Society of South Australia 99, 35–38.
Seddon, J. M., and Baverstock, P. R. (1999). Variation on islands: major histocompatibility complex (Mhc) polymorphism in populations of the Australian bush rat. Molecular Ecology 8, 2071–2079.
| Variation on islands: major histocompatibility complex (Mhc) polymorphism in populations of the Australian bush rat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FpvVersg%3D%3D&md5=29ef8be058e44e1ef753a997b8595666CAS |
Short, J., and Turner, B. (2000). Reintroduction of the burrowing bettong Bettongia lesueur (Marsupialia: Potoroidae) to mainland Australia. Biological Conservation 96, 185–196.
| Reintroduction of the burrowing bettong Bettongia lesueur (Marsupialia: Potoroidae) to mainland Australia.Crossref | GoogleScholarGoogle Scholar |
Sokal, R. R., and Rohlf, F. J. (1995). ‘Biometry: the Principles and Practice of Statistics in Biological Research.’ (W.H. Freeman & Co: New York.)
Spencer, P. B. S., Odorico, D. M., Jones, S. J., Marsh, H. D., and Miller, D. J. (1995). Highly variable microsatellites in isolated colonies of the rock-wallaby (Petrogale assimilis). Molecular Ecology 4, 523–525.
| Highly variable microsatellites in isolated colonies of the rock-wallaby (Petrogale assimilis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXosFertLk%3D&md5=789a0631b5a637365ec4433a2bc567bdCAS |
Spencer, P. B. S., Adams, M., Marsh, H. D., Miller, D. J., and Eldridge, M. D. B. (1997). High levels of genetic variability in an isolated colony of rock-wallabies (Petrogale assimilis). Evidence from three classes of molecular markers. Australian Journal of Zoology 45, 199–210.
| High levels of genetic variability in an isolated colony of rock-wallabies (Petrogale assimilis). Evidence from three classes of molecular markers.Crossref | GoogleScholarGoogle Scholar |
Taylor, A. C., and Cooper, D. W. (1998). A set of tammar wallaby (Macropus eugenii) microsatellites tested for genetic linkage. Molecular Ecology 7, 925–926.
| 1:CAS:528:DyaK1cXlsFKlur4%3D&md5=3465f8f40bed9194fc1d50dcfeeb869eCAS |
Telfer, W. R., and Eldridge, M. D. B. (2010). High levels of mitochondrial DNA divergence within short-eared rock-wallaby (Petrogale brachyotis) populations in northern Australia. Australian Journal of Zoology 58, 104–112.
| High levels of mitochondrial DNA divergence within short-eared rock-wallaby (Petrogale brachyotis) populations in northern Australia.Crossref | GoogleScholarGoogle Scholar |
Thomas, I. M., and Delroy, L. B. (1971). Pearson Island expedition (1969). 4. The Pearson Island wallaby. Transactions of the Royal Society of South Australia 95, 143–145.
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 |
Zenger, K. R., and Cooper, D. W. (2001). A set of highly polymorphic microsatellite markers developed for the eastern grey kangaroo (Macropus giganteus). Molecular Ecology Notes 1, 98–100.
| A set of highly polymorphic microsatellite markers developed for the eastern grey kangaroo (Macropus giganteus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlslaksbc%3D&md5=c61d003318b7503b9a78fb778e977aa2CAS |
