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Comprehensive evidence for subspecies designations in Cook’s Petrel Pterodroma cookii with implications for conservation management

Published online by Cambridge University Press:  05 October 2020

MATT J. RAYNER Open the ORCID record for MATT J. RAYNER [Opens in a new window] ,
AYLA L. VAN LOENEN Open the ORCID record for AYLA L. VAN LOENEN [Opens in a new window] ,
LARA D. SHEPHERD Open the ORCID record for LARA D. SHEPHERD [Opens in a new window] ,
ILINA CUBRINOVSKA ,
R. PAUL SCOFIELD Open the ORCID record for R. PAUL SCOFIELD [Opens in a new window] ,
ALAN J. D. TENNYSON Open the ORCID record for ALAN J. D. TENNYSON [Opens in a new window] ,
MICHAEL BUNCE Open the ORCID record for MICHAEL BUNCE [Opens in a new window]  and
TAMMY E. STEEVES Open the ORCID record for TAMMY E. STEEVES [Opens in a new window]
MATT J. RAYNER*
Affiliation:
Auckland Museum, Private Bag 92018, Auckland, 1141, New Zealand.
AYLA L. VAN LOENEN*
Affiliation:
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand.
LARA D. SHEPHERD
Affiliation:
Museum of New Zealand Te Papa Tongarewa, PO Box 467, Wellington, New Zealand.
ILINA CUBRINOVSKA
Affiliation:
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand.
R. PAUL SCOFIELD
Affiliation:
Canterbury Museum, Christchurch, New Zealand.
ALAN J. D. TENNYSON
Affiliation:
Museum of New Zealand Te Papa Tongarewa, PO Box 467, Wellington, New Zealand.
MICHAEL BUNCE
Affiliation:
Trace and Environmental DNA (TrEnD) Laboratory, School of Molecular and Life Sciences, Curtin University, Perth, Western Australia6102, Australia.
TAMMY E. STEEVES
Affiliation:
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand.
*
*Authors for correspondence (both authors contributed equally); emails: [email protected]; [email protected]
*Authors for correspondence (both authors contributed equally); emails: [email protected]; [email protected]
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Summary

Cook’s Petrel Pterodroma cookii is an endemic New Zealand seabird that has experienced a large range decline since the arrival of humans and now only breeds on two offshore islands (Te Hauturu-o-Toi/Little Barrier Island and Whenua Hou/Codfish Island) at the extreme ends of its former distribution. Morphological, behavioural, and mitochondrial cytochrome oxidase 1 (CO1) sequence data led a previous study to recognise the two extant populations as distinct conservation management units. Here, we further examine the genetic relationship between the extant populations using two nuclear introns (β-fibint7 and PAX). Using one mitochondrial locus (CO1), we also investigate the past distribution of a single nucleotide polymorphism (SNP) that differentiates the modern populations using bone and museum skins sourced from within its former range across New Zealand’s North and South Islands. We found significant population genetic structure between the two extant Cook’s Petrel populations for one of the two nuclear introns (β-fibint7). The mitochondrial DNA CO1 analysis indicated that the SNP variant found in the Codfish Island population was formerly widely distributed across both the North and South Islands, whereas the Little Barrier Island variant was detected only in North Island samples. We argue that these combined data support the recognition of the extant populations as different subspecies. Previous names for these taxa exist, thus Cook’s Petrel from Little Barrier Island becomes Pterodroma cookii cookii and Cook’s Petrel from Codfish Island becomes P. c. orientalis. Furthermore, we suggest that both genetic and non-genetic data should be taken into consideration when planning future mainland translocations. Namely, any translocations on the South Island should be sourced from Codfish Island and future translocations on the North Island should continue to be sourced from Little Barrier Island only.

Keywords

Cook’s Petrelconservation geneticstranslocationseabird conservation
Type
Research Article
Information
Bird Conservation International , Volume 31 , Issue 1 , March 2021 , pp. 1 - 13
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of BirdLife International

