Abstract
Musk Ducks (Biziura lobata) are endemic to Australia and occur as two geographically isolated populations separated by the Nullarbor Plain, a vast arid region in southern Australia. We studied genetic variation in Musk Duck populations at coarse (eastern versus western Australia) and fine scales (four sites within eastern Australia). We found significant genetic structure between eastern and western Australia in the mtDNA control region (ΦST = 0.747), one nuclear intron (ΦST = 0.193) and eight microsatellite loci (FST = 0.035). In contrast, there was little genetic structure between Kangaroo Island and adjacent mainland regions within eastern Australia. One small population of Musk Ducks in Victoria (Lake Wendouree) differed from both Kangaroo Island and the remainder of mainland eastern Australia, possibly due to genetic drift exacerbated by inbreeding and small population size. The observed low pairwise distance between the eastern and western mtDNA lineages (0.36%) suggests that they diverged near the end of the Pleistocene, a period characterised by frequent shifts between wet and arid conditions in central Australia. Our genetic results corroborate the display call divergence and Mathews’ (Austral Avian Record 2:83–107, 1914) subspecies classification, and confirm that eastern and western populations of Musk Duck are currently isolated from each other.
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References
Anonymous (1988a) Recovery round-up. Corella 12:64–67
Anonymous (1988b) Wetlands conservation program for Victoria. Department of Conservation, Forests and Lands, Water Victoria and Ministry for Planning and Environment, Melbourne, Australia
Anonymous (2000) Recovery round-up. Corella 24:51–52
Ayliffe LK, Marianelli PC, Moriarty KC, Wells RT, McCulloch MT, Mortimer GE, Hellstrom JC (1998) 500 ka precipitation record from southeastern Australia: evidence for interglacial relative aridity. Geology 26:147–150
Barrett G, Silcocks A, Barry S, Cunningham R, Poulter R (2003) The new atlas of Australian birds. Royal Australasian Ornithologists Union, Hawthorn East, Australia
Bartley D, Bagley M, Gall G, Bentley B (1992) Use of linkage disequilibrium data to estimate effective size of hatchery and natural fish populations. Conserv Biol 6:365–375
Baxter C (1989) An annotated list of the birds of Kangaroo Island. Angel Press, Kingscote, Australia
Biro PA, Dingemase NJ (2009) Sampling bias resulting from animal personality. Trends Ecol Evol 24:66–67
Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. Biotechniques 31:24–27
Bowler JM, Teller JT (1986) Quaternary evaporites and hydrological changes, Lake Tyrrell, northwest Victoria. Aust J Earth Sci 33:43–63
Bowler JM, Huang Q, Chen KZ, Head MJ, Yuan BY (1986) Radiocarbon dating of Playa Lake hydrologic changes––examples from northwestern China and central Australia. Palaeogeogr Palaeoclimatol Palaeoecol 54:241–260
Briggs S (1992) Movement patterns and breeding characteristics of arid zone ducks. Corella 16:15–22
Brooker MG, Ridpath MG, Estbergs AJ, Bywater J, Hart DS, Jones MS (1979) Bird observations on the north-western Nullarbor Plain and neighbouring regions, 1967–1978. Emu 79:177–190
Bruford MW, Hanotte O, Brookfield JFY, Burke T (1992) Single locus and multi-locus fingerprinting. In: Hoelzel AR (ed) Molecular genetics analysis of population––a molecular approach. IRL Press, Oxford, UK, pp 227–229
Bryant S, Jackson J (1999) Tasmania threatened fauna handbook: what, where and when to protect Tasmania’s threatened animals. Threatened species unit. Parks and Wildlife Service, Hobart, Australia
Burbidge AA, Casperson KD, Fuller PJ (1987) Birds. In: McKenzie NL, Robinson AC (eds) A biological survey of the Nullarbor region south and western australia in 1984. D. J. Woolman Government Printer, Adelaide, Australia, pp 153–178
Campbell AJ (1901) Nest and eggs of Australian birds, including the geographical distribution of the species and popular observation thereon. Pawson & Brailsford, Sheffield, Australia
Chapple DG, Keogh JS, Hutchinson MN (2004) Molecular phylogeography and systematics of the arid-zone members of the Egernia whitii (Lacertilia: Scincidae) species group. Mol Phylogenet Evol 33:549–561
Congreve D, Congreve P (1982) The beach census. Royal Australian Ornithologists Union Report 3:28–43
Congreve D, Congreve P (1985) Wardens’ report: Kanidal Beach counts. Royal Australian Ornithologists Union Report 9:50–65
Cracraft J (1986) Origin and evolution of continental biotas––speciation and historical congruence within the Australian avifauna. Evolution 40:977–996
Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295
