Skip to main content

Advertisement

Log in

Population expansion, current and past gene flow in Gould’s petrel: implications for conservation

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

Abstract

Seabird life-history traits such as long generation time, low annual fecundity and delayed sexual maturation make them more prone to population loss and consequently to extinction; petrels are indeed amongst the most threatened birds. Based on coalescence and multiloci inference this study examines the extent of genetic differentiation of a vulnerable New Caledonia (caledonica) and Australia (leucoptera) subspecies of Pterodroma leucoptera (Gould’s Petrel), and whether the genetic relationship between them results from the influence of past events like variation in sea level, or is dominated by contemporary gene flow. Sequences of two mitochondrial genes and five nuclear introns were obtained from 86 individuals from both populations. Haplotype networks were used to infer relationships between the haplotypes of both populations. The demographic history of the P. leucoptera complex was studied using neutrality tests and Extended Bayesian Skyline Plots. A weak population differentiation was revealed. The Extended Bayesian Skyline plot suggested a population expansion approximately 80,000 years before present (bp) for caledonica and 30,000 years bp for leucoptera. The split was dated to 30,000 years bp by means of multilocus inference through *BEAST. Despite genetic similarity of the two taxa, we advocate to consider them as independent units for conservation management, given their strong ecological distinctiveness (foraging distribution, winter distribution, breeding phenology and breeding distribution).

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Allendorf FW, Luikart G (2009) Conservation and the genetics of populations. Wiley

  • Armstrong PH (1992) Human impacts on Australia’s Indian ocean tropical island ecosystems: a review. Environmentalist 12:191–206

    Article  Google Scholar 

  • Axelsson E, Smith NGC, Sundström H et al (2004) Male-biased mutation rate and divergence in autosomal, z-linked and w-linked introns of chicken and Turkey. Mol Biol Evol 21:1538–1547

    Article  CAS  PubMed  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Barrows TT, Juggins S, De Deckker P et al (2007) Long-term sea surface temperature and climate change in the Australian-New Zealand region. Paleoceanography 22:1–17

    Article  Google Scholar 

  • Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773

    CAS  PubMed  PubMed Central  Google Scholar 

  • Birdlife International (2015) Species fact sheet: Pterodroma leucoptera. http://www.birdlife.org/datazone/speciesfactsheet.php?id=3887

  • Bisconti R, Canestrelli D, Colangelo P, Nascetti G (2011) Multiple lines of evidence for demographic and range expansion of a temperate species (Hyla sarda) during the last glaciation. Mol Ecol 20:5313–5327

    Article  PubMed  Google Scholar 

  • Bretagnolle V, Shirihai H (2010) A new taxon of collared petrel pterodroma brevipes from the Banks Islands. Vanuatu 130:286–301

    Google Scholar 

  • Brown RP, Tejangkura T, El Mouden EH et al (2012) Species delimitation and digit number in a North African skink. Ecol Evol 2:2962–2973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burg TM, Croxall JP (2001) Global relationships amongst black-browed and grey-headed albatrosses: analysis of population structure using mitochondrial DNA and microsatellites. Mol Ecol 10:2647–2660

    Article  CAS  PubMed  Google Scholar 

  • Carlile N, Priddel D, Zino F et al (2003) A review of four successful recovery programmes for threatened sub-tropical petrels. Mar Ornithol 31:185–192

    Google Scholar 

  • Caughley G (1994) Directions in conservation biology. J Anim Ecol 63:215–244

    Article  Google Scholar 

  • Cheang CC, Tsang LM, Ng WC et al (2012) Phylogeography of the cold-water barnacle chthamalus challengeri in the north-western pacific: effect of past population expansion and contemporary gene flow. J Biogeogr 39:1819–1835

    Article  Google Scholar 

  • Chiucchi JE, Gibbs HL (2010) Similarity of contemporary and historical gene flow among highly fragmented populations of an endangered rattlesnake. Mol Ecol 19:5345–5358

    Article  PubMed  Google Scholar 

  • Dearborn DC, Anders AD, Schreiber EA et al (2003) Inter-island movements and population differentiation in a pelagic seabird. Mol Ecol 12:2835–2843

    Article  CAS  PubMed  Google Scholar 

  • Degnan JH, Rosenberg NA (2006) Discordance of species trees with their most likely gene trees. PLoS Genet 2:e68

    Article  PubMed  PubMed Central  Google Scholar 

  • Dobson FS, Jouventin P (2007) How slow breeding can be selected in seabirds: testing lack’s hypothesis. Proc R Soc B 274:275–279

    Article  PubMed  Google Scholar 

  • Drummond A, Bouckaert R (2015) Bayesian evolutionary analysis with BEAST. Cambridge University press, Cambridge

    Book  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under linux and windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press

  • Friesen VL, González JA, Cruz-Delgado F (2006) Population genetic structure and conservation of the Galápagos petrel (Pterodroma phaeopygia). Conserv Genet 7:105–115

    Article  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 14:915–925

    Google Scholar 

  • Gangloff B, Shirihai H, Watling D et al (2012) The complete phylogeny of Pseudobulweria, the most endangered seabird genus: systematics, species status and conservation implications. Conserv Genet 13:39–52

    Article  Google Scholar 

  • Gangloff B, Zino F, Shirihai H et al (2013) The evolution of north-east Atlantic gadfly petrels using statistical phylogeography. Mol Ecol 22:495–507

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Moreno J (2004) Is there a universal molecular clock for birds? J Avian Biol 35:465–468

    Article  Google Scholar 

  • Gómez-Díaz E, González-Solís J, Peinado MA, Page RDM (2006) Phylogeography of the Calonectris shearwaters using molecular and morphometric data. Mol Phylogenet Evol 41:322–332

    Article  PubMed  Google Scholar 

  • Gould J (1865) Handbook to the birds of Australia, vol Vol 1. Cambridge University, London

    Book  Google Scholar 

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

    CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano TA (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Heled J, Drummond AJ (2008) Bayesian inference of population size history from multiple loci. BMC Evol Biol 15:1–15

    Google Scholar 

  • Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580

    Article  CAS  PubMed  Google Scholar 

  • Henriques R, Potts WM, Santos CV et al (2014) Population connectivity and phylogeography of a coastal fish, Atractoscion aequidens (Sciaenidae), across the Benguela current region: evidence of an ancient vicariant event. PLoS One 9:e87907

    Article  PubMed  PubMed Central  Google Scholar 

  • Hey J (2005) On the number of new world founders: a population genetic portrait of the peopling of the Americas. PLoS Biol 3:0965–0975

    Article  CAS  Google Scholar 

  • Hey J. (2007). Introduction to the IM and IMa computer programs. http://lifesci.rutgers.edu/~heylab/Programsand-Data/Programs/IM

  • Hey J (2009) Using IM documentation. https://bio.cst.temple.edu/~hey/software/software.htm

  • Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568

    Article  CAS  PubMed  Google Scholar 

  • Ho SYW, Heupink TH, Rambaut A, Shapiro B (2007) Bayesian estimation of sequence damage in ancient DNA. Mol Biol Evol 24:1416–1422

    Article  CAS  PubMed  Google Scholar 

  • Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huyvaert K, Anderson D (2004) Limited dispersal by Nazca boobies Sula granti. J Avian Biol 35:46–53

    Article  Google Scholar 

  • Ibarguchi G, Friesen VL, Lougheed SC (2006) Defeating numts: Semi-pure mitochondrial DNA from eggs and simple purification methods for field-collected wildlife tissues. Genome 49(11):1438–1450

    Article  CAS  PubMed  Google Scholar 

  • Illera JC, Rando JC, Richardson DS, Emerson BC (2012) Age, origins and extinctions of the avifauna of Macaronesia: a synthesis of phylogenetic and fossil information. Quat Sci Rev 50:14–22

    Article  Google Scholar 

  • Imber MJ, Jenkins JAF (1981) The New Caledonian Petrel. Department of Internal Affaires

  • IUCN (2015) The IUCN Red List of Threatened Species. Version 2015.1. http://www.iucnredlist.org. Downloaded on 1 Feb 2015

  • Jacobsen F, Omland KE (2012) Extensive introgressive hybridization within the northern oriole group (genus icterus) revealed by three-species isolation with migration analysis. Ecol Evol 2:2413–2429

    Article  PubMed  PubMed Central  Google Scholar 

  • Jesus J, Menezes D, Gomes S et al (2009) Phylogenetic relationships of gadfly petrels Pterodroma spp. from the Northeastern Atlantic Ocean: molecular evidence for specific status of Bugio and Cape Verde petrels and implications for conservation. Bird Conserv Int 19(3):199–214

    Article  Google Scholar 

  • Kimball RT, Braun EL, Barker FK et al (2009) A well-tested set of primers to amplify regions spread across the avian genome. Mol Phylogenet Evol 50:654–660

    Article  CAS  PubMed  Google Scholar 

  • Kingman JFC (1982) The coalescent. Stoch Process Appl 13:235–248

    Article  Google Scholar 

  • Kubatko LS, Degnan JH (2007) Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst Biol 56:17–24

