Skip to main content
SpringerLink
Log in

Conservation status of the White-Bellied Sea-Eagle Haliaeetus leucogaster in Australia determined using mtDNA control region sequence data

  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Considered to have a declining world population, concern has been expressed in recent years over the conservation status of the White-bellied Sea-Eagle Haliaeetus leucogaster (Gmelin, 1788) within Australia. We used mitochondrial (mtDNA) control region sequence data to investigate the current distribution of genetic variation in this species at the continental level and within and between specified regional units. We were specifically interested in identifying breaks in genetic connectivity between the west and east of the continent and between Tasmania and the Australian mainland. We also investigated the likelihood of a bottleneck at the time of colonisation, and propose hypotheses regarding colonisation history. Sequence data were obtained from 128 individuals describing 15 haplotypes. Overall, diversity was low and AMOVA results failed to provide any significant level of genetic subdivision between regions. We suggest that the population expanded from a bottleneck approximately 160,000 years ago during the late Pleistocene, and spread throughout the continent through a contiguous range expansion. There is insufficient evidence to suggest division of the population into different units for conservation management purposes based on the theoretical definition of the ‘evolutionary significant unit’. It is clear from the analysis that there are signatures of both historical and contemporary processes affecting the current distribution. Additional sampling and confirmation of the perceived pattern of population structure using a nuclear marker is recommended to validate conservation monitoring and management at a continental scale.

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

Similar content being viewed by others

References

  • GR Allen (1989) Freshwater Fishes of Australia TFH Publications Brookvale, NSW

    Google Scholar 

  • JC Avise (1994) Molecular Markers, Natural History and Evolution Chapman & Hall NY

    Google Scholar 

  • JC Avise (1996) ArticleTitleThree fundamental contributions of molecular genetics to avian ecology and evolution IBIS 138 16–25

    Google Scholar 

  • JC Avise D Walker (1998) ArticleTitlePleistocene phylogeographic effects on avian populations and the speciation process Proc. Roy. Soc. Lond. Ser. B 265 457–463

    Google Scholar 

  • AJ Baker HD Marshall (1997) Mitochondrial control region sequences as tools for understanding evolution DP Mindell (Eds) Avian Molecular Evolution and Systematics Academic Press USA 51–82

    Google Scholar 

  • RM Ball S Freeman FC James E Bermingham (1988) ArticleTitlePhylogeographic population structure of Red-Winged Blackbirds assessed by mitochondrial DNA Proc. Natl. Acad. Sci. USA 85 1558–1562

    Google Scholar 

  • F Barker GF Barrowclough JG Groth (2002) ArticleTitleA phylogenetic hypothesis for passerine birds: Taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data Proc. Roy. Soc. Lond. Ser. B 269 295–308

    Google Scholar 

  • M Blakers SJJF Davies PN Reilly (1984) The Atlas of Australian Birds Royal Australian Ornithologists Union, Melbourne University Press Victoria

    Google Scholar 

  • R Chakraborty M Nei (1977) ArticleTitleBottleneck effects on average heterozygosity and genetic distance with the stepwise mutation model Evolution 31 347–356

    Google Scholar 

  • J Chappell (1983) ArticleTitleA revised sea-level record for the last 300,000 years from Papua New Guinea Search 14 IssueID3–4 99–101

    Google Scholar 

  • M Clement J Derington D Posada (2001) TCS: Estimating Gene Geneologies Version 1.13 Brigham Young University Provo, UT 84602, US

    Google Scholar 

  • P Clunie (1994) Action Statement No. 60 – White-bellied Sea-Eagle Department of Conservation & Natural Resources Victoria

    Google Scholar 

  • KA Crandall AR Templeton (1993) ArticleTitleEmpirical tests of some predictions from coalescent theory and application to intraspecific phylogeny reconstruction Genetics 134 959–969

    Google Scholar 

  • KA Crandall (1996) ArticleTitleMultiple interspecies transmissions of human and simian T-cell leukemia/lymphoma virus type I sequences Mol. Biol. Evol. 13 IssueID1 115–131

