Skip to main content
SpringerLink
Log in

Morphological and molecular evidence of population divergence in a widespread shorebird across its southern mainland Australian distribution

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

We characterize geographical variation in the genetics, ecology, morphology and plumage of the Hooded Plover Charadrius cucullatus, a threatened shorebird widespread on coasts (south-east) and saltlakes (south-west) across the southern mainland of Australia. We confirm the distinctness of populations on either side of the Nullabor Plain/Great Australian Bight indicating that this apparent biogeographic barrier to terrestrial flora and fauna also influenced the phylogeographic pattern of a resident shorebird which is dependent on access to saline/hypersaline water. Western birds are genetically distinct, larger and have darker plumage than those in the east. Distinct ecological differences also exist, with eastern birds being resident, usually occurring on ocean beaches, with generalised diets and seasonal, solitary breeding. Western birds are nomadic, breeding when suitable conditions prevail, and exhibit more specialized diets, and may at times breed semi-colonially. Within the extensive eastern population, genetic analyses revealed an isolation by distance pattern, as well as genetic evidence of a long distance dispersal event. South Australian birds are distinct from Victorian birds, but cluster closely with Victorian birds in all genetic analyses. The western population features little genetic structuring, consistent with nomadism and congregatory behavior associated with drought/flood events. The distinctness of western populations found using multiple lines of evidence and the lack of evidence for any recent migration events across the Nullabor Plain, suggests that previously described subspecies warrant reinstatement, and that these evolutionary units require conservation assessment, as has been recognized by national conservation authorities. Conservation management of the eastern population should occur across its distribution, taking care to capture the genetic variability which is evident within this population. Further exploration of genetic variation between Eastern states is suggested.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allen JA (1877) The influence of physical conditions in the genesis of species. Rad Rev 1:108–140

    Google Scholar 

  • Akbari M, Wenzl P, Caig V et al (2006) Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor Appl Genet 113:1409–1420

    CAS  PubMed  Google Scholar 

  • Almalki M, Kupán K, Carmona-Isunza MC, López P, Veiga A, Kosztolányi A, Székely T, Küpper C (2016) Morphological and genetic differentiation among Kentish Plover Charadrius alexandrinus populations in Macaronesia. Ardeola 64:3–16

    Google Scholar 

  • Barrett G, Silcocks A, Barry S, Cunningham R, Poulter R (2003) The New Atlas of Australian Birds. Royal Australasian Ornithologists Union, Melbourne

    Google Scholar 

  • Bergmann C (1847) Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Gött Stud 3:595–708

    Google Scholar 

  • Byrne M, Yeates DK, Joseph L, Kearney M, Bowler J, Williams MAJ, Cooper S, Donnellan SC, Keogh JS, Leys R, Melville J, Murphy D, Porch N, Wyrwoll K-H (2008) Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Mol Ecol 17:4398–4417

    CAS  PubMed  Google Scholar 

  • Byrne M, Steane DA, Joseph L, Yeates DK, Jordan GJ, Crayn D, Aplin K, Cantrill DJ, Cook LG, Crisp MD, Keogh JS, Melville J, Moritz C, Porch N, Kale Sniderman JM, Sunnucks P, Weston PH (2011) Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. J Biogeogr 38:1635–1656

    Google Scholar 

  • Cameron D, Weston M (1999) The Hooded Plover: First confirmed record in Queensland, the longest movement yet recorded, and a discussion of the range contraction in eastern Australia. Aust Bird Watcher 18:8–18

    Google Scholar 

  • Canales-Delgadillo JC, Scott-Morales L, Korb J (2012) The influence of habitat fragmentation on genetic diversity of a rare bird species that commonly faces environmental fluctuations. J Avian Biol 43:168–176

    Google Scholar 

  • Cattell RB (1966) The scree test for the number of factors. Multivar Behav Res 1:245–276

    CAS  Google Scholar 

  • Cronin MA, Grand JB, Esler D, Derksen DV, Scribner KT (1996) Breeding populations of Northern Pintails have similar mitochondrial DNA. Can J Zool 74:992–999

    Google Scholar 

  • Cruz VMV, Kilian A, Dierig DA (2013) Development of DArT marker platforms and genetic diversity assessment of the US collection of the new oilseed crop lesquerella and related species. PLoS ONE 8:e64062. https://doi.org/10.1371/journal.pone.0064062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuttriss A, Maguire GS, Ehmke G, Weston MA (2015) Breeding habitat selection in an obligate beach bird: a test of the food resource hypothesis. Marine Fresh Res 66:841–846

