Skip to main content

Advertisement

SpringerLink
Log in

Effects of long-term isolation on genetic variation and within-island population genetic structure in Christmas Island (Indian Ocean) seabirds

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

Abstract

Seabirds endemic to remote oceanic islands face several unique threats to their population viability. Christmas Island is a small oceanic island with remarkable seabird biodiversity, including two endangered endemics: Christmas Island frigatebirds (Fregata andrewsi) and Abbott’s boobies (Papasula abbotti). Christmas Island seabirds are currently threatened by habitat destruction at breeding sites due to phosphate mining and by the adverse effects of the invasive yellow crazy ant (Anoplolepis gracilipes); however, conservation initiatives are limited by a paucity of genetic data on the breeding seabirds. To address this shortcoming, we collected genetic samples from five breeding seabird species, including the two endemics. We surveyed mitochondrial and nuclear genetic diversity, estimated effective population sizes, and tested whether species had undergone recent or long-term effective population size decline. Effective population sizes for Christmas Island frigatebirds and Abbott’s boobies were both low (approximately 5,000 and 2,100 individuals, respectively). Moreover, four out of the five species appeared to have undergone long-term population decline, suggesting that mitigation of the threats to population viability of Christmas Island seabirds is critical. We also detected cryptic population genetic structure within Abbott’s booby, perhaps due to in situ divergence on Christmas Island or due to the influx of individuals from an extirpated colony. Within-island differentiation may be common among endemic seabird species due to high levels of natal philopatry, and we suggest that careful consideration of population genetic structure on small geographic scales is crucial when designing conservation initiatives.

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

Similar content being viewed by others

References

  • Abbott CL, Double MC, Trueman JWH, Robinson A, Cockburn A (2005) An unusual source of mitochondrial heteroplasmy: duplicate mitochondrial control regions in Thalassarche albatrosses. Mol Ecol 14:3605–3613

    Article  PubMed  CAS  Google Scholar 

  • Akst EP, Boersma PD, Fleischer RC (2002) A comparison of genetic diversity between the Galápagos Penguin and the Magellanic Penguin. Cons Gen 3:375–383

    Article  CAS  Google Scholar 

  • Andrews C (1900) A monograph of Christmas Island (Indian Ocean): physical features and geology. British Museum, London

    Google Scholar 

  • Baker AJ, Marshall HD (1997) Mitochondrial control-region sequences as tools for understanding the evolution of avian taxa. In: Mindell DP (ed) Avian molecular systematics and evolution. Academic Press, New York, pp 51–82

    Chapter  Google Scholar 

  • Barlow EJ, Daunt F, Wanless S, Álvarez D, Reid JM, Cavers S (2011) Weak large-scale population genetic structure in a philopatric seabird, the European Shag Phalacrocorax aristotelis. Ibis 153:768–778

    Article  Google Scholar 

  • BirdLife International (2011) Important Bird Areas factsheet: Christmas Island. http://www.birdlife.org. Accessed on 17 November 2011

  • Boessenkool S, Star B, Seddon PJ, Waters JM (2010) Temporal genetic samples indicate small effective population size of the endangered yellow-eyed penguin. Conserv Genet 11:539–546

    Article  Google Scholar 

  • Bourne W (1976) On subfossil bones of Abbott’s booby Sula abbotti from the Mascarene Islands, with a note on the proportions and distribution of the Sulidae. Ibis 118:119–123

    Article  Google Scholar 

  • Brook BW, Tonkyn DW, O’Grady JJ, Frankham R (2002) Contribution of inbreeding to extinction risk in threatened species. Conserv Ecol 6:16

    Google Scholar 

  • Claussen J (2005) Native plants of Christmas Island. Flora Aust Suppl Ser 22:1–146

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) tcs: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Commonwealth of Australia (2001) Background information for the Abbott’s Booby, Papasula abbotti Recovery Plan. Department of the Environment and Heritage, Canberra