    Google Scholar 

  • P Crochet (2000) ArticleTitleGenetic structure of avian populations – allozymes revisited Mol. Ecol. 9 1463–1496

    Google Scholar 

  • JF Crow K Aoki (1984) ArticleTitleGroup Selection for polygenic behavioural trait: A differential proliferation model Proc. Natl. Acad. Sci. USA 79 2628–2631

    Google Scholar 

  • TE Dennis AFC Lashmar (1996) ArticleTitleDistribution and Abundance of White-bellied Sea-Eagles in South Australia Corella 20 IssueID3 93–102

    Google Scholar 

  • Double M, Abbott C (1998) A report on the development of a DNA-based sexing technique for the North Island kokako (Callaeas cinerae wilsoni). Division of Botony and Zoology, Australian National University, ACT 0200, Australia, Canberra, p. 12

  • SV Edwards (1993a) ArticleTitleMitochondrial gene geneology and gene flow among island and mainland populations of a sedentary songbird, the grey-crowned babbler (Pomatostomus temporalis) Evolution 47 IssueID4 1118–1137

    Google Scholar 

  • SV Edwards (1993b) ArticleTitleLong-distance gene flow in a cooperative breeder detected in geneologies of mitochondrial DNA sequences Proc. Roy. Soc. Lond. Ser. B 252 177–185

    Google Scholar 

  • PG Ericson L Christidis A Cooper M Irestedt J Jackson US Johansson JA Norman (2002) ArticleTitleA Gondwanan origin of passerine birds supported by DNA sequences of the endemic New Zealand wrens Proc. Roy. Soc. Lond. Ser. B 269 235–241

    Google Scholar 

  • ESRI (1996) ARCVIEW 3.2. Environmental Systems Research Institute, Inc

  • A Estoup P Jarne J Cornuet (2002) ArticleTitleHomology and mutation models at microsatellite loci and their consequences for population genetic analysis Mol. Ecol. 11 1591–1604

    Google Scholar 

  • L Excoffier PE Smouse JM Quattro (1992) ArticleTitleAnalysis of molecular variance inferred from metric distances among Dna haplotypes: Application to human mitochondrial DNA restriction data Genetics 131 479–491

    Google Scholar 

  • L. Excoffier (2004) ArticleTitlePatterns of DNA sequence diversity and genetic structure after a range expansion: Lessons from the infinite-island model Mol. Ecol. 13 853–864

    Google Scholar 

  • N Favaloro (1944) ArticleTitleThe White-Breasted Sea-Eagle Along the Murray River EMU XL111 233–242

    Google Scholar 

  • J Ferguson-Lees DA Christie (2001) Raptors of the World Christohper Helm London

    Google Scholar 

  • J Ford (1987) ArticleTitleMinor isolates and minor geographical barriers in avian speciation in continental Australia EMU 87 90–102

    Google Scholar 

  • Futuyma DJ (1986) Evolutionary Biology, 2nd. Sinauer Associates Inc., Sunderland, Massachusetts

  • TC Glenn S Wolfgang MJ Braun (1999) ArticleTitleEffects of a population bottleneck on whooping crane mitochondrial DNA variation Conserv. Biol. 13 IssueID5 1097–1107

    Google Scholar 

  • D Gopurenko JM Hughes (2002) ArticleTitleRegional patterns of genetic structure among Australian populations of the mud crab, Scylla serrata (Crustacea: Decapoda): Evidence from mitochondrial DNA Mar. Freshwater Res. 53 849–857

    Google Scholar 

  • AD Greenwood S Pääbo (1999) ArticleTitleNuclear insertion sequences of mitochondrial DNA predominate in hair but not in blood of elephants Mol. Ecol. 8 133–137

    Google Scholar 

  • T Hall (1999) ArticleTitleBIOEDIT: A user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucl. Acids Symp. Ser. 41 95–98

    Google Scholar 

  • Hewitt GM (2000) The genetic legacy of quartenary ice ages. Nature, 405(June), 907–913

    Google Scholar 

  • A Hodson (1992) Essential Genetics Bloomsbury London.