    Google Scholar 

  • Department of the Environment (2014) Conservation Advice Thinornis rubricollis rubricollis Hooded Plover (eastern). Department of the Environment, Canberra

    Google Scholar 

  • Dolman G, Joseph L (2012) A species assemblage approach to comparative phylogeography of birds in southern Australia. Ecol Evol 2:354–369

    PubMed  PubMed Central  Google Scholar 

  • Dolman G, Joseph L (2015) Evolutionary history of birds across southern Australia: structure, history and taxonomic implications of mitochondrial DNA diversity in an ecologically diverse suite of species. Emu 115:35–48

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Driessen J, Maguire G (2015) Report on the 2014 Biennial Hooded Plover Count. Birdlife Australia, Carlton

    Google Scholar 

  • Eberhart-Phillips LJ, Hoffman JI, Brede EG, Zefania S, Kamrad MJ, Székely T, Bruford MW (2015) Contrasting genetic diversity and population structure among three sympatric Madagascan shorebirds: parallels with rarity, endemism, and dispersal. Ecol Evol 5:997–1010

    PubMed  PubMed Central  Google Scholar 

  • Ehmke G, Maguire GS, Bird T, Ierodiaconou D, Weston MA (2016) An obligate beach bird selects sub-, inter-and supra-tidal habitat elements. Estuarine Coast Shelf Sci 181:266–276

    Google Scholar 

  • Ekanayake KB, Weston MA, Nimmo DG, Maguire GS, Endler JA, Küpper C (2015) The bright incubate at night: sexual dichromatism and adaptive incubation division in an open-nesting shorebird. Proc R Soc (Lond) 282(1806):20143026

    Google Scholar 

  • Ford J, Sedgwick EH (1967) Bird distribution in the Nullarbor Plain and Great Victoria Desert region, Western Australia. Emu 67:99–124

    Google Scholar 

  • Funk WC, Mullins TD, Haig SM (2007) Conservation genetics of Snowy Plovers (Charadrius alexandrinus) in the Western Hemisphere: population genetic structure and delineation of subspecies. Conserv Genet 8:1287–1309

    Google Scholar 

  • Garnett S, Szabo J, Dutson G (2011) The action plan for Australian birds 2010. CSIRO Publishing, Clayton

    Google Scholar 

  • Geering A, Agnew L, Harding S (2007) Shorebirds of Australia. CSIRO Publishing, Collingwood

    Google Scholar 

  • Georges A, Gruber B, Pauly GB, White D, Adams M, Young MJ, Kilian A, Zhang X, Shaffer HB, Unmack PJ (2018) Genomewide SNP markers breathe new life into phylogeography and species delimitation for the problematic short-necked turtles (Chelidae: Emydura) of eastern Australia. Mol Ecol 27:5195–5213

    PubMed  Google Scholar 

  • Gloger CL (1833) Das Abiindern der Vogel durch Einfluss des Klimas. A Schultz & Co, Breslau

    Google Scholar 

  • Gruber B, Unmack PJ, Berry OF, Georges A (2018) DARTR: an r package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Mol Ecol Resour 18:691–699

    PubMed  Google Scholar 

  • Guay PJ, Chesser RT, Mulder RA, Afton AD, Paton DC, McCracken KG (2010) East–west genetic differentiation in Musk Ducks (Biziura lobata) of Australia suggests late Pleistocene divergence at the Nullarbor Plain. Conserv Genet 11:2105–2120

    Google Scholar 

  • Hawkins BA, Diniz-Filho JAF, Soeller SA (2005) Water links the historical and contemporary components of the Australian bird diversity gradient. J Biogeogr 32:1035–1042

    Google Scholar 

  • Howes J, Bakewell D (1989) Shorebirds study manual. AWB Publication, Kuala Lumpur

    Google Scholar 

  • Keast A (1959) Australian birds: their zoogeography and adaptations to an arid continent. Biogeography and ecology in Australia. Springer, Dordrecht, pp 89–114

    Google Scholar 

  • Kilian A, Wenzl P, Huttner E, Carling J, Xia L, Blois H, Caig V, Heller-Uszynska K, Jaccoud D, Hopper C, Aschenbrenner-Kilian M (2012) Diversity arrays technology: a generic genome profiling technology on open platforms. In: Pompanon F, Bonin A (eds) Data production and analysis in population genomics: methods and protocols. Humana Press, New York, pp 67–89