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Dearborn DC, Hailer F, Fleischer RC (2008) Microsatellite primers for relatedness and population structure in great frigatebirds (Pelecaniformes: Fregatidae). Mol Ecol Resour 8:1399–1401

    Article  PubMed  CAS  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214–221

    Article  PubMed  Google Scholar 

  • Duffie C, Glenn TC, Vargas FH, Parker PG (2009) Genetic structure within and between island populations of the flightless cormorant (Phalacrocorax harrisi). Mol Ecol 18:2103–2111

    Article  PubMed  Google Scholar 

  • Eda M, Kuro-O M, Higuchi H, Hasegawa H, Koike H (2010) Mosaic gene conversion after a tandem duplication of mtDNA sequence in Diomedeidea (albatrosses). Genes Genet Syst 85:129–139

    Article  PubMed  CAS  Google Scholar 

  • Ellegren H, Moore S, Robinson N, Byrne K, Ward W, Sheldon BC (1997) Microsatellite evolution—a reciprocal study of repeat lengths at homologous loci in cattle and sheep. Mol Biol Evol 14:854–860

    Article  PubMed  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the sortware structure: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Evans SR, Sheldon BC (2008) Interspecific patterns of genetic diversity in birds: correlations with extinction risk. Conserv Biol 22:1016–1025

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Scneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Faircloth BC, Ramos A, Drummond H, Gowaty PA (2009) Isolation and characterization of microsatellite loci from blue-footed boobies (Sula nebouxii). Conserv Genet Resour 1:159–162

    Article  Google Scholar 

  • Fleischer RC, Boarman WI, Gonzalez EG et al (2008) As the raven flies: using genetic data to infer the history of invasive common raven (Corvus corax) populations in the Mojave Desert. Mol Ecol 17:464–474

    Article  PubMed  CAS  Google Scholar 

  • Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Anim Conserv 1:69–73

    Article  Google Scholar 

  • Friesen VL, Birt TP, Piatt JF, Golightly RT, Newman SH, Hébert PN, Congdon BC, Gissing G (2005) Population genetic structure and conservation of marbled murrelets (Brachyramphus marmoratus). Conserv Genet 6:607–614

    Article  Google Scholar 

  • Garnett ST, Szabo JK, Dutson G (2011) The action plan for Australian birds 2010. CSIRO Publishing, Collingwood

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hailer F, Schreiber EA, Miller JM, Levin II, Parker PG, Chesser RT, Fleischer RC (2011) Long-term isolation of a highly mobile seabird on the Galapagos. Proc Roy Soc Lond B Bio 278:817–825

    Article  Google Scholar 

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

  • Hill R, Dunn A (2004) National recovery plan for the Christmas Island frigatebird Fregata andrewsi. Commonwealth of Australia, Canberra

    Google Scholar 

  • Holderegger R, Kamm U, Gugerli F (2006) Adaptive vs. neutral genetic diversity: implications for landscape genetics. Landsc Ecol 21:797–807

    Article  Google Scholar 

  • Huyvaert KP, Anderson DJ (2004) Limited natal dispersal in Nazca boobies Sula granti. J Avian Biol 35:46–53

    Article  Google Scholar 

  • Ibarguchi G, Gaston AJ, Friesen VL (2011) Philopatry, morphological divergence, and kin groups: structuring in thick-billed murres Uria lomvia within a colony in Arctic Canada. J Avian Biol 42:134–150

    Article  Google Scholar 

  • IUCN (2011) IUCN Red List of Threatened Species. Version 2011.2. http://www.iucnredlist.org. Accessed 17 November 2011

  • Kennedy M, Spencer HG (2004) Phylogenies of the frigatebirds (Fregatidae) and tropicbirds (Phaethonidae), two divergent groups of the traditional order Pelecaniformes, inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 31:31–38

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1980) A simple method for measuring evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Kuhner MK (2006) lamarc 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770