    Google Scholar 

  • RR Hudson (1990) Gene geneologies and the coalescent process DJ Futuyma J. Antonovics (Eds) Oxford Surveys in Evolutionary Biology Oxford University Press Oxford 1–44

    Google Scholar 

  • WG Hunt (1998) ArticleTitleRaptor floaters at Moffat’s equilibrium Oikos 82 IssueID1 191–197

    Google Scholar 

  • Huynen L, Millar CD, Scofield RP, Lambert DM (2003) Nuclear DNA sequences detect species limits in ancient moa. Nature, 425(September), 175–178

    Google Scholar 

  • DR Karns A O’Bannon HK Voris LA Weight (2000) ArticleTitleBiogeographical implications of mitochondrial DNA variation in the Bockadam snake (Cerberus rynchops, Sepentes: Homalopsinae) in Southeast Asia J. Biogeogr. 27 391–402

    Google Scholar 

  • Keast A (1981a) The evolutionary biogeography of Australian birds. In: Ecological Biogeography of Australia. (Ed. Keast A), pp. 1587–1635. Dr. W. Junk, The Hague–Boston–London

  • Keast A (1981b) Distributional patterns, regional biotas, and adaptations in the Australian biota: A synthesis. In: Ecological Biogeography of Australia. (Ed. Keast A), pp. 1895–1997 Dr. W. Junk, The Hague–Boston–London

  • Kikkawa J, Monteith GB, Ingram G (1981) Cape York Peninsula: Major region of faunal interchange. In: Ecological Biogeography of Australia. (Eds. Keast A), pp. 1697–1742. Dr. W. Junk, The Hague–Boston–London

  • S Kumar K Tamura M Nei (1993) MEGA: Molecular Evolutionary Genetics Analysis 2.0 Pennsylvania State University University Park

    Google Scholar 

  • DH Lunt LE Whipple BC Hyman (1998) ArticleTitleMitochondrial DNA variable number of tandem repeats (VNTRs): Utility and problems in molecular ecology Mol. Ecol. 7 1441–1455

    Google Scholar 

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

    Google Scholar 

  • McElroy D, Moran P, Bermingham E, Kornfield I (1991) REAP – The Restriction Enzyme Analysis Package Version 4.0. Dept of Zoology, University of Maine

  • McManus JW (1985) Marine speciation, tectonics and sea-level changes in Southeast Asia. Proceedings of the Fifth International Coral Reef Congress, pp. 133–138, Tahiti

  • B Mila DJ Girman M Kimura TB Smith (2000) ArticleTitleGenetic evidence for the effect of the postglacial population expansion of the phylogeography of a north American Songbird Proc. Roy. Soc. Lond. Ser. B 267 1033–1040

    Google Scholar 

  • Mindell DP (1997) Avian Molecular Evolution and Systematics, Academic Press, USA.

  • DP Mindell MD Sorenson DE Dimcheff (1998) ArticleTitleMultiple Independent origins of Mitochondrial Gene Order in Birds Proc. Natl. Acad. Sci. USA 95 10693–10697

    Google Scholar 

  • N Mooney N Brothers (1986) ArticleTitleSea Eagles’ greatest problem is nest disturbance, says NPWS FINTAS 9 39–41

    Google Scholar 

  • C Moritz (1994) ArticleTitleDefining ‘Evolutionarily Significant Units’ for conservation Trend Ecol. Evol. 9 IssueID10 373–375

    Google Scholar 

  • M Nei T Maruyama R Chakraborty (1975) ArticleTitleThe bottleneck effect and genetic variability in populations Evolution 29 IssueID1 1–10

    Google Scholar 

  • M Nei (1987) Molecular Evolutionary Systematics Columbia University Press New York