    Google Scholar 

  • Kvistad L, Ingwersen D, Pavlova A, Bull JK, Sunnucks P (2015) Very low population structure in a highly mobile and wide-ranging endangered bird species. PLoS ONE 10:e0143746

    PubMed  PubMed Central  Google Scholar 

  • Larson WA, Seeb JE, Pascal CE, Templin WD, Seeb LW (2015) Single-nucleotide polymorphisms (SNPs) identified through genotyping-by-sequencing improve genetic stock identification of Chinook Salmon (Oncorhynchus tshawytscha) from western Alaska. Can J Fish Aquat Sci 71:698–708

    Google Scholar 

  • Leaché AD, Banbury BL, Felsenstein J, de Oca AN, Stamatakis A (2015) Short tree, long tree, right tree, wrong tree: new acquisition bias corrections for inferring SNP phylogenies. Syst Biol 64:1032–1047. https://doi.org/10.1093/sysbio/syv053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JY, Edwards SV (2008) Divergence across Australia's Carpentarian barrier: statistical phylogeography of the Red-backed Fairy Wren (Malurus melanocephalus). Evol 62:3117–3134

    Google Scholar 

  • Marchant S, Higgins P (1993) Handbook of Australian New Zealand and Antarctic Birds. Oxford University Press, Melbourne

    Google Scholar 

  • Mathews GM (1912) A reference-list to the birds of Australia. Witherby, London

    Google Scholar 

  • McCracken KG, Fullagar PJ, Slater EC, Paton DC, Afton AD (2013) Advertising displays of male Musk Ducks indicate population subdivision across the Nullabor Plain of Australia. Wildfowl 53:137–154

    Google Scholar 

  • Melville J, Haines ML, Boysen K, Hodkinson L, Kilian A, Smith Date KL, Potvin DA, Parris KM. (2017) Identifying hybridization and admixture using SNPs: application of the DArTseq platform in phylogeographic research on vertebrates. R Soc Open Sci 19:161061

    Google Scholar 

  • Menkhorst P, Rogers D, Clarke R, Davies J, Marsack P, Franlin K (2017) The Australian bird guide. CSIRO, Collingwood

    Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010a) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA pp 1–8

  • Miller MP, Haig SM, Gratto-Trevor CL, Mullins TD (2010b) Subspecies status and population genetic structure in Piping Plover (Charadrius melodus). Auk 127:57–71

    Google Scholar 

  • Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. TREE 9:373–375

    CAS  PubMed  Google Scholar 

  • Pedler RD, Ribot RFH, Bennett ATD (2014) Extreme nomadism in desert waterbirds: flights of the banded stilt. Biol Lett 10:20140547

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peel MC, Finlayson BL, Mcmahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 4:439–473

    Google Scholar 

  • Petch N, Maguire GS, Schlacher TA, Weston MA (2018) Motivations and behavior of off-road drivers on sandy beaches. Ocean Coast Manage 163:82–91

    Google Scholar 

  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, De Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raj A, Stephens M, Pritchard JK (2014) fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197:573–589. https://doi.org/10.1534/genetics.114.164350

    Article  PubMed  PubMed Central  Google Scholar 

  • Rawlinson PA (1974) Biogeography and ecology of the reptiles of Tasmania and the Bass Strait area. Biogeography and ecology in Tasmania. Springer, Dordrecht, pp 291–338

    Google Scholar 

  • Rogers KG, Rogers DI, Weston MA (2014) Prolonged and flexible primary moult overlaps extensively with breeding in beach-nesting Hooded Plovers Thinornis rubricollis. Ibis 156:840–849

    Google Scholar 

  • Runge CA, Tulloch A, Hammill E, Possingham HP, Fuller RA (2015) Geographic range size and extinction risk assessment in nomadic species. Cons Biol 29:865–876

    Google Scholar 

  • Sansaloni CP, Petroli CD, Carling J, Hudson CJ, Steane DA, Myburg AA, Grattapaglia D, Vaillancourt RE, Kilian A. (2010) A high-density Diversity Arrays Technology (DArT) microarray for genome-wide genotyping in Eucalyptus. Plant Methods. 6:16

  • Sansaloni C, Petroli C, Jaccoud D, Carling J, Detering F, Grattapaglia D, Kilian A. (2011) Diversity Arrays Technology (DArT) and next-generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus. BioMed Cent 5:54

  • Schodde R, Mason IJ (1999) Directory of Australian birds: passerines: Passerines. CSIRO publishing, Clayton

