Skip to main content

Advertisement

Log in

Population genetic and behavioural variation of the two remaining colonies of Providence petrel (Pterodroma solandri)

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

Abstract

Knowledge of the dispersal capacity of species is crucial to assess their extinction risk, and to establish appropriate monitoring and management strategies. The Providence petrel (Pterodroma solandri) presently breeds only at Lord Howe Island (~32,000 breeding pairs) and Phillip Island-7 km south of Norfolk Island (~20 breeding pairs). A much larger colony previously existed on Norfolk Island (~1,000,000 breeding pairs) but was hunted to extinction in the 18th Century. Differences in time of return to nesting sites are presently observed between the two extant colonies. Information on whether the Phillip Island colony is a relict population from Norfolk Island, or a recent colonization from Lord Howe Island, is essential to assess long-term sustainability and conservation significance of this small colony. Here, we sequenced the mitochondrial cytochrome b gene and 14 nuclear introns, in addition to genotyping 10 microsatellite loci, to investigate connectivity of the two extant P. solandri populations. High gene flow between populations and recent colonization of Phillip Island (95 % HPD 56–200 ya) are inferred, which may delay or prevent the genetic differentiation of these insular populations. These results suggest high plasticity in behaviour in this species and imply limited genetic risks surrounding both the sustainability of the small Phillip Island colony, and a proposal for translocation of Lord Howe Island individuals to re-establish a colony on Norfolk Island.

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

Access this article

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
Fig. 5

Similar content being viewed by others

References

  • Anderson A (2003) Investigating early settlement on Lord Howe Island. Aust Archaeol 57:98–102

    Article  Google Scholar 

  • Anderson A, White JP (2001) The Prehistoric Archaeology of Norfolk Island. Southwest Pacific, Australian Museum, Sydney

    Google Scholar 

  • Avise JC (1996) Introduction: the scope of conservation genetics. conservation genetics. Springer, US, pp 1–9

    Chapter  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Axelsson E, Smith NG, Sundström H, Berlin S, Ellegren H (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 

  • Backström N, Fagerberg S, Ellegren H (2008) Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Mol Ecol 17:964–980

    Article  PubMed  CAS  Google Scholar 

  • Baduini CL (2002) Parental provisioning patterns of wedge-tailed shearwaters and their relation to chick body condition. Condor 104:823–831

    Article  Google Scholar 

  • Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bester AJ (2003) The Breeding, Foraging Ecology and Conservation of the Providence Petrel, Pterodroma solandri, on Lord Howe Island, Australia. Ph.D. Thesis, Charles Sturt University, Albury, NSW

  • Bester A, Klomp NI, Priddel D, Carlile N (2002) Chick-provisioning behaviour of the Providence Petrel, Pterodroma solandri. Emu 102:297–304

    Article  Google Scholar 

  • Boessenkool S, Austin JJ, Worthy TH, Scofield P, Cooper A, Seddon PJ, Waters JM (2009) Relict or colonizer? Extinction and range expansion of penguins in southern New Zealand. P Roy Soc Lond B Bio 276:815–821

    Article  CAS  Google Scholar 

  • Bonadonna F, Bretagnolle V (2002) Smelling home: a good solution for burrow-finding in nocturnal petrels? J Exp Biol 205:2519–2523

    PubMed  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Brooke M (2004) Albatrosses and petrels across the world. Oxford University Press, Oxford

    Google Scholar 

  • Brown RM et al (2010) Range expansion and hybridization in Round Island petrels (Pterodroma spp.): evidence from microsatellite genotypes. Mol Ecol 19:3157–3170

    Article  PubMed  Google Scholar 

  • Burg T, Croxall J (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 

  • Caliński T, Harabasz J (1974) A dendrite method for cluster analysis. Commun Stat A-Theor 3:1–27

    Article  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • Clarke K, Warwick R (2005) Primer-6 computer program. Natural Environment Research Council, Plymouth

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Dell’Ariccia G, Bonadonna F (2013) Back home at night or out until morning? Nycthemeral variations in homing of anosmic Cory’s shearwaters in a diurnal colony. J Exp Biol 216:1430–1433

    Article  PubMed  Google Scholar 

  • Dellicour S, Mardulyn P (2014) SPADS 1.0: a toolbox to perform spatial analyses on DNA sequence data sets. Mol Ecol Res 14:647–651

    Article  Google Scholar 

  • Dias MP, Granadeiro JP, Catry P (2012) Working the day or the night shift? Foraging schedules of Cory’s shearwaters vary according to marine habitat. Mar Ecol-Prog Ser 467:245

    Article  Google Scholar 

  • Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards SV, Arctander P, Wilson AC (1991) Mitochondrial resolution of a deep branch in the genealogical tree for perching birds. P Roy Soc Lond B Bio 243:99–107

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  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 

  • Falk K, Benvenuti S, Dall’Antonia L, Gilchrist G, Kampp K (2002) Foraging behaviour of thick-billed murres breeding in different sectors of the North Water polynya: an inter-colony comparison. Mar Ecol-Prog Ser 231:293–302

    Article  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Friesen VL (2015) Speciation in seabirds: why are there so many species… and why aren’t there more? J Ornithol 156:27–39

    Article  Google Scholar 

  • Friesen V, Smith A, Gomez-Diaz E, Bolton M, Furness R, González-Solís J, Monteiro L (2007) Sympatric speciation by allochrony in a seabird. P Natl Acad Sci USA 104:18589–18594

    Article  CAS  Google Scholar 

  • Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci. 7:457–472

    Article  Google Scholar 

  • Girod C, Vitalis R, Leblois R, Fréville H (2011) Inferring population decline and expansion from microsatellite data: a simulation-based evaluation of the Msvar method. Genetics 188:165–179

    Article  PubMed  PubMed Central  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Goudet J, Raymond M, de Meeüs T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hasegawa M, Kishino H, T-a Yano (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 

  • Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162

    Article  Google Scholar 

  • Hermes N, Evans O, Evans B (1986) Norfolk Island birds: a review 1985. Notornis 33:141–149

    Google Scholar 

  • 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 

  • Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. P Natl Acad Sci USA 104:2785–2790

    Article  CAS  Google Scholar 

  • Hindwood KA (1940) The birds of Lord Howe Island. Emu 40:1–86

    Article  Google Scholar 

  • Holdaway RN (1999) Introduced predators and avifaunal extinction in New Zealand. Extinctions in near time. Springer, US, pp 189–238

    Chapter  Google Scholar 

  • Holdaway R, Christian M (2010) Stopping the fourth wave: conservation and restoration of the Norfolk Island ecosystem. Wingspan 20:30–35

    Google Scholar 

  • Holdaway RN, Jacomb C (2000) Rapid extinction of the moas (Aves: Dinornithiformes): model, test, and implications. Science 287:2250–2254

    Article  CAS  PubMed  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  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 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST (2005) hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Keitt BS, Tershy BR, Croll DA (2004) Nocturnal behavior reduces predation pressure on black-vented shearwaters Puffinus opisthomelas. Mar Ornithol 32:173–178

    Google Scholar 

  • Kimura M (1969) The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics 61:893

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. P Natl Acad Sci USA 75:2868–2872

    Article  CAS  Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. P Natl Acad Sci USA 86:6196–6200

    Article  CAS  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 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Lombal AJ, Wenner TJ, Burridge CP (2015) Assessment of high-resolution melting (HRM) profiles as predictors of microsatellite variation: an example in Providence Petrel (Pterodroma solandri). Genes Genomics 37:977–983

    Article  CAS  Google Scholar 

  • Mardulyn P, Mikhailov YE, Pasteels JM (2009) Testing phylogeographic hypotheses in a Euro-Siberian cold-adapted leaf beetle with coalescent simulations. Evolution 63:2717–2729

    Article  CAS  PubMed  Google Scholar 

  • Matisoo-Smith E, Horsburgh K, Robins JH, Anderson A (2001) Genetic variation in archaeological Rattus exulans remains from the Emily Bay settlement site, Norfolk Island. Rec Aust Mus 53:81–84

    Article  Google Scholar 

  • McCarthy FD (1934) Norfolk Island: additional evidence of a former native occupation. J Polyn Soc 43:267–270

    Google Scholar 

  • McNeil R, Drapeau P, Pierotti R (1993) Nocturnality in colonial waterbirds: occurrence, special adaptations, and suspected benefits. Current ornithology. Springer, US, pp 187–246

    Chapter  Google Scholar 

  • Medway DG (2002a) History and causes of the extirpation of the Providence petrel (Pterodroma solandri) on Norfolk Island. Notornis 49:246–258

    Google Scholar 

  • Medway DG (2002b) Why were Providence petrels (Pterodroma solandri) nocturnal at Norfolk Island? Notornis 39:263–289

    Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

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

    Google Scholar 

  • Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oro D (2003) Managing seabird metapopulations in the Mediterranean: constraints and challenges. Sci Mar 67:13–22

    Article  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  PubMed  Google Scholar 

  • Paiva VH, Geraldes P, Ramírez I, Meirinho A, Garthe S, Ramos JA (2009) Foraging plasticity in a pelagic seabird species along a marine productivity gradient. Mar Ecol-Prog Ser 398:259–274

    Article  CAS  Google Scholar 

  • Palsboll PJ, Zachariah Peery M, Berube M (2010) Detecting populations in the ambiguous zone: kinship-based estimation of population structure at low genetic divergence. Mol Ecol Res 10:797–805

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Plummer M, Best N, Cowles K, Vines K (2006) CODA: convergence diagnosis and output analysis for MCMC. R News 6:7–11

    Google Scholar 

  • Priddel D, Carlile N, Evans O, Evans B, McCoy H (2010) A review of the seabirds of Phillip Island in the Norfolk Island Group. Notornis 57:113–127

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. P Natl Acad Sci USA 94:9197–9201

    Article  CAS  Google Scholar 

  • Rayner MJ, Hauber ME, Imber MJ, Stamp RK, Clout MN (2007) Spatial heterogeneity of mesopredator release within an oceanic island system. P Natl Acad Sci USA 104:20862–20865

    Article  CAS  Google Scholar 

  • Reed TE, Warzybok P, Wilson AJ, Bradley RW, Wanless S, Sydeman WJ (2009) Timing is everything: flexible phenology and shifting selection in a colonial seabird. J Anim Ecol 78:376–387

    Article  PubMed  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Sæther BE et al (2004) Life-history variation predicts the effects of demographic stochasticity on avian population dynamics. Am Nat 164:793–802

    Google Scholar 

  • Serrano D, Forero MG, Donázar JA, Tella JL (2004) Dispersal and social attraction affect colony selection and dynamics of lesser kestrels. Ecology 85:3438–3447

    Article  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 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith BJ (2007) boa: an R package for MCMC output convergence assessment and posterior inference. J Stat Softw 21:1–37

    Article  Google Scholar 

  • Smith A, Friesen V (2007) Differentiation of sympatric populations of the band-rumped storm-petrel in the Galapagos Islands: an examination of genetics, morphology, and vocalizations. Mol Ecol 16:1593–1603

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56:154–166

    Article  CAS  PubMed  Google Scholar 

  • Storz JF, Beaumont MA, Alberts SC (2002) Genetic evidence for long-term population decline in a savannah-dwelling primate: inferences from a hierarchical Bayesian model. Mol Biol Evol 19:1981–1990

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tennyson AJD, Martinson P (2006) Extinct birds of New Zealand. Te Papa Press, Wellington

    Google Scholar 

  • Towns DR (2009) Eradications as reverse invasions: lessons from Pacific rat (Rattus exulans) removals on New Zealand islands. Biol Invasions 11:1719–1733

    Article  Google Scholar 

  • Venables WN, Smith DM (2001) An Introduction to R. Notes on R: a programming environment for data analysis and graphics. J Environ Qual

  • Warham J (1990) The petrels: their ecology and breeding systems. A&C Black

  • Watanuki Y (1986) Moonlight avoidance behavior in Leach’s storm-petrels as a defense against slaty-backed gulls. Auk 103:14–22

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Welch A et al (2012) Population divergence and gene flow in an endangered and highly mobile seabird. Heredity 109:19–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitlock MC (2011) GST and D do not replace FST. Mol Ecol 20:1083–1091

    Article  PubMed  Google Scholar 

  • Wiley AE et al (2012) Foraging segregation and genetic divergence between geographically proximate colonies of a highly mobile seabird. Oecologia 168:119–130

    Article  PubMed  Google Scholar 

  • Wilmshurst JM, Higham TF (2004) Using rat-gnawed seeds to independently date the arrival of Pacific rats and humans in New Zealand. Holocene 14:801–806

    Article  Google Scholar 

  • Worthy TH (1999) What was on the menu? Avian extinction in New Zealand. New Zeal J Archaeol 19:125–160

    Google Scholar 

Download references

Acknowledgments

We are grateful to David Binns, Norfolk Island Parks and Wildlife for providing logistics, transportation and accommodation during field-work on Norfolk Island. We thank Honey McCoy for sharing his data on Phillip Island seabirds. The Sea world Research and Rescue Foundation Inc (Grant SWR/4/2011) supported this work. Field sample collection of Providence petrel blood samples was conducted with Animal Ethics permission from University of Tasmania Ethics Committee (Permit# A00011680). We thank the anonymous reviewers for their careful reading of our paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anicee J. Lombal.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 406 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lombal, A.J., Wenner, T.J., Carlile, N. et al. Population genetic and behavioural variation of the two remaining colonies of Providence petrel (Pterodroma solandri). Conserv Genet 18, 117–129 (2017). https://doi.org/10.1007/s10592-016-0887-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-016-0887-5

Keywords

Navigation