Regional population structuring and conservation units in the platypus (Ornithorhynchus anatinus)
Stephen H. Kolomyjec A B E , Tom R. Grant C , Christopher N. Johnson A D and David Blair A
+ Author Affiliations
- Author Affiliations
A School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia.
B Present address: Department of Biological and Allied Health Sciences, Ohio Northern University, Ada, OH 45810, USA.
C School of Biological, Earth and Environmental Science, University of New South Wales, Sydney, NSW 2052, Australia.
D Present address: School of Zoology, University of Tasmania, Hobart, Tas. 7001, Australia.
E Corresponding author. Email: s-kolomyjec@onu.edu
Australian Journal of Zoology 61(5) 378-385 https://doi.org/10.1071/ZO13029
Submitted: 1 April 2013 Accepted: 23 October 2013 Published: 18 November 2013
Abstract
The platypus (Ornithorhynchus anatinus) has a wide distribution in Australia, encompassing the southern island of Tasmania and a broad latitudinal range of the mainland from the temperate south to the tropical north. We used 12 microsatellite markers from 235 individuals sampled from 13 river systems to examine patterns of genetic differentiation and gene flow throughout the species’ range. Using a Bayesian approach we identified three large-scale groupings that correspond closely to geographically distinct regions of the species’ distribution: the tropical northern mainland, the subtropical and temperate southern mainland, and Tasmania. Six additional clusters were found within the regional groups, three in the northern, two in the southern mainland regions, and the last in Tasmania. These clusters coincided with major river drainages. Genetic differentiation was generally high, with pairwise Fst values ranging from 0.065 to 0.368 for regions and 0.037 to 0.479 for clusters. We found no evidence of contemporary gene flow among the three clusters in the north, but some migration may occur between the larger clusters in the south. Due to the high genetic structuring and lack of gene flow between these three regional populations of the platypus we recommend their treatment as evolutionarily significant units (ESUs) within the platypus species. We have also detailed several smaller management units (MUs) existing within our study area based on subregional clusters and geographically significant features.
References
Akiyama, S. (1998). Molecular ecology of the platypus (Ornithorynchus anatinus). Ph.D. Thesis, La Trobe University, Victoria, Australia.Akiyama, S. (2000). Molecular ecology of the platypus in Tasmania. Australian Mammalogy 21, 263.
Akiyama, S., Grant, T. R., Gemmell, N. J., Graves, J. A. M., and Murray, N. D. (1996). Microsatellite loci and population structure in the platypus. In ‘Proceedings of the National Symposium on Platypus Biology’. pp. 299–313. (Charles Sturt University: Bathurst.)
Connolly, J. H., and Obendorf, D. L. (1998). Distribution, captures and physical characteristics of the platypus (Ornithorhynchus anatinus) in Tasmania. Australian Mammalogy 20, 231–237.
Connolly, J. H., Obendorf, D. L., Whittington, R. J., and Muir, D. B. (1998). Causes of morbidity and mortality in platypus (Ornithorhynchus anatinus) from Tasmania, with particular reference to Mucor amphibiorum infection. Australian Mammalogy 20, 177–187.
Corander, J., and Marttinen, P. (2006). Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology 15, 2833–2843.
| Bayesian identification of admixture events using multilocus molecular markers.Crossref | GoogleScholarGoogle Scholar | 16911204PubMed |
Corander, J., Marttinen, P., and Mäntyniemi, S. (2006). Bayesian identification of stock mixtures from molecular marker data. Fishery Bulletin 104, 550–558.
Corander, J., Marttinen, P., Sirén, J., and Tang, J. (2008). Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9, 539.
| Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations.Crossref | GoogleScholarGoogle Scholar | 19087322PubMed |
Dight, I. (2009). Burdekin water quality improvement plan. NQ Dry Tropics, Townsville, Queensland.
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=1167baf60642a311f7d48c107f13dc7fCAS | 15969739PubMed |
Fielding, C. R., and Alexander, J. (1996). Sedimentology of the Upper Burdekin River of north Queensland, Australia – an example of a tropical, variable discharge river. Terra Nova 8, 447–457.
| Sedimentology of the Upper Burdekin River of north Queensland, Australia – an example of a tropical, variable discharge river.Crossref | GoogleScholarGoogle Scholar |
Furlan, E., Umina, P. A., Mitrovski, P. J., Gust, N., Griffiths, J., and Weeks, A. R. (2010). High levels of genetic divergence between Tasmanian and Victorian platypuses, Ornithorhynchus anatinus, as revealed by microsatellite loci. Conservation Genetics 11, 319–323.
| High levels of genetic divergence between Tasmanian and Victorian platypuses, Ornithorhynchus anatinus, as revealed by microsatellite loci.Crossref | GoogleScholarGoogle Scholar |
Furlan, E., Griffiths, J., Gust, N., Armistead, R., Mitrovski, P., Handasyde, K. A., Serena, M., Hoffmann, A. A., and Weeks, A. R. (2012). Is body size variation in the platypus (Ornithorhynchus anatinus) associated with environmental variables? Australian Journal of Zoology 59, 201–215.
| Is body size variation in the platypus (Ornithorhynchus anatinus) associated with environmental variables?Crossref | GoogleScholarGoogle Scholar |
George, G. G., Dixon, J., Challis, G., and Lacy, R. C. (1990). The taxonomy and palaeontology of the eastern barred bandicoot: their bearings on management of the Victorian population. In ‘Management and Conservation of Small Populations’. (Eds T. W. Clark and J. H. Seebeck.) pp. 33–46. (Chicago Zoological Society: Brookfield, IL.)
Gongora, J., Swan, A. B., Chong, A. Y., Ho, S. Y. W., Damayanti, C. S., Kolomyjec, S., Grant, T., Miller, E., Blair, D., Furlan, E., and Gust, N. (2012). Genetic structure and phylogeography of platypuses revealed by mitochondrial DNA. Journal of Zoology 286, 110–119.
| Genetic structure and phylogeography of platypuses revealed by mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar |
Goudet, J. (1995). Fstat (version 1.2): a computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.
Goudie, A. (2006). The human impact on the waters. In ‘The Human Impact on the Natural Environment’. pp. 121–158. (Blackwell Publishing: Oxford.)
Grant, T. R. (1992). Historical and current distribution of the platypus, Ornithorynchus anatinus, in Australia. In ‘Platypus and Echidnas’. (Ed. M. L. Augee.) pp. 232–254. (The Royal Zoological Society of New South Wales: Sydney.)
Grant, T. R. (2007). ‘Platypus.’ 4th edn. (CSIRO Publishing: Melbourne.)
Grant, T. R., and Carrick, F. N. (1974). Capture and marking the platypus, Ornithorhynchus anatinus in the wild. Australian Zoologist 18, 133–135.
Grant, T. R., and Temple-Smith, P. D. (1998). Field biology of the platypus (Ornithorhynchus anatinus): historical and current perspectives. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 353, 1081–1091.
| Field biology of the platypus (Ornithorhynchus anatinus): historical and current perspectives.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czos1Gktw%3D%3D&md5=d556539e4f232e3fec5a53fccd0322a5CAS | 9720106PubMed |
Grant, T. R., and Whittington, R. J. (1991). The use of freeze-branding and implanted transponder tags as a permanent marking method for the platypus, Ornithorhynchus anatinus (Monotremata: Ornithorhynchidae). Australian Mammalogy 14, 147–150.
Herrin, R. O. (2009). Distribution and individual characteristics of the platypus in the Plenty River, southeast Tasmania. B.Sc.(Hons)/M.Sc. Thesis, University of Tasmania, Australia/Lund University, Sweden.
Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6, 56–70.
Iredale, T., and Troughton, E. Le G. (1934). ‘A Check-list of the Mammals recorded from Australia.’ (The Australian Museum: Sydney.)