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References

Allentoft, M. E., Collins, M., Harker, D., Haile, J., Oskam, C. L., Hale, M. L., Campos, P. F., Samaniego, J. A., Gilbert, M. T. P., Willerslev, E., Zhang, G., Scofield, R. P., Holdaway, R. N. and Bunce, M. (2012) The half-life of DNA in bone: measuring decay kinetics in 158 dated fossils. Proc. Roy. Soc. B: Biol. Sci. 279(1748): 4724–4733.CrossRefGoogle ScholarPubMed
Bandelt, H. J., Forster, P. and Rohl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16: 37–48.CrossRefGoogle ScholarPubMed
Bartle, J. A., Hu, D., Stahl, J. C., Pyle, P., Simons, T. R. and Woodby, D. (1990) Status and ecology of gadfly petrels in the temperate North Pacific. Proceedings of an International Symposium of the Pacific Seabird Group, Canadian Wildlife Service, and the British Columbia Ministry of Environment, Lands and Parks. Ontario, Canada: Canadian Wildlife Service, Publications Division.Google Scholar
Boessenkool, S., Austin, J. J., Worthy, T. H., Scofield, P., Cooper, A., Seddon, P. J. and Waters, J. M. (2009) Relict or colonizer? Extinction and range expansion of penguins in southern New Zealand. Proc. Roy. Soc. B: Biol. Sci. 276: 815.CrossRefGoogle ScholarPubMed
Brooke, M. D. L. (2004) Albatrosses and petrels across the world. Oxford, UK: Oxford University Press.Google Scholar
Brooke, M. D. L. and Rowe, G. (1996), Behavioural and molecular evidence for specific status of light and dark morphs of the Herald Petrel Pterodroma heraldica. Ibis 138: 420–432.CrossRefGoogle Scholar
Burg, T. M. and Croxall, J. P. (2001) Global relationships amongst black-browed and grey-headed albatrosses: Analysis of population structure using mitochondrial DNA and microsatellites. Mol. Ecol. 10: 2647–2660.CrossRefGoogle ScholarPubMed
Darriba, D., Taboada, G.L., Doallo, R. and Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Meth. 9: 772.CrossRefGoogle ScholarPubMed
Excoffier, L. and Lischer, H. E. L. (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.CrossRefGoogle ScholarPubMed
Friesen, V. (2015) Speciation in seabirds: why are there so many species…and why aren’t there more? J. Ornithol. 156: 27–39.CrossRefGoogle Scholar
Friesen, V. L., Burg, T. M. and McCoy, K. D. (2007a) Mechanisms of population differentiation in seabirds. Molec. Ecol. 16: 1765–1785.CrossRefGoogle Scholar
Friesen, V. L., Smith, A. L., Gomez-Diaz, E., Bolton, M., Furness, R. W., Gonzalez-Solis, J., Monteiro, L. R. (2007b) Sympatric speciation by allochrony in a seabird. Proc. Natl. Ac. Sci. U.S.A. 104: 18589–18594.CrossRefGoogle Scholar
Gangloff, B., Shirihai, H., Watling, D., Cruaud, C., Couloux, A., Tillier, A., Pasquet, E. and Bretagnolle, V. (2012a) The complete phylogeny of Pseudobulweria, the most endangered seabird genus: systematics, species status and conservation implications. Conserv. Genet. 13: 39–52.CrossRefGoogle Scholar
Gangloff, B., Zino, F. S., Gonzalez-Solis, J., Couloux, A., , E., , P. and Bretangolle, V. (2012b) The evolution of north-east Atlantic gadfly petrels using statistical phylogeography. Mol. Ecol. 22: 495–507.CrossRefGoogle Scholar
Garrick, R. C., Sunnucks, P. and Dyer, R. J. (2010) Nuclear gene phylogeography using PHASE: dealing with unresolved genotypes, lost alleles, and systematic bias in parameter estimation. BMC Evol. Biol. 10: 118.CrossRefGoogle ScholarPubMed
Gray, G. R. (1843) Fauna of New Zealand. Pp. 177–296 in E. Dieffenbach Travels in New Zealand, Book 2. London, UK: John Murray.Google Scholar
Haouchar, D., Pacioni, C., Haile, J., McDowell, M. C., Baynes, A., Phillips, M. J., Austin, J. J., Pope, L. C. and Bunce, M. (2016) Ancient DNA reveals complexity in the evolutionary history and taxonomy of the endangered Australian brush-tailed bettongs (Bettongia: Marsupialia: Macropodidae: Potoroinae). Biodivers. Conserv. 25: 2907–2927.CrossRefGoogle Scholar
Hofkin, B. V., Wright, A., Altenbach, J., Rassmann, K., Snell, H. M., Miller, R. D., Stone, A. C. and Snell, H. L. (2003) Ancient DNA gives green light to Galápagos Land Iguana repatriation. Conserv. Genet. 4: 105–108.CrossRefGoogle Scholar
Hung, C.-M., Drovetski, S. V. and Zink, R. M. (2016) Matching loci surveyed to questions asked in phylogeography. Proc. Biol. Sci. 283: 20152340.Google ScholarPubMed