    Article  CAS  PubMed  Google Scholar 

  • Kulikova IV, Drovetski SV, Gibson DD et al (2005) Phylogeography of the Mallard (Anas Platyrhynchos): hybridization, dispersal, and lineage sorting contribute to complex geographic structure. Auk 122:949–965

    Article  Google Scholar 

  • Lambeck K, Esat TM, Potter E-K (2002) Links between climate and sea levels for the past three million years. Nature 419:199–206

    Article  CAS  PubMed  Google Scholar 

  • Lande R (1998) Anthropogenic, ecological and genetic factors in extinction and conservation. Res. Popul. Ecol. (Kyoto) 40:259–269

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lovette I (2004) Mitochondrial dating and mixed support for the “2% rule” in birds. Auk 121:1–6

    Google Scholar 

  • Maddison WP, Knowles LL (2006) Inferring phylogeny despite incomplete lineage sorting. Syst Biol 55:21–30

    Article  PubMed  Google Scholar 

  • Mareile Techow N, Ryan P, O’Ryan C (2009) Phylogeography and taxonomy of white-chinned and spectacled petrels. Mol Phylogenet Evol 52:25–33

    Article  CAS  PubMed  Google Scholar 

  • Meyer BS, Matschiner M, Salzburger W (2016) Disentangling incomplete lineage sorting and introgression to refine species-tree estimates for Lake Tanganyika cichlid fishes. BioRxiv. doi:10.1093/sysbio/syw069

    Google Scholar 

  • Miller B, Mullette KJ (1985) Rehabilitation of an endangered Australian bird: the Lord Howe Island woodhen Tricholimnas sylvestris (Sclater). Biol Conserv 34:55–95

    Article  Google Scholar 

  • Moritz C (2002) Strategies to protect biological diversity and the evolutionary. Syst Biol 51:238–254

    Article  PubMed  Google Scholar 

  • Naurois R, Rancurel P (1978) Observations nouvelles sur les Laridae reproducteurs en Nouvelle-Caledonie. Sci Nat 287:495–498

    Google Scholar 

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

    Google Scholar 

  • Nei M, Tajima F (1983) Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105:207–217

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nunn G, Stanley S (1998) Corrigendum for: body size effects and rates of cytochrome-b evolution in tube-nosed seabirds. Mol Biol Evol 17:1774

    Article  Google Scholar 

  • Onley D, Scofield P (2007) Field Guide to the albatrosses. petrels and shearwaters of the World Christopher Helm Publishers Ltd

  • Ovenden J, Wust-Saucy A, Bywater R et al (1991) Genetic evidence for philopatry in a colonially nesting seabird, the Fairy Prion (Pachyptila turtur). Auk 108:688–694

    Article  Google Scholar 

  • Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16

    Article  PubMed  Google Scholar 

  • Peterson AT (2006) Application of molecular clocks in ornithology revisited. J Avian Biol 37:541–544

    Article  Google Scholar 

  • Pielou E (2008) After the ice age: the return of life to glaciated North America. University of Chicago Press, Chicago

    Google Scholar 

  • Priddel D, Carlile N (1995) Mortality of adult Gould’s petrels Pterodroma leucoptera leucoptera at the nesting site on Cabbage Tree Island, New South Wales. Emu 95:259–264

    Article  Google Scholar 

  • Priddel D, Carlile N (2009) Key elements in achieving a successful recovery programme: a discussion illustrated by the Gould’s Petrel case study. Ecol Manag Restor 10:97–102

    Article  Google Scholar 

  • Priddel D, Carlile N, Portelli D et al (2014) Pelagic distribution of Gould’s petrel (Pterodroma leucoptera): linking shipboard and onshore observations with remote-tracking data. Emu 114(4):360–370

    Article  Google Scholar 

  • Primmer CR, Borge T, Lindell J, Sætre GP (2002) Single-nucleotide polymorphism characterization in species with limited available sequence information: high nucleotide diversity revealed in the avian genome. Mol Ecol 11:603–612

    Article  CAS  PubMed  Google Scholar 

  • Rabouam C, Thibault J, Bretagnolle V (1998) Natal philopatry and close inbreeding in Cory’s shearwater (Calonectris diomedea). Auk 115:483–486

    Article  Google Scholar 

  • Rambaut A, Suchard M, Xie D, Drummond A (2014) Tracer v1.6. Available from http://beast.bio.ed.ac.uk/Tracer