Kingsford, R. T. (2000). Ecological impacts of dams, water diversion and river management on floodplain wetlands in Australia. Austral Ecology 25, 109–127.
| Ecological impacts of dams, water diversion and river management on floodplain wetlands in Australia.Crossref | GoogleScholarGoogle Scholar |
Klamt, M., Thompson, R., and Davis, J. (2011). Early response of the platypus to climate warming. Global Change Biology 17, 3011–3018.
| Early response of the platypus to climate warming.Crossref | GoogleScholarGoogle Scholar |
Kolomyjec, S. H. (2010). The history and relationships of northern platypus (Ornithorhynchus anatinus) populations: a molecular approach. Ph.D. Thesis, James Cook University, Townsville.
Kolomyjec, S. H., Grant, T. R., and Blair, D. (2008). Ten polymorphic microsatellite DNA markers for the platypus, Ornithorhynchus anatinus. Molecular Ecology Resources 8, 1133–1135.
| Ten polymorphic microsatellite DNA markers for the platypus, Ornithorhynchus anatinus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFCisLzL&md5=ddbae45fc0bdd83bea32bc7b30d78fe6CAS | 21585993PubMed |
Kolomyjec, S. H., Chong, J. Y. T., Blair, D., Gongora, J., Grant, T. R., Johnson, C. N., and Moran, C. (2009). Population genetics of the platypus (Ornithorhynchus anatinus): a fine-scale look at adjacent river systems. Australian Journal of Zoology 57, 225–234.
| Population genetics of the platypus (Ornithorhynchus anatinus): a fine-scale look at adjacent river systems.Crossref | GoogleScholarGoogle Scholar |
Lintermans, M. (1998). The status and distribution of the platypus (Ornithorhynchus anatinus) in the Australian Capital Territory with notes on some localised declines. Australian Mammalogy 20, 306.
Lunney, D., Grant, T. R., Matthews, A., Esson, C., Moon, C., and Ellis, M. (1998). Determining the distribution of the platypus (Ornithorhynchus anatinus) in the Eden region of south-eastern New South Wales through community-based surveys. Australian Mammalogy 20, 239–250.
Lunney, D., Dickman, C., Copley, P., Grant, T., Munks, S., Carrick, F., Serena, M., and Ellis, M. (2008). Ornithorhynchus anatinus. In ‘IUCN Red List of Threatened Species. Version 2010.4’. Available at: http://www.iucnredlist.org (accessed 26 May 2011).
Mahoney, J. A. (1988). Ornithorhynchidae. In ‘Zoological Catalogue of Australia: Vol. 5 – Mammalia’. (Ed. D. W. Walton.) pp. 7–10. (CSIRO Publishing & Australian Biological Resources Study: Melbourne.)
Mitsouras, K., and Faulhaber, E. A. (2009). Saliva as an alternative source of high yield canine genomic DNA for genotyping studies. BMC Research Notes 2, 219.
| Saliva as an alternative source of high yield canine genomic DNA for genotyping studies.Crossref | GoogleScholarGoogle Scholar | 19874604PubMed |
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=418d66d783ad2fabc35800e65093f56bCAS |
Moritz, C. (1995). Use of molecular phylogenies for conservation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 349, 113–118.
| Use of molecular phylogenies for conservation.Crossref | GoogleScholarGoogle Scholar |
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 |
Munks, S. A., Otley, H. M., Jackson, J., and Hindell, M. (1998). Captures, body mass and diet of platypuses in a subalpine Tasmanian lake. Australian Mammalogy 20, 311.
Nevill, P. G., Bossinger, G., and Ades, P. K. (2010). Phylogeography of the world’s tallest angiosperm, Eucalyptus regnans: evidence for multiple isolated Quaternary refugia. Journal of Biogeography 37, 179–192.
| Phylogeography of the world’s tallest angiosperm, Eucalyptus regnans: evidence for multiple isolated Quaternary refugia.Crossref | GoogleScholarGoogle Scholar |
Norgate, M., Chamings, J., Pavlova, A., Bull, J. K., Murray, N. D., and Sunnucks, P. (2009). Mitochondrial DNA indicates late Pleistocene divergence of populations of Heteronympha merope, an emerging model in environmental change biology. PLoS ONE 4, e7950.
| Mitochondrial DNA indicates late Pleistocene divergence of populations of Heteronympha merope, an emerging model in environmental change biology.Crossref | GoogleScholarGoogle Scholar | 19956696PubMed |
Otley, H. M. (2001). The use of a community-based survey to determine the distribution of the platypus Ornithorhynchus anatinus in the Huon River catchment, southern Tasmania. Australian Zoologist 31, 632–641.