Imber, M. J., West, J., , A. and Cooper, W. J. (2003) Cook's petrel (Pterodroma cookii): historic distribution, breeding biology, and effects of predators. Notornis 50: 221–230.Google Scholar
Iglesias-Vasquez, A., Gangloff, B., Ruault, S., Ribout, C., Priddel, D., Carlile, N., Friesen, V. L., Cibois, A. and Bretagnolle, V. (2017) Population expansion, current and past gene flow in Gould’s petrel: implications for conservation. Conserv. Genet. 18: 105–115.CrossRefGoogle Scholar
Karl, S. A., Toonen, R. J., Grant, W. S. and Bowen, B. W.. (2012) Common misconceptions in molecular ecology: Echoes of the modern synthesis. Mol. Ecol. 21: 4171–4189.CrossRefGoogle ScholarPubMed
Leonard, J. A. (2008) Ancient DNA applications for wildlife conservation. Mol. Ecol. 17: 4186–4196.CrossRefGoogle ScholarPubMed
Librado, P. and Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.CrossRefGoogle ScholarPubMed
Matthews, G. M. (1912) The birds of Australia . Vol 2. London, UK: Witherby & Co.Google Scholar
Medway, D. G. (2004) The type localities of Cook’s petrel (Pterodroma cookii), reef heron (Egretta sacra sacra) and wandering tattler (Tringa incana). Notornis 51: 155–158.Google Scholar
Milne, I., Lindner, D., Bayer, M., Husmeier, D., McGuire, G., Marshall, D. F. and Wright, F. (2008) TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25: 126–127.CrossRefGoogle ScholarPubMed
Miskelly, C. M., Taylor, G. A., Gummer, H. and Williams, R. (2009) Translocations of eight species of burrow-nesting seabirds (genera Pterodroma, Pelecanoides, Pachyptila and Puffinus: Family Procellariidae). Biol. Conserv. 142: 1965–1980.CrossRefGoogle Scholar
Morris-Pocock, J. A., Anderson, D. J. and Friesen, V. L. (2016) Biogeographical barriers to dispersal and rare gene flow shape population genetic structure in red-footed boobies (Sula sula). J. Biogeogr. 43: 2125–2135.CrossRefGoogle Scholar
Murphy, R. C. (1929) On Pterodroma cookii and its allies. Am. Mus. Novit. 370: 1–17.Google Scholar
Patel, S., Waugh, J., Millar, C. D. and Lambert, D. M. (2010) Conserved primers for DNA barcoding historical and modern samples from New Zealand and Antarctic birds. Mol. Ecol. Resourc. 10: 431–438.CrossRefGoogle ScholarPubMed
Prychitko, T. M. and Moore, W. S. (2003) Alignment and phylogenetic analysis of β-fibrinogen intron 7 sequences among avian orders reveal conserved regions within the intron. Mol. Biol. Evol. 20: 762–771.CrossRefGoogle ScholarPubMed
Rawlence, N. J., Scofield, R.P., Spencer, H. G., Lalas, C., Easton, L. J., Tennyson, A. J. D., Adams, M., Pasquet, E., Fraser, C., Waters, J. M. and Kennedy, M. (2016) Genetic and morphological evidence for two species of Leucocarbo shag (Aves, Pelecaniformes, Phalacrocoracidae) from southern South Island of New Zealand. Zool. J. Linn. Soc. 177: 676–694.CrossRefGoogle Scholar
Rawlence, N. J., Till, C. E., Easton, L. J., Spencer, H. G., Schuckard, R., Melville, D. S., Scofield, R. P., Tennyson, A. J. D., Rayner, M. J., Waters, J. M. and Kennedy, M. (2017) Speciation, range contraction and extinction in the endemic New Zealand King Shag complex. Mol. Phylogenet. Evol. 115: 197–209.CrossRefGoogle ScholarPubMed
Rayner, M. J., Clout, M. N., Stamp, R. K., Imber, M. J., Brunton, D. H. and Hauber, M. E. (2007) Predictive habitat modelling improves the population census accuracy of a burrowing seabird: a study of the endangered Cook's petrel. Biol. Conserv. 138: 235–247.CrossRefGoogle Scholar
Rayner, M. J., Carragher, C. J. F. and Hauber, M. E. (2010a) Mitochondrial DNA analysis reveals genetic structure in two New Zealand Cook’s petrel (Pterodroma cookii) populations. Conserv. Genet. 11: 2073–2077.CrossRefGoogle Scholar
Rayner, M. J., Hartill, B. W., Hauber, M. E. and Phillips, R. A. (2010b) Central place foraging by breeding Cook’s petrel Pterodroma cookii: foraging duration reflects range, diet and chick meal mass. Mar. Biol. 157: 2187–2194.CrossRefGoogle Scholar
Rayner, M. J., Parker, K. A. and Imber, M. J. (2008a) Population census of Cook's petrel Pterodroma cookii breeding on Codfish Island (New Zealand) and the global conservation status of the species. Bird Conserv. Internatn. 18: 211–218.CrossRefGoogle Scholar
Rayner, M. J., Hauber, M. E., Clout, M. N., Seