Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Delineation of conservation units in an endangered marsupial, the southern brown bandicoot (Isoodon obesulus obesulus), in South Australia/western Victoria, Australia

You Li A B F , Melanie L. Lancaster A B C , Susan M. Carthew A E , Jasmin G. Packer A and Steven J. B. Cooper A B D
+ Author Affiliations
- Author Affiliations

A School of Earth and Environmental Sciences, the University of Adelaide, Adelaide, SA 5005, Australia.

B Australian Centre for Evolutionary Biology and Biodiversity, the University of Adelaide, Adelaide, SA 5005, Australia.

C Healesville Sanctuary, Healesville, Vic. 3777, Australia.

D Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.

E Research Institute for Environment and Livelihoods, Charles Darwin University, Darwin, NT 0909, Australia.

F Corresponding author. Email: you.li@alumni.adelaide.edu.au

Australian Journal of Zoology 62(5) 345-359 https://doi.org/10.1071/ZO14038
Submitted: 30 May 2014  Accepted: 24 August 2014   Published: 23 September 2014

Abstract

Conservation programs for threatened species are greatly benefiting from genetic data, for their power in providing knowledge of dispersal/gene flow across fragmented landscapes and for identifying populations of high conservation value. The endangered southern brown bandicoot (Isoodon obesulus obesulus) has a disjunct distribution range in South Australia, raising the possibility that populations of the subspecies may represent distinct conservation units. In the current study, we used a combination of 14 microsatellite and two mitochondrial sequence markers to investigate the phylogeography and population structure of I. o. obesulus in South Australia and south-western Victoria, with the aim of identifying any potential evolutionarily significant units and management units relevant to conservation management. Our phylogenetic/population analyses supported the presence of two distinct evolutionary lineages of I. o. obesulus. The first lineage comprised individuals from the Mount Lofty Ranges, Fleurieu Peninsula and Kangaroo Island. A second lineage comprised individuals from the south-east of South Australia and south-western Victoria. We propose that these two lineages represent distinct evolutionarily significant units and should be managed separately for conservation purposes. The findings also raise significant issues for the national conservation status of I. o. obesulus and suggest that the current subspecies classification needs further investigation.

Additional keywords: evolutionarily significant unit, management unit, microsatellite, mtDNA.


References

Aitken, P. (1983). Mammals. In ‘Natural History of the South East’. (Eds M. J. Tyler, C. R. Twidale, J. K. Ling, and J. W. Holmes.) pp. 127–133. (Royal Society of South Australia: Adelaide.)

Allendorf, F. W., Luikart, G., and Aitken, S. N. (2013). ‘Conservation and the Genetics of Populations.’ 2nd edn. (Wiley-Blackwell.)

Ashby, E., Lunney, D., Robertshaw, J., and Harden, R. (1990). Status of bandicoots in New South Wales. In ‘Bandicoots and Bilbies’. (Eds J. H. Seebeck, P. R. Brown, R. L. Wallis, and C. M. Kemper.) pp. 43–50. (Surrey Beatty: Sydney.)

Brown, G. W., and Main, M. L. (2010). National recovery plan for the southern brown bandicoot Isoodon obesulus obesulus. Department of Sustainability and Environment, Victoria.

Bulazel, K. V., Ferreri, G. C., Eldridge, M. D. B., and O’Neill, R. J. (2007). Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biology 8, R170.
Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages.Crossref | GoogleScholarGoogle Scholar | 17708770PubMed |

Clegg, S. M., Hale, P., and Moritz, C. (1998). Molecular population genetics of the red kangaroo (Macropus rufus): mtDNA variation. Molecular Ecology 7, 679–686.
Molecular population genetics of the red kangaroo (Macropus rufus): mtDNA variation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktlemu70%3D&md5=0e76e50a0a6108f80fe9de9944e225e9CAS | 9640648PubMed |

Coates, T., Nicholls, D., and Willig, R. (2008). The distribution of the southern brown bandicoot Isoodon obesulus in south central Victoria. The Victorian Naturalist 125, 128–139.

Crandall, K. A., Bininda-Emonds, O. R. P., Mace, G. M., and Wayne, R. K. (2000). Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution 15, 290–295.
Considering evolutionary processes in conservation biology.Crossref | GoogleScholarGoogle Scholar |

Department of Environment and Conservation (DEC) (2006). Recovery plan for the southern brown bandicoot (Isoodon obesulus). Hurstville, New South Wales.