Davey C (1989) A comment on declining numbers of Musk Duck in Canberra. Canberra Bird Notes 14:3–5
Delacour J (1959) The waterfowl of the world, vol 3. Country Life Ltd., London, UK
Donnellan SC, Armstrong J, Pickett M, Milne T, Baulderstone J, Hollfelder T, Bertozzi T (2009) Systematic and conservation implications of mitochondrial DNA diversity in emu-wrens, Stipiturus (Aves: Maluridae). Emu 109:143–152
El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree Argania spinosa (L) Skeels endemic to Morocco. Theor Appl Genet 92:832–839
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1:47–50
Ford J (1971) Distribution and taxonomy of southern birds in the Great Victorian Desert. Emu 71:27–36
Ford J (1987) Minor isolates and minor geographical barriers in avian speciation in continental Australia. Emu 87:90–102
Frith HJ (1957) Breeding and movement of wild ducks in inland New South Wales. C.S.I.R.O. Wildlife Research 2:19–31
Frith HJ (1959) The ecology of wild ducks in inland New South Wales II. Movements. C.S.I.R.O. Movements. C.S.I.R.O. Wildlife Research 4:108–131
Frith HJ (1962) Movement of the Grey Teal, Anas gibberifrons Muller (Anatidae). C.S.I.R.O. Wildlife Research 7:50–70
Frith HJ (1967) Waterfowl in Australia. Angus and Robertson Ltd, Sydney, Australia
Fullagar PJ, Carbonell M (1986) The display postures of the Musk Duck. Wildfowl 37:142–150
Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: Frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst 34:397–423
Goodrick GN (1970) A survey of wetlands of coastal New South Wales. C.S.I.R.O. Division of Wildlife Research Technical Memorandum 5
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Guay PJ (2007) A new record for the longest banding recovery distance in Musk Ducks Biziura lobata. Corella 31:13–14
Guay PJ, Mulder RA (2005) Isolation and characterization of microsatellite markers in the Musk Duck (Biziura lobata: Aves) and their application to other waterfowl species. Mol Ecol Notes 5:249–252
Guay PJ, Mulder RA (2007) Skewed paternity distribution in the extremely size dimorphic Musk Duck (Biziura lobata). Emu 107:190–195
Hardy OJ, Vekemans X (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Hardy OJ, Charbonnel N, Freville H, Heuertz M (2003) Microsatellite allele sizes: A simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482
Hartert E (1931) Types of birds in the Tring Museum. D. Gregory M. Mathews’s type of Australian birds. Novitates Zoologicae 37:35–52
Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 21:160–174
Holm S (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistic 6:65–70
Johnsgard PA (1966) Behavior of the Australian Musk Duck and Blue-billed Duck. Auk 83:98–110
Johnsgard PA, Carbonell M (1996) Ruddy Ducks and other stifftails: Their behavior and biology. University of Oklahoma Press, Norman, USA
Johnson JA, Dunn PO (2006) Low genetic variation in the Heath Hen prior to extinction and implications for the conservation of Prairie-Chicken populations. Conserv Genet 7:37–48
Joseph L, Adcock GJ, Linde C, Omland KE, Heinsohn R, Chesser RT, Roshier D (2009) A tangled tale of two teal: population history of the Grey Anas gracilis and Chestnut Teal A. castanea of Australia. J Avian Biol 40:430–439
Keast A (1981) Ecological biogeography of Australia. Dr W. Junk BV Publishers, The Hague, Netherlands
Keogh JS, Scott IAW, Hayes C (2005) Rapid and repeated origin of insular gigantism and dwarfism in Australian Tiger Snakes. Evolution 59:226–233
Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kulikova IV, Drovetski SV, Gibson DD, Harrigan RJ, Rohwer S, Sorenson MD, Winker K, Zhuravlev YN, McCracken KG (2005) Phylogeography of the Mallard (Anas platyrhynchos): Hybridization, dispersal, and lineage sorting contribute to complex geographic structure. Auk 122:949–965
Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lowe VT (1966) Notes on the Musk Duck. Emu 65:279–290
Marchant S, Higgins PJ (1990) Handbook of Australian, New Zealand, and Antarctic birds. Pelican to Ducks, vol 1B. Oxford University Press, Oxford, UK
Martindale J (1980) The warden’s report, 1977–1979: Birds. Royal Australian Ornithologists Union Report 1:4–40
Mathews GM (1914) Additions and corrections to my list of the birds of Australia. Austral Avian Record 2:83–107
Mathews GM (1927) Systema avium australasianarum. British Ornithologists’ Union, Tring, UK
McCracken KG (1999) Systematics, ecology, and social biology of the Musk Duck (Biziura lobata) of Australia. Ph.D. Dissertation, Louisiana State University
McCracken KG (2005) Musk Duck Biziura lobata. In: Kear J (ed) Ducks, geese and swans. Oxford University Press, New York, USA, pp 213–217