  • Rocha S, Harris DJ, Posada D (2011) Cryptic diversity within the endemic prehensile-tailed gecko Urocotyledon inexpectata across the Seychelles Islands: patterns of phylogeographical structure and isolation at the multilocus level. Biol J Linn Soc 104:177–191

    Article  Google Scholar 

  • Rohling EJ, Fenton M, Jorinsen FJ et al (1998) Magnitudes of sea-level lowstands of the past 500,000 years. Nature 394(6689):162–165

    Article  CAS  Google Scholar 

  • Shaffer SA, Tremblay Y, Weimerskirch H et al (2006) Migratory shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer. Proc Natl Acad Sci USA 103:12799–12802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shapiro B, Ho S (2011) Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol Ecol Resour 11(3):423–434

    Article  PubMed  Google Scholar 

  • Silva MC, Duarte MA, Coelho MM (2011) Anonymous nuclear loci in the white-faced storm-petrel Pelagodroma marina and their applicability to other Procellariiform seabirds. J Hered 102:362–365

    Article  PubMed  Google Scholar 

  • Silva MC, Matias R, Wanless RM et al (2015) Understanding the mechanisms of anti-tropical divergence in the seabird white-faced Storm-petrel (Procellariiformes: pelagodroma marina) using a multi-locus approach. Mol Ecol 24:3122–3137

    Article  PubMed  Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sorenson MD, Quinn TW (1998) Numts: a challenge for avian systematics and population biology. Auk 115:214–221

    Article  Google Scholar 

  • Steadman DW (2006) Extinction and biogeography of tropical Pacific birds. University of Chicago Press

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601

    CAS  PubMed  PubMed Central  Google Scholar 

  • Techow NM, Ryan PG, O’Ryan C (2009) Phylogeography and taxonomy of white-chinned and Spectacled Petrels. Mol Phylogenet Evol 52:25–33

    Article  Google Scholar 

  • Techow NMSM, O’Ryan C, Phillips RA et al (2010) Speciation and phylogeography of giant petrels Macronectes. Mol Phylogenet Evol 54:472–487

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F et al (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tobias JA, Seddon N, Spottiswoode CN et al (2010) Quantitative criteria for species delimitation. Ibis 152(4):724–746

    Article  Google Scholar 

  • van Bekkum M, Sagar PM, Stahl J-C, Chambers GK (2006) Natal philopatry does not lead to population genetic differentiation in Buller’s albatross (Thalassarche bulleri bulleri). Mol Ecol 15:73–79

    Article  PubMed  Google Scholar 

  • Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17:2321–2328

    Article  CAS  PubMed  Google Scholar 

  • Welch AJ, Yoshida AA, Fleischer RC (2011) Mitochondrial and nuclear DNA sequences reveal recent divergence in morphologically indistinguishable petrels. Mol Ecol 20:1364–1377

    Article  PubMed  Google Scholar 

  • Zieliński P, Nadachowska-Brzyska K, Wielstra B et al (2013) No evidence for nuclear introgression despite complete mtDNA replacement in the Carpathian newt (Lissotriton montandoni). Mol Ecol 22:1884–1903

    Article  PubMed  Google Scholar 

  • Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank T.P. Birt for alignment advice and primer dessign. We also thank to the Genome Québec Innovation Centre (McGill University Montreal, QC, Canada) for facilitating part of the sequencing of this work. We are also grateful to A. Gotscho and S.P. Tseng for discussions that improved the IM and EBSP analyses. For field work in New Caledonia, VB thanks I. Brun, M. Pandolfi and especially L. Renaudet and P. Villard. We thank A. Welch who helped to improve the manuscript, and P. Duncan for English corrections on a first draft. Thanks also go to the editors and referees for commenting on and correcting the manuscript. We also thank M. Guichard and E. Pante who provided critical assistance with the SuperMachine YMIR- Université de la Rochelle. Finally this work was supported by the Région Poitou–Charentes and Deux-Sèvres department, who funded AI-V PHD grant.

Authors contributions

VB, DP and NC collected the samples. VB, BG and AI-V conceived the research. SR, CR, BG and AI-V performed the laboratory work. AI-V analyzed the data, with the help of AC and BG. AI-V and VB wrote the manuscript. All the authors read and approved the final manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Iglesias-Vasquez.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 273 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iglesias-Vasquez, A., Gangloff, B., Ruault, S. et al. Population expansion, current and past gene flow in Gould’s petrel: implications for conservation. Conserv Genet 18, 105–115 (2017). https://doi.org/10.1007/s10592-016-0886-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-016-0886-6

Keywords