    Google Scholar 

  • Singor M (2008) Inland movements of the Hooded Plover Thinornis rubricollis tregellasi in Western Australia. Stilt 55:25–26

    Google Scholar 

  • Soler JJ, Martinez JG, Soler M, Møller AP (1999) Genetic and geographic variation in rejection behavior of cuckoo eggs by European Magpie populations: an experimental test of rejecter-gene flow. Evolution 53:947–956

    PubMed  Google Scholar 

  • Thom BG, Short AD (2006) Introduction: Australian coastal geomorphology 1984–2004. J Coast Res 22:1–10

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Vidal M, Hernandez MA, Luis A, Dominguez J (2015) Lack of genetic structure in Kentish Plover Charadrius alexandrinus from the Iberian coast. What’s wrong with the endangered north-western population? Bird Conserv Int 25:153–165

    Google Scholar 

  • Wenzl P, Carling J, Kudrna D, Jaccoud D, Huttner E, Kleinhofs A, Kilian A (2004) Diversity arrays technology (DArT) for whole-genome profiling of barley. Proc Natl Acad Sci USA 101:9915–9920. https://doi.org/10.1073/pnas.0401076101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weston MA (1998) Some undescribed aggressive behaviours, displays and calls of the Hooded Plover in Western Australia. West Aust Nat 22:105–114

    Google Scholar 

  • Weston M (2007) The foraging and diet of non-breeding Hooded Plovers Thinornis rubricollis in relation to habitat type. J R Soc West Aust 90:89–95

    Google Scholar 

  • Weston M, Elgar M (2000) The effect of a major rainfall event on Hooded Plovers on a salt-lake in Western Australia. Emu 100:64–69

    Google Scholar 

  • Weston MA, Elgar MA (2007) Responses of incubating Hooded Plovers (Thinornis rubricollis) to disturbance. J Coast Res 23:569–576

    Google Scholar 

  • Weston M, Kraaijeveld-Smit F, McIntosh R, Sofrondis G, Elgar M (2004) A male-biased sex ratio in non-breeding Hooded Plovers on a saltlake in Western Australia. Pac Cons Biol 9:273–277

    Google Scholar 

  • Weston MA, Ehmke GC, Maguire GS (2009) Manage one beach or two? Movements and space-use of the threatened Hooded Plover (Thinornis rubricollis) in south-eastern Australia. Wildl Res 36:289–298

    Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zaccara S, Crosa G, Vanetti I, Binelli G, Childress B, McCulloch G, Harper DM (2011) Lesser Flamingo Phoeniconaias minor as a nomadic species in African shallow alkaline lakes and pans: genetic structure and future perspectives. Ostrich 82:95–100

    Google Scholar 

Download references

Acknowledgements

This research was conducted under Department of Conservation and Land Management (CALM) permits (NE001169, SF001423 and ES001031), Vic. Department of Environment, Water, Land and Planning permits (RP97208, RP96113, RP95067, 10007183 and 10005938, 10007918, 10008428), SA Department of Environment and Water permit (E26037-8), Parks Victoria permits (NP978/095, NP945/156 and NP67/011), Ethics Approval Permits (UoM AEEC 6540720921120; Deakin AEC A52-2009, A34-2011, B10-2016, B13-2017), and appropriate Australian Bird and Bat Banding Scheme (ABBBS) permits (1763/1). Part of the write-up was supported by the Beach Ecology and Conservation Hub (BEACH; Venus Bay).

Author information

Authors and Affiliations

  1. Deakin University, Geelong, Australia

    Michael A. Weston

  2. School of Life and Environmental Sciences, Faculty of Engineering, Science and the Built Environment, 221 Burwood Highway, Burwood, VIC, 3125, Australia

    Michael A. Weston

  3. Museums Victoria, GPO Box 666, Melbourne, VIC, 3001, Australia

    Kylea Clarke & Joanna Sumner

  4. BirdLife Australia, Suite 2-05, 60 Leicester Street, Carlton, VIC, 3053, Australia

    Grainne S. Maguire

Authors
  1. Michael A. Weston
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kylea Clarke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Grainne S. Maguire
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joanna Sumner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael A. Weston.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 892 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Weston, M.A., Clarke, K., Maguire, G.S. et al. Morphological and molecular evidence of population divergence in a widespread shorebird across its southern mainland Australian distribution. Conserv Genet 21, 757–770 (2020). https://doi.org/10.1007/s10592-020-01286-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-020-01286-2

Keywords

Search

Navigation