    Google Scholar 

  • JE Neigel (2002) ArticleTitleIs F ST obsolete? Conserv. Gene. 3 167–173

    Google Scholar 

  • I Newton (1991) Population limitation in birds of prey: A comparative approach CM Perrins JD Lebreton GJM Hirons (Eds) Bird Population Studies: Relevance to Conservation and Management Oxford University Press Oxford 3–21

    Google Scholar 

  • RA Nichols GM Hewitt (1994) ArticleTitleThe genetic consequences of long distance dispersal during colonisation Heredity 72 312–317

    Google Scholar 

  • Olsen PD (1995) Australian Birds of Prey: The Biology and Ecology of Raptors. University of New South Wales Press

  • Palumbi S, Martin A, Romano S, Owen McMillan W, Stice L (1991) The simple fool’s guide to PCR. Version 2.0. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, Honolulu.

  • D Posada KA Crandall AR Templeton (2000) ArticleTitleGeoDis: A program for the cladistic nested analysis of the geographical distribution of genetic haplotypes Mol. Ecol. 9 487–488

    Google Scholar 

  • TW Quinn (1992) ArticleTitleThe genetic legacy of mother goose: Phylogeographic patterns of lesser snow goose Chen caerulescens caerulescens maternal lineages Mol. Ecol. 1 105–117

    Google Scholar 

  • DM Rand (1996) ArticleTitleNeutrality tests of molecular markers and the connection between DNA polymorphism, demography, and conservation biology Conserv. Biol. 10 IssueID2 665–671

    Google Scholar 

  • N Ray M Currat L Excoffier (2003) ArticleTitleIntra-deme molecular diversity in spatially expanding populations Mol. Biol. Evol. 20 IssueID1 76–86

    Google Scholar 

  • AR Rogers H Harpending (1992) ArticleTitlePopulation growth makes waves in the distribution of pairwise genetic differences Mol. Biol. Evol. 9 IssueID3 552–569

    Google Scholar 

  • J Rozas R Rozas (1999) ArticleTitleDnaSP Version 3: An integrated program for molecular population genetics and molecular evolutionary analysis Bioinformatics 15 174–175

    Google Scholar 

  • S Schneider L Excoffier (1999) ArticleTitleEstimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: Application to human mitochondrial DNA Genetics 152 1079–1089

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN Version 2.0. Genetics and biometry laboratory, Dept of Anthropology and Ecology, University of Geneva

  • I Seibold AJ Helbig (1996) ArticleTitlePhylogenetic relationships of the sea eagles (genus Haliaeetus): Reconstructions based on morphology, allozymes and mitochondrial DNA sequences J. Zool. Syst. Evol. Res. 34 103–112

    Google Scholar 

  • Shephard JM (2003) A multi-scale approach to defining historical and contemporary factors responsible for the current distribution of the White-bellied Sea-Eagle Haliaeetus leucogaster (Gmelin, 1788) in Australia. PhD thesis, Griffith␣University. <http://www.griffith.edu.au/cgi-bin/frameit? http://www.griffith.edu.au:80/ins/collections/adt/content_thesisto students.html>

  • JM Shephard CP Catterall JM Hughes (2005) ArticleTitleLong-term variation in the distribution of the White-bellied Sea-Eagle (Haliaeetus leucogaster) across Australia Austral Ecol. 30 131–145

    Google Scholar 

  • M Slatkin WP Maddison (1989) ArticleTitleA cladistic measure of gene flow inferred from the phylogenies of alleles Genetics 123 603–613

    Google Scholar 

  • MD Sorenson TW Quinn (1998) ArticleTitleNumts: A challenge for avian systematics and population biology Auk 115 IssueID1 214–221

    Google Scholar 

  • CA Stockwell M Mulvey GL Vinyard (1996) ArticleTitleTranslocations and the preservation of allelic diversity Conserv. Biol. 10 IssueID4 1133–1141

    Google Scholar 

  • K Strimmer A von Haeseler (1996) ArticleTitleQuartet puzzling: A quartet maximum likelihood method for reconstructing tree topologies Mol. Biol. Evol. 13 964–969