Otley, H. M., Munks, S. A., and Hindell, M. A. (2000). Activity patterns, movements and burrows of platypuses (Ornithorhynchus anatinus) in a sub-alpine Tasmanian lake. Australian Journal of Zoology 48, 701–713.
| Activity patterns, movements and burrows of platypuses (Ornithorhynchus anatinus) in a sub-alpine Tasmanian lake.Crossref | GoogleScholarGoogle Scholar |
Paetkau, D. (1999). Using genetics to identify intraspecific conservation units: a critique of current methods. Conservation Biology 13, 1507–1509.
| Using genetics to identify intraspecific conservation units: a critique of current methods.Crossref | GoogleScholarGoogle Scholar |
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 |
Pritchard, J. K., and Wen, W. (2003). ‘Documentation for STRUCTURE Software: Version 2.’ Available at: http://pritch.bsd.uchicago.edu.
Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure from multilocus genotype data. Genetics 155, 945–959.
| 1:STN:280:DC%2BD3cvislKrtA%3D%3D&md5=c7a8ff87644f6b26224365136082068eCAS | 10835412PubMed |
Rice, W. R. (1989). Analyzing table of statistical tests. Evolution 43, 223–225.
| Analyzing table of statistical tests.Crossref | GoogleScholarGoogle Scholar |
Rohweder, D. A., and Baverstock, P. R. (1999). Distribution of platypus Ornithorhynchus anatinus in the Richmond River Catchment, northern New South Wales. Australian Zoologist 31, 30–37.
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 |
Schneider, S., Roessli, D., and Excoffier, L. (2000). Arlequin: A software for population genetics data analysis. Genetics and Biometry Laboratory, Department of Anthropology, University of Geneva.
Serena, M., and Pettigrove, V. (2005). Relationship of sediment toxicants and water quality to the distribution of platypus populations in urban streams. Journal of the North American Benthological Society 24, 679–689.
Serena, M., Thomas, J. L., Williams, G. A., and Officer, R. C. E. (1998). Use of stream and river habitats by the platypus, Ornithorhynchus anatinus, in an urban fringe environment. Australian Journal of Zoology 46, 267–282.
| Use of stream and river habitats by the platypus, Ornithorhynchus anatinus, in an urban fringe environment.Crossref | GoogleScholarGoogle Scholar |
Sikes, R. S., Gannon, W. L., Animal Care and Use Committee of the American Society of Mammalogists (2011). Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92, 235–253.
| Guidelines of the American Society of Mammalogists for the use of wild mammals in research.Crossref | GoogleScholarGoogle Scholar |
Strahan, R., and van Dyck, S. (2008). ‘The Mammals of Australia.’ 3rd edn. (New Holland: Sydney.)
Sunnucks, P., and Hales, D. F. (1996). Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13, 510–524.
| Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xht1Kgurk%3D&md5=96aa0f41c00a5a3f1b266f7f0e7a3afcCAS | 8742640PubMed |
Tang, J., Hanage, W. P., Fraser, C., and Corander, J. (2009). Identifying currents in the gene pool for bacterial populations using an integrative approach. PLoS Computational Biology 5, e1000455.
| Identifying currents in the gene pool for bacterial populations using an integrative approach.Crossref | GoogleScholarGoogle Scholar | 19662158PubMed |
Watson, J. A. L., and Theischinger, G. (1984). Regions of taxonomic disjunction in Australian Odonata and other freshwater insects. Odonatologica 13, 147–157.