    Article  PubMed  CAS  Google Scholar 

  • Lambert DM, Ritchie PA, Millar CD, Holland B, Drummond AJ, Baroni C (2002) Rates of evolution in ancient DNA from Adélie penguins. Science 295:2270–2273

    Article  PubMed  CAS  Google Scholar 

  • Lande R (1995) Mutation and conservation. Conserv Biol 9:782–791

    Article  Google Scholar 

  • Lawrence HA, Scofield RP, Crockett DE, Millar CD, Lambert DM (2008) Ancient genetic variation in one of the world’s rarest seabirds. Heredity 101:543–547

    Article  PubMed  CAS  Google Scholar 

  • Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373

    Article  CAS  Google Scholar 

  • Lumsden L, Schulz M, Ashton R, Middleton D (2007) Investigation of threats to the Christmas Island Pipistrelle. A report to the Department of the Environment and Water Resources. Arthur Rylah Institute for Environmental Research, Department of Sustainability and Environment. Heidelberg, Victoria

  • Milot E, Weimerskirch H, Duchesne P, Bernatchez L (2007) Surviving with low genetic diversity: the case of albatrosses. Proc R Soc Lond B Biol Sci 274:779–787

    Article  CAS  Google Scholar 

  • Milot E, Weimerskirch H, Bernatchez L (2008) The seabird paradox: dispersal, genetic structure and population dynamics in a highly mobile, but philopatric albatross species. Mol Ecol 17:1658–1673

    Article  PubMed  CAS  Google Scholar 

  • Molecular Ecology Resources Primer Development Consortium, An J, Bechet A et al (2010) Permanent genetic resources added to Molecular Ecology Resources Database 1(October), pp. 2009–30, November 2009. Mol Ecol Resour 10:404–408

    Article  PubMed  Google Scholar 

  • Morris-Pocock JA, Steeves TE, Estela FA, Anderson DJ, Friesen VL (2010a) Comparative phylogeography of brown (Sula leucogaster) and red-footed boobies (S. sula): the influence of physical barriers and habitat preference on gene flow in pelagic seabirds. Mol Phylogenet Evol 54:883–896

    Article  PubMed  CAS  Google Scholar 

  • Morris-Pocock JA, Taylor SA, Birt TP, Friesen VL (2010b) Concerted evolution of duplicated mitochondrial control regions in three related seabird species. BMC Evol Biol 10:14

    Article  PubMed  Google Scholar 

  • Morris-Pocock JA, Anderson DJ, Friesen VL (2011) Mechanisms of global diversification in the brown booby (Sula leucogaster) revealed by uniting statistical phylogeographic and multilocus phylogenetic methods. Mol Ecol 20:2835–2850

    Article  PubMed  CAS  Google Scholar 

  • Munilla I, Arcos JM, Oro D, Álvarez D, Leyenda PM, Velando A (2011) Mass mortality of seabirds in the aftermath of the Prestige oil spill. Ecosphere 2:83

    Article  Google Scholar 

  • Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nelson JB (1974) The distribution of Abbott’s booby Sula abbotti. Ibis 116:368–369

    Article  Google Scholar 

  • Nelson JB (1978) The Sulidae: gannets and boobies. Oxford University Press, Oxford

    Google Scholar 

  • Nelson JB (2005) Pelicans, cormorants and their allies. Oxford University Press, Oxford

    Google Scholar 

  • Nims BD, Vargas FH, Merkel J, Parker PG (2008) Low genetic diversity and lack of population structure in the endangered Galápagos penguin (Spheniscus mendiculus). Conserv Genet 9:1413–1420

    Article  Google Scholar 

  • Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genetic Res 22:201–204

    Article  Google Scholar 

  • Patterson SA, Morris-Pocock JA, Friesen VL (2011) A multilocus phylogeny of the Sulidae (Aves: Pelecaniformes). Mol Phylogenet Evol 58:181–191