Earl, D. A., and vonHoldt, B. M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |

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., Wilson, A. C. C., Metcalfe, C. J., Dollin, A. E., Bell, J. N., Johnson, P. M., Johnston, P. G., and Close, R. L. (2001). Taxonomy of rock-wallabies, Petrogale (Marsupialia: Macropodidae). III. Molecular data confirms the species status of the purple-necked rock-wallaby (Petrogale purpureicollis Le Souef). 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).Crossref | GoogleScholarGoogle Scholar |

Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=eb59ed4aa80797d01ea0ca7504502ccfCAS | 15969739PubMed |

Excoffier, L., and Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |

Firestone, K. B., Elphinstone, M. S., Sherwin, W. B., and Houlden, B. A. (1999). Phylogeographical population structure of tiger quolls Dasyurus maculatus (Dasyuridae: Marsupialia), an endangered carnivorous marsupial. Molecular Ecology 8, 1613–1625.
Phylogeographical population structure of tiger quolls Dasyurus maculatus (Dasyuridae: Marsupialia), an endangered carnivorous marsupial.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FltFansA%3D%3D&md5=45c4127fee42eb91dcef69521f2da140CAS | 10583825PubMed |

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 | 9119706PubMed |

Frankham, R. (2010). Challenges and opportunities of genetic approaches to biological conservation. Biological Conservation 143, 1919–1927.
Challenges and opportunities of genetic approaches to biological conservation.Crossref | GoogleScholarGoogle Scholar |

Frankham, R., Ballou, J. D., and Briscoe, D. A. (2002). ‘Introduction to Conservation Genetics.’ (Cambridge University Press: Cambridge.)

Frankham, R., Ballou, J. D., Eldridge, M. D. B., Lacy, R. C., Ralls, K., Dudash, M. R., and Fenster, C. B. (2011). Predicting the probability of outbreeding depression. Conservation Biology 25, 465–475.
Predicting the probability of outbreeding depression.Crossref | GoogleScholarGoogle Scholar | 21486369PubMed |

Fumagalli, L., Pope, L. C., Taberlet, P., and Moritz, C. (1997). Versatile primers for the amplification of the mitochondrial DNA control region in marsupials. Molecular Ecology 6, 1199–1201.
Versatile primers for the amplification of the mitochondrial DNA control region in marsupials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisVWntA%3D%3D&md5=cbe6495963811fc0fc031c3b883c54b8CAS | 9421920PubMed |

Funk, W. C., McKay, J. K., Hohenlohe, P. A., and Allendorf, F. W. (2012). Harnessing genomics for delineating conservation units. Trends in Ecology & Evolution 27, 489–496.
Harnessing genomics for delineating conservation units.Crossref | GoogleScholarGoogle Scholar |

Gerlach, G., Jueterbock, A., Kraemer, P., Deppermann, J., and Harmand, P. (2010). Calculations of population differentiation based on G(ST) and D: forget G(ST) but not all of statistics! Molecular Ecology 19, 3845–3852.
Calculations of population differentiation based on G(ST) and D: forget G(ST) but not all of statistics!Crossref | GoogleScholarGoogle Scholar | 20735737PubMed |

Goudet, J. (2001). FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3).

Haby, N. A., and Long, K. (2005). Recovery plan for the southern brown bandicoot in the Mount Lofty Ranges, South Australia. Department for Environment and Heritage.

Heller, N. E., and Zavaleta, E. S. (2009). Biodiversity management in the face of climate change: a review of 22 years of recommendations. Biological Conservation 142, 14–32.
Biodiversity management in the face of climate change: a review of 22 years of recommendations.Crossref | GoogleScholarGoogle Scholar |

Hope, B. (2012). Short-term response of the long-nosed bandicoot, Perameles nasuta, and the southern brown bandicoot, Isoodon obesulus obesulus, to low-intensity prescribed fire in heathland vegetation. Wildlife Research 39, 731–744.
Short-term response of the long-nosed bandicoot, Perameles nasuta, and the southern brown bandicoot, Isoodon obesulus obesulus, to low-intensity prescribed fire in heathland vegetation.Crossref | GoogleScholarGoogle Scholar |

Horn, T. (2003). South East Biodiversity Corridors Strategy. ForestrySA.