McCracken KG, Afton AD, Paton DC (2000) Nest and eggs of Musk Ducks Biziura lobata at Murray Lagoon, Cape Gantheaume Conservation Park, Kangaroo Island, South Australia. South Australian Ornithologist 33:65–70
McCracken KG, Fullagar PJ, Slater EC, Paton DC, Afton AD (2002) Advertising displays of male Musk Ducks indicate population subdivision across the Nullarbor Plain of Australia. Wildfowl 53:137–154
McCracken KG, Hemmings J, Paton DC, Afton AD (2003) Capture methods for Musk Ducks. Wildfowl 54:209–212
McCracken KG, Bulgarella M, Johnson KP, Kuhner MK, Trucco J, Valqui TH, Wilson RE, Peters JL (2009) Gene flow in the face of countervailing selection: adaptation to high-altitude hypoxia in the βA hemoglobin subunit of Yellow-billed Pintail in the Andes. Mol Biol Evol 26:815–827
Miller GH, Magee JW, Jull AJT (1997) Low-latitude glacial cooling in the Southern Hemisphere from amino-acid racemization in Emu eggshells. Nature 385:241–244
Moore WS (1995) Inferring phylogenies from mtDNA variation––mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718–726
Morgan DG (1954) Seasonal changes in population of Anatidae at the Laverton saltworks, Victoria. Emu 54:263–278
Moritz C (1994) Defining evolutionarily-significant-units for conservation. Trends Ecol Evol 9:373–375
Nanson GC, Price DM, Short SA (1992) Wetting and drying of Australia over the past 300 Ka. Geology 20:791–794
Neaves LE, Zenger KR, Prince RIT, Eldridge MDB, Cooper DW (2009) Landscape discontinuities influence gene flow and genetic structure in a large, vagile Australian mammal, Macropus fuliginosus. Mol Ecol 18:3363–3378
Nei M, Takahata N (1993) Effective population-size, genetic diversity, and coalescence time in subdivided populations. J Mol Evol 37:240–244
Palumbi SR, Cipriano F, Hare MP (2001) Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution 55:859–868
Parker SA, Eckert HJ, Ragless GB (1985) An annotated checklist of the birds of South Australia, part 2A: waterfowl. The South Australian Ornithological Association, Adelaide, Australia
Paton DC, Carpenter G, Sinclair RG (1994) A second bird atlas of the Adelaide region. Part 1. Changes in the distribution of birds: 1974–1975 vs 1984–1985. South Australian Ornithologist 31:151–193
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Peel D, Ovenden JR, Peel SL (2004) NeEstimator: software for estimating effective population size, version 1.3. Queensland Government, Department of Primary Industries and Fisheries
Peters JL, Gretes W, Omland KE (2005) Late Pleistocene divergence between eastern and western populations of Wood Ducks (Aix sponsa) inferred by the ‘isolation with migration’ coalescent method. Mol Ecol 14:3407–3418
Peters JL, Zhuravlev Y, Fefelov I, Logie A, Omland KE (2007) Nuclear loci and coalescent methods support ancient hybridization as cause of mitochondrial paraphyly between Gadwall and Falcated Duck (Anas spp.). Evolution 61:1992–2006
Phillips JC (1926) A natural history of the ducks, vol 4. Houghton Mifflin, Boston, USA
Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503
Poiani A (2006) Effects of floods on distribution and reproduction of aquatic birds. Adv Ecol Res 39:63–83
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic-markers. Evolution 43:258–275
Ramsey EP (1867) Illustration of Australian oology. Ibis 3:413–421
Raymond M, Rousset F (1995) Genepop (Version-1.2)––population-genetics software for exact tests and ecumenicism. J Hered 86:248–249
Robinson FN, Robinson AH (1970) Regional variation in the visual and acoustic signals of the male Musk Duck, Biziura lobata. C.S.I.R.O. Wildlife Research 15:73–78
Robinson AC, Casperson KD, Hutchinson MN (2000) A list of the vertebrates of South Australia. Department of Environment and Heritage, Adelaide, Australia
Roshier DA, Robertson AI, Kingsford RT (2002) Responses of waterbirds to flooding in an arid region of Australia and implications for conservation. Biol Conserv 106:399–411
Salinas M, Bunce M, Cancilla D, Alpers DL, Spencer PBS (2009) Divergent lineages in the Heath Mouse (Pseudomys shortridgei) are indicative of major contraction to geographically isolated refugia on the eastern and western sides of Australia during the early Pleistocene. Australian Journal of Zoology 57:41–47
Saunders DA, Ingram JA (1995) Birds of southwestern Australia: an atlas of changes in the distribution and abundance of the wheatbelt avifauna. Surrey Beatty & Sons, Chipping Norton, Australia
Schodde R, Mason IJ (1999) The directory of Australian Birds: passerines. CSIRO Publishing, Collingwood, Australia