    Article  PubMed  CAS  Google Scholar 

  • Peery MZ, Hall LA, Sellas A, Beissinger ST, Moritz C, Bérubé M et al (2010) Genetic analyses of historic and modern marbled murrelets suggest decoupling of migration and gene flow after habitat fragmentation. Proc R Soc Lond B Biol Sci 277:697–706

    Article  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Primmer CR, Møller AP, Ellegren H (1996) A wide-range survey of cross-species microsatellite amplification in birds. Mol Ecol 5:365–378

    PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Rains D, Weimerskirch H, Burg TM (2011) Piecing together the global population puzzle of wandering albatrosses: genetic analysis of the Amsterdam albatross Diomedea amsterdamensis. J Avian Biol 42:69–79

    Article  Google Scholar 

  • Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103

    PubMed  CAS  Google Scholar 

  • Reville BJ, Tranter JD, Yorkston HD (1990) Conservation of the endangered Abbott’s booby on Christmas Island 1983–1989. Australian National Parks Wildlife Service, Occasional Paper no. 20, Canberra

  • Ritchie PA, Millar CA, Gibb GC, Baroni C, Lambert DM (2004) Ancient DNA enables timing of the Pleistocene origin and Holocene expansion of two Adélie penguin lineages in Antarctica. Mol Biol Evol 21:240–248

    Article  PubMed  CAS  Google Scholar 

  • Sambrook JD, Russell W (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schreiber EA, Burger J (2002) Biology of marine birds. CRC Press, Boca Raton

    Google Scholar 

  • Spennemann DHR (1998) Excessive exploitation of central Pacific seabird populations at the turn of the 20th century. Mar Ornithol 26:49–57

    Google Scholar 

  • Steadman DW (1989) Extinction of birds in Eastern Polynesia: a review of the record, and comparisons with other Pacific island groups. J Archaeol Sci 16:177–205

    Article  Google Scholar 

  • Steadman DW, Pahlavan DS, Kirch PV (1990) Extinction, biogeography, and human exploitation of birds on Tikopia and Anuta, Polynesian outliers in the Solomon Islands. Bishop Mus Occas Pap 30:118–153

    Google Scholar 

  • Steeves TE, Anderson DJ, Friesen VL (2005) A role for nonphysical barriers to gene flow in the diversification of a highly vagile seabird, the masked booby (Sula dactylatra). Mol Ecol 14:3877–3887

    Article  PubMed  CAS  Google Scholar 

  • Steeves TE, Holdaway RN, Hale ML, McLay E, McAllan IAW, Christian M, Hauber ME, Bunce M (2010) Merging ancient and modern DNA: extinct seabird taxon rediscovered in the North Tasman Sea. Biol Lett 6:94–97

    Article  PubMed  Google Scholar 

  • Stoddart DR (1981) Abbott’s booby on assumption. Atoll Res Bull 255:27–32

    Google Scholar 

  • Stokes T (1988) A review of the birds of Christmas Island, Indian Ocean. Australian National Parks Wildlife Service, Occasional Paper no. 16, Canberra

  • Tajima F (1983) Evolutionary relationships of DNA sequences in finite populations. Genetics 105:437–460

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Taylor SA, Morris-Pocock JA, Sun Z, Friesen VL (2010) Isolation and characterization of ten microsatellite loci in Blue-footed (Sula nebouxii) and Peruvian Boobies (S. variegata). J Ornithol 151:525–528

    Article  Google Scholar 

  • Taylor SA, Maclagen L, Anderson DJ, Friesen VL (2011a) Could specialization to cold-water upwelling systems influence gene flow and population differentiation in marine organisms? A case study using the blue-footed booby, Sula nebouxii. J Biogeogr 38:883–893

    Article  Google Scholar 

  • Taylor SA, Zavalaga CB, Luna-Jorquera G, Simeone A, Anderson DJ, Friesen VL (2011b) Panmixia and high genetic diversity in a Humboldt Current endemic, the Peruvian Booby (Sula variegata). J Ornithol 152:623–630