Jakobsson, M., and Rosenberg, N. A. (2007). CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.
CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1ahtbs%3D&md5=61c992f921bfe68f428dc45a18b23044CAS | 17485429PubMed |

Jensen, H., Moe, R., Hagen, I. J., Holand, A. M., Kekkonen, J., Tufto, J., and Saether, B. E. (2013). Genetic variation and structure of house sparrow populations: is there an island effect? Molecular Ecology 22, 1792–1805.
Genetic variation and structure of house sparrow populations: is there an island effect?Crossref | GoogleScholarGoogle Scholar | 23379682PubMed |

Jombart, T. (2008). adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405.
adegenet: a R package for the multivariate analysis of genetic markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtVais7s%3D&md5=c236c71e34c43bc4550d688093f52dc8CAS | 18397895PubMed |

Jombart, T., Devillard, S., Dufour, A. B., and Pontier, D. (2008). Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101, 92–103.
Revealing cryptic spatial patterns in genetic variability by a new multivariate method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1eis7g%3D&md5=c1ed02cbf08e189020b409489aa110deCAS | 18446182PubMed |

Jones, F. W. (1924). The bandicoots and herbivorous marsupials. In ‘The Mammals of South Australia: Part II’. pp. 133–270. (Government Printer: Adelaide.)

Jost, L. (2008). G(ST) and its relatives do not measure differentiation. Molecular Ecology 17, 4015–4026.
G(ST) and its relatives do not measure differentiation.Crossref | GoogleScholarGoogle Scholar | 19238703PubMed |

Jump, A. S., and Penuelas, J. (2005). Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters 8, 1010–1020.
Running to stand still: adaptation and the response of plants to rapid climate change.Crossref | GoogleScholarGoogle Scholar |

Kemper, C. (1990). Status of bandicoots in South Australia. In ‘Bandicoots and Bilbies’. (Eds J. H. Seebeck, P. R. Brown, R. L. Wallis, and C. M. Kemper.) pp. 67–72. (Surrey Beatty: Sydney.)

Krefft, G. (1866). On the vertebrated animals of the Lower Murray and Darling, their habits, economy, and geographical distribution. In ‘Transactions of the Philosophical Society of New South Wales 1862–1865’. pp. 1–33. (Reading and Wellbank: Sydney.)

Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of patitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
PartitionFinder: combined selection of patitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=7b00db0d4d8de2b34032ea1c0108d86cCAS | 22319168PubMed |

Li, Y., Lancaster, M. L., Cooper, S. J. B., Packer, J. G., and Carthew, S. M. (2013). Characterization of nine microsatellite loci from the endangered southern brown bandicoot (Isoodon obesulus) using 454 pyrosequencing. Conservation Genetics Resources 5, 105–107.
Characterization of nine microsatellite loci from the endangered southern brown bandicoot (Isoodon obesulus) using 454 pyrosequencing.Crossref | GoogleScholarGoogle Scholar |

Lowe, W. H., and Allendorf, F. W. (2010). What can genetics tell us about population connectivity? Molecular Ecology 19, 3038–3051.
What can genetics tell us about population connectivity?Crossref | GoogleScholarGoogle Scholar | 20618697PubMed |

Lunney, D., and Leary, T. (1988). The impact on native mammals of land-use changes and exotic species in the Bega district, New South Wales, since settlement. Australian Journal of Ecology 13, 67–92.
The impact on native mammals of land-use changes and exotic species in the Bega district, New South Wales, since settlement.Crossref | GoogleScholarGoogle Scholar |

Lyne, A. G., and Mort, P. A. (1981). A comparison of skull morphology in the marsupial bandicoot genus Isoodon: its taxonomic implications and notes on a new species, Isoodon arnhemensis. Australian Mammalogy 4, 107–133.

Malekian, M., Cooper, S. J. B., and Carthew, S. M. (2010a). Phylogeography of the Australian sugar glider (Petaurus breviceps): evidence for a new divergent lineage in eastern Australia. Australian Journal of Zoology 58, 165–181.
Phylogeography of the Australian sugar glider (Petaurus breviceps): evidence for a new divergent lineage in eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Malekian, M., Cooper, S. J. B., Norman, J. A., Christidis, L., and Carthew, S. M. (2010b). Molecular systematics and evolutionary origins of the genus Petaurus (Marsupialia: Petauridae) in Australia and New Guinea. Molecular Phylogenetics and Evolution 54, 122–135.
Molecular systematics and evolutionary origins of the genus Petaurus (Marsupialia: Petauridae) in Australia and New Guinea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFagsb7N&md5=03b812d23db7dfa87eaa38759ecf1c7fCAS | 19647084PubMed |

Menkhorst, P. W., and Seebeck, J. H. (1990). Distribution and conservation status of bandicoots in Victoria. In ‘Bandicoots and Bilbies’. (Eds J. H. Seebeck, P. R. Brown, R. L. Wallis, and C. M. Kemper.) pp. 51–60. (Surrey Beatty: Sydney.)