Scribner KT, Petersen MR, Fields RL, Talbot SL, Pearce JM, Chesser RK (2001) Sex-biased gene flow in Spectacled Eiders (Anatidae): Inferences from molecular markers with contrasting modes of inheritance. Evolution 55:2105–2115
Serventy VN (1946) Display in the Musk Duck. Emu 45:318–321
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
Sonsthagen SA, Talbot SL, Lanctot RB, Scribner K, McCracken KG (2009) Hierarchical spatial genetic structure of Common Eiders (Somateria mollissima) breeding along a migratory corridor. Auk 126:744–754
Sorenson MD, Fleischer RC (1996) Multiple independent transpositions of mitochondrial DNA control region sequences to the nucleus. Proc Natl Acad Sci USA 93:15239–15243
Sorenson MD, Ast JC, Dimcheff DE, Yuri T, Mindell DP (1999) Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol Phylogenet Evol 12:105–114
Specht RL (1981) Major vegetation formations in Australia. In: Keast A (ed) Ecological biogeography of Australia. Junk, The Hague, Netherlands, pp 163–297
Spencer PBS, Rhind SG, Eldridge MDB (2001) Phylogeographic structure within Phascogale (Marsupialia: Dasyuridae) based on partial cytochrome b sequence. Australian Journal of Zoology 49:369–377
Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989
Stranger RH (1961) Display in the Musk Duck. Western Australian Naturalist 7:210–211
Thomas R, Wheeler J (1983) Birds of the Ballarat region. Roger Thomas, Linton, Victoria
Todd FS (1997) Natural history of the waterfowl. Ibis Publishing Company, Vista, USA
Toon A, Mather PB, Baker AM, Durrant KL, Hughes JM (2007) Pleistocene refugia in an arid landscape: analysis of a widely distributed Australian passerine. Mol Ecol 16:2525–2541
Victorian Department of Sustainability and Environment (2007) Advisory list of threatened vertebrate fauna in Victoria––2007. Department of Sustainability and Environment, East Melbourne
Wasson RJ (1982) Landform development in Australia. In: Barker WP, Greenslade PJM (eds) Evolution of the flora and fauna of arid Australia. Peacocke, Frewville, Australia, pp 23–33
Wetlands International (2006) Waterbird population estimates, 4th edn. Wetland International, Wanegingen, The Netherlands
Wood VJ (1960) Recovery of a banded Giant Petrel. South Australian Ornithologist 23:42
Worthy TH (2002) The New Zealand Musk Duck (Biziura delautouri Forbes, 1892). Notornis 49:19–28
Acknowledgements
Our research was supported by funding from the Department of Zoology and the Faculty of Science of the University of Melbourne, le Fonds québécois de la recherche sur la nature et les technologies, the Hermon Slade Foundation, the Holsworth Wildlife Research Endowment, Birds Australia, the M.A. Ingram Trust, the Norman Wettenhall Foundation, Louisiana State University Agricultural Center, College of Agriculture, Cooperative Fish and Wildlife Research Unit, Board of Regents, Museum of Natural Science, and School of Renewable Natural Resources. We thank the South Australia Department of Environment and Heritage and Wildlife personnel for their assistance with fieldwork and the following institutions for allowing access to their tissue collections and/or for allowing us to take samples from study skins and/or skeletons: The Australian Museum, the Bourne Bird Museum, CSIRO Sustainable Ecosystems––Australian National Wildlife Collection, the Department of Ornithology of the American Museum of Natural History, Museum Victoria, the Queen Victoria Museum and Art Gallery, the Queensland Museum, the South Australian Museum, the Tasmanian Museum, the University of Alaska Museum and the Western Australian Museum. J. Van Remsen and S. Taylor provided helpful comments on an earlier version of the manuscript. Blood samples were collected under the University of Melbourne Faculty of Science Animal Experimentation and Ethics Committee Register 02088, 04064, 05122, 06186, permits 10002458, 10003407, and 10004007, from the Department of Sustainability and Environment, Victoria and permits SF005117, SF005760, SF006080 and SF006659 from the Department of Environment and Conservation Western Australia. The use of trade, product, industry or firm names or products is for informative purposes only and does not constitute an endorsement by the U.S. Government or the U.S. Geological Survey.
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Guay, PJ., Chesser, R.T., Mulder, R.A. et al. East–west genetic differentiation in Musk Ducks (Biziura lobata) of Australia suggests late Pleistocene divergence at the Nullarbor Plain. Conserv Genet 11, 2105–2120 (2010). https://doi.org/10.1007/s10592-010-0097-5
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DOI: https://doi.org/10.1007/s10592-010-0097-5