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Traill LW, Brook BW, Frankham RR, Bradshaw CJA (2010) Pragmatic population viability targets in a rapidly changing world. Biol Conserv 143:28–34

    Article  Google Scholar 

  • Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167

    Article  Google Scholar 

  • Wanless RM, Angel A, Cuthbert RJ, Hilton GM, Ryan PG (2007) Can predation by invasive mice drive seabird extinctions? Biol Lett 3:241–244

    Article  PubMed  Google Scholar 

  • Weimerskirch H, Brothers N, Jouventin P (1997) Population dynamics of wandering albatross Diomedea exulans and Amsterdam albatross D. amsterdamensis in the Indian Ocean and their relationships with long-line fisheries: conservation implications. Biol Conserv 79:257–270

    Article  Google Scholar 

  • Yorkston HD, Green PT (1997) The breeding distribution and status of Abbott’s booby (Sulidae: Papasula abbotti) on Christmas Island, Indian Ocean. Biol Conserv 79:293–301

    Article  Google Scholar 

Download references

Acknowledgments

Fieldwork was conducted within the framework of the Christmas Island Seabird Project (www.seabirdproject.cx) which was supported by grants from the Universität Hamburg, MiniWunderland Hamburg, Christmas Island Trust, Christmas Island Territory Week Committee, Christmas Island Tourist Association, and several private sponsors. We thank L. Braun, N. Denhard, K. Flachsbarth, K. Grenz, K. Kleiss, S. Luecht, J. Navarro, L. Pein, M. Schiffler, F. Schuster, and M. Van der Stap for assistance with sample collection. Funding was supplied by a National Science and Engineering Research Council of Canada (NSERC) Discovery Grant (V.F.L.) and a NSERC Alexander Graham Bell Canada Graduate Scholarship (J.A.M.P.). Grube KG Hützel, Germany, Rische & Herfurth Hamburg, Germany, and The North Face Inc., USA, provided in-kind support. Christmas Island National Park kindly provided logistical support and accommodation. We would like to thank, in particular, L. Ott and Z. Sun for lab support. T. Birt, P. Deane, G. Ibarguchi, S. Taylor, and S. Wallace also provided lab support and/or helpful discussion. Technical assistance was provided by Corine Zotti of the sequencing platform at the McGill University and Genome Quebec Innovation Centre. All experiments were carried out with permits from Parks Australia North, Christmas Island National Park, the Department of Environment of Australia, Bundesamt für Naturschutz, Germany, and Amt für Gesundheit und Verbraucherschutz der Hansestadt Hamburg, Germany, and in accordance with the principles and guidelines of the German and Australian laws on animal welfare. Christmas Island frigatebird and Abbott’s booby samples were transferred to Queen’s University in Canada under the Convention of International Trade in Endangered Species of Wild Fauna and Flora (CITES) permit 09CA00253/CWHQ.

Author information

Authors and Affiliations

  1. Department of Biology, Queen’s University, Kingston, ON, K7L 3N6, Canada

    James A. Morris-Pocock & Vicki L. Friesen

  2. Department of Animal Ecology and Conservation, Biozentrum Grindel, Universität Hamburg, Martin-Luther-King Platz 3, 20146, Hamburg, Germany

    Janos C. Hennicke

  3. Centre d’Etudes Biologiques de Chizé, CNRS UPR 1934, 79360, Villiers-en-Bois, France

    Janos C. Hennicke

Authors
  1. James A. Morris-Pocock
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Janos C. Hennicke
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vicki L. Friesen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to James A. Morris-Pocock.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morris-Pocock, J.A., Hennicke, J.C. & Friesen, V.L. Effects of long-term isolation on genetic variation and within-island population genetic structure in Christmas Island (Indian Ocean) seabirds. Conserv Genet 13, 1469–1481 (2012). https://doi.org/10.1007/s10592-012-0390-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-012-0390-6

Keywords

Search

Navigation