Moritz, C. (1994). Defining ‘evolutionarily significant units’ for conservation. Trends in Ecology & Evolution 9, 373–375.
Defining ‘evolutionarily significant units’ for conservation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFWhsA%3D%3D&md5=807e9b1c6637836734c00157ce889224CAS |

Moritz, C. (1999). Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130, 217–228.
Conservation units and translocations: strategies for conserving evolutionary processes.Crossref | GoogleScholarGoogle Scholar |

Moritz, C. (2002). Strategies to protect biological diversity and the evolutionary processes that sustain it. Systematic Biology 51, 238–254.
Strategies to protect biological diversity and the evolutionary processes that sustain it.Crossref | GoogleScholarGoogle Scholar | 12028731PubMed |

Osborne, M. J., and Christidis, L. (2001). Molecular phylogenetics of Australo-Papuan possums and gliders (family Petauridae). Molecular Phylogenetics and Evolution 20, 211–224.
Molecular phylogenetics of Australo-Papuan possums and gliders (family Petauridae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFSnsrg%3D&md5=0fe19ba4fd3186d4599ded56b2234251CAS | 11476630PubMed |

Palsbøll, P. J., Bérubé, M., and Allendorf, F. W. (2007). Identification of management units using population genetic data. Trends in Ecology & Evolution 22, 11–16.
Identification of management units using population genetic data.Crossref | GoogleScholarGoogle Scholar |

Paull, D. J. (1993). The distribution, ecology and conservation status of the southern brown bandicoot (Isoodon obesulus obesulus) in South Australia. M.A. Thesis, University of Adelaide.

Paull, D. J. (1995). The distribution of the southern brown bandicoot (Isoodon obesulus obesulus) in South Australia. Wildlife Research 22, 585–600.
The distribution of the southern brown bandicoot (Isoodon obesulus obesulus) in South Australia.Crossref | GoogleScholarGoogle Scholar |

Paull, D. J., Mills, D. J., and Claridge, A. W. (2013). Fragmentation of the southern brown bandicoot Isoodon obesulus: unraveling past climate change from vegetation clearing. International Journal of Ecology 2013, Article ID 536524.

Pope, L. C., Sharp, A., and Moritz, C. (1996). Population structure of the yellow-footed rock-wallaby Petrogale xanthopus (Gray, 1854) inferred from mtDNA sequences and microsatellite loci. Molecular Ecology 5, 629–640.
Population structure of the yellow-footed rock-wallaby Petrogale xanthopus (Gray, 1854) inferred from mtDNA sequences and microsatellite loci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmsValsb4%3D&md5=5524ea72423f1440516f8b0142159363CAS | 8873466PubMed |

Pope, L. C., Storch, D., Adams, M., Moritz, C., and Gordon, G. (2001). A phylogeny for the genus Isoodon and a range extension for Isoodon obesulus peninsulae based on mtDNA control region and morphology. Australian Journal of Zoology 49, 411–434.
A phylogeny for the genus Isoodon and a range extension for Isoodon obesulus peninsulae based on mtDNA control region and morphology.Crossref | GoogleScholarGoogle Scholar |

Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 1:STN:280:DC%2BD3cvislKrtA%3D%3D&md5=abf0aa80c117c442e1137ae79fc63099CAS | 10835412PubMed |

Pusey, A., and Wolf, M. (1996). Inbreeding avoidance in animals. Trends in Ecology & Evolution 11, 201–206.
Inbreeding avoidance in animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFCgsQ%3D%3D&md5=d3106f9b5000e75f22a8419e37f103d7CAS |

Rees, M., and Paull, D. (2000). Distribution of the southern brown bandicoot (Isoodon obesulus) in the Portland region of southwestern Victoria. Wildlife Research 27, 539–545.
Distribution of the southern brown bandicoot (Isoodon obesulus) in the Portland region of southwestern Victoria.Crossref | GoogleScholarGoogle Scholar |

Reusch, T. B. H., Ehlers, A., Hammerli, A., and Worm, B. (2005). Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences of the United States of America 102, 2826–2831.
Ecosystem recovery after climatic extremes enhanced by genotypic diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitVSksLY%3D&md5=b503ad19e5c464117fb5b5cc37d4d29bCAS |

Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43, 223–225.
Analyzing tables of statistical tests.Crossref | GoogleScholarGoogle Scholar |