    Google Scholar 

  • F Tajima (1989) ArticleTitleStatistical method for testing the neutral mutation hypothesis by DNA polymorphism Genetics 123 585–595

    Google Scholar 

  • K Tamura M Nei (1993) ArticleTitleEstimation of the number of nucleotide substitutions in the control region of the mitochondrial DNA in humans and chimpanzees Mol. Biol. Evol. 10 512–526

    Google Scholar 

  • BL Taylor SJ Chivers S Sexton AE Dizon (2000) ArticleTitleEvaluating dispersal estimates using mtDNA data: Comparing analytical and simulation approaches Conserv. Biol. 14 IssueID5 1287–1297

    Google Scholar 

  • AR Templeton E Routman CA Phillips (1995) ArticleTitleSeparating population structure from population history: A cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum Genetics 140 767–782

    Google Scholar 

  • AR Templeton (1998) ArticleTitleNested clade analyses of phylogeographic data: Testing hypotheses about gene flow and population history Mol. Ecol. 7 381–397

    Google Scholar 

  • AR Templeton (2004) ArticleTitleStatistical phylogeography: Methods of evaluating and minimizing inference errors Mol. Ecol. 13 789–809

    Google Scholar 

  • Thackway R, Cresswell ID (1995) An interim biogeographic regionalisation of Australia: A framework for setting priorities in the national reserves system cooperative program. Version 4.0. Australian Nature Conservation Agency, Reserve Systems Unit, Canberra

  • M Vallianatos SC Lougheed PT Boag (2002) ArticleTitleConservation genetics of the loggerhead shrike (Lanius ludovivianus) in central and eastern North America Conserv. Gene. 3 1–13

    Google Scholar 

  • BS Weir C Cockerham (1984) ArticleTitleEstimating F-Statistics for the analysis of population structure Evolution 38 IssueID6 1358–1370

    Google Scholar 

  • PW Wenink AJ Baker H-U Rosner MG Tilanus (1996) ArticleTitleGlobal mitochondrial DNA phylogeography of holarctic breeding dunlins (Calidris alpina) Evolution 50 IssueID1 318–331

    Google Scholar 

  • JM Wiersma W Nermut JM Shephard (2001) ArticleTitleA variation on the ‘noosed fish’ method and its suitability for trapping the White-Bellied Sea-Eagle Haliaeetus leucogaster Corella 25 IssueID4 97–99

    Google Scholar 

  • S Wright (1951) ArticleTitleThe genetical structure of populations Ann. Eugenics 15 323–354

    Google Scholar 

  • R Zink (1994) ArticleTitleThe geography of mitochondrial DNA variation, population structure, and species limits in the fox sparrow (Passerella iliaca) Evolution 48 96–111

    Google Scholar 

  • RM Zink (1997) Phylogeographic studies of North American Birds DP Mindell (Eds) Avian Molecular Evolution and Systematics Academic Press San Diego 301–324

    Google Scholar 

  • RM Zink GF Barrowclough JL Atwood RRC Blackwell (2000) ArticleTitleGenetics, taxonomy, and conservation of the threatened California Gnatcatcher Conserv. Biol. 14 IssueID5 1394–1405

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Molecular Ecology Laboratory, Australian School of Environmental Studies, Griffith University, Nathan Campus, Kessels Road, 4111, Brisbane, Queensland, Australia

    Jill M. Shephard, Jane M. Hughes & Carla P. Catterall

  2. Department of Zoology, Australian National University, 0200, Canberra, Australia

    Penny D. Olsen

Authors
  1. Jill M. Shephard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jane M. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carla P. Catterall
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Penny D. Olsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jill M. Shephard.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shephard, J.M., Hughes, J.M., Catterall, C.P. et al. Conservation status of the White-Bellied Sea-Eagle Haliaeetus leucogaster in Australia determined using mtDNA control region sequence data. Conserv Genet 6, 413–429 (2005). https://doi.org/10.1007/s10592-005-4987-x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-005-4987-x

Keywords

Search

Navigation