Rodríguez, F., Oliver, J. F., Marín, A., and Medina, J. R. (1990). The general stochastic model of nucleotide substitutions. Journal of Theoretical Biology 142, 485–501.
The general stochastic model of nucleotide substitutions.Crossref | GoogleScholarGoogle Scholar | 2338834PubMed |

Rosenberg, N. A. (2004). DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137–138.
DISTRUCT: a program for the graphical display of population structure.Crossref | GoogleScholarGoogle Scholar |

Ryder, O. A. (1986). Species conservation and systematics – the dilemma of subspecies. Trends in Ecology & Evolution 1, 9–10.
Species conservation and systematics – the dilemma of subspecies.Crossref | GoogleScholarGoogle Scholar |

Short, J., and Smith, A. (1994). Mammal decline and recovery in Australia. Journal of Mammalogy 75, 288–297.
Mammal decline and recovery in Australia.Crossref | GoogleScholarGoogle Scholar |

Stamatakis, A., Hoover, P., and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758–771.
A rapid bootstrap algorithm for the RAxML web servers.Crossref | GoogleScholarGoogle Scholar | 18853362PubMed |

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=e841dcb65bf5743a3261692bb5310fe6CAS | 21546353PubMed |

Thompson, M. B., Medlin, G., Hutchinson, R., and West, N. (1989). Short-term effects of fuel reduction burning on populations of small terrestrial mammals. Australian Wildlife Research 16, 117–129.
Short-term effects of fuel reduction burning on populations of small terrestrial mammals.Crossref | GoogleScholarGoogle Scholar |

Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
| 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=642d3c27a53cc46b25cea2a96ea87beeCAS |

Waples, R. S. (1991). Pacific salmon, Oncorhynchus spp., and the definition of ‘species’ under the Endangered Species Act. U S National Marine Fisheries Service, Marine Fisheries Review 53, 11–22.

Waples, R. S. (1998). Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. The Journal of Heredity 89, 438–450.
Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species.Crossref | GoogleScholarGoogle Scholar |

Waples, R. S., and Gaggiotti, O. (2006). What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Molecular Ecology 15, 1419–1439.
What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsVCjur4%3D&md5=6707d667ffc97451b072a50ce551fd73CAS | 16629801PubMed |

Weeks, A. R., Sgro, C. M., Young, A. G., Frankham, R., Mitchell, N. J., Miller, K. A., Byrne, M., Coates, D. J., Eldridge, M. D. B., Sunnucks, P., Breed, M. F., James, E. A., and Hoffmann, A. A. (2011). Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evolutionary Applications 4, 709–725.
Assessing the benefits and risks of translocations in changing environments: a genetic perspective.Crossref | GoogleScholarGoogle Scholar | 22287981PubMed |

Westerman, M., and Krajewski, C. (2000). Molecular relationships of the Australian bandicoot genera Isoodon and Perameles (Marsupialia: Peramelina). Australian Mammalogy 22, 1–8.

Westerman, M., Kear, B. P., Aplin, K., Meredith, R. W., Emerling, C., and Springer, M. S. (2012). Phylogenetic relationships of living and recently extinct bandicoots based on nuclear and mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 62, 97–108.
Phylogenetic relationships of living and recently extinct bandicoots based on nuclear and mitochondrial DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38%2FotFelug%3D%3D&md5=1aa6658e1b7446d5dfba69d7f55e7380CAS | 22100729PubMed |

Yang, Z. (1996). Among-site rate variation and its impact on phylogenetic analyses. Trends in Ecology & Evolution 11, 367–372.
Among-site rate variation and its impact on phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFGjtw%3D%3D&md5=2a7c32049a02122782d3750d6a5f8141CAS |

Zenger, K. R., and Johnston, P. G. (2001). Isolation and characterization of microsatellite loci in the southern brown bandicoot (Isoodon obesulus), and their applicability to other marsupial species. Molecular Ecology Notes 1, 149–151.
Isolation and characterization of microsatellite loci in the southern brown bandicoot (Isoodon obesulus), and their applicability to other marsupial species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslKku78%3D&md5=59eee0b0fd58bb4684b3594d7c5f3209CAS |

Zenger, K. R., Eldridge, M. D. B., and Johnston, P. G. (2005). Phylogenetics, population structure and genetic diversity of the endangered southern brown bandicoot (Isoodon obesulus) in south-eastern Australia. Conservation Genetics 6, 193–204.
Phylogenetics, population structure and genetic diversity of the endangered southern brown bandicoot (Isoodon obesulus) in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvF2msLY%3D&md5=b126b9f32f7a443dab236d9ed4230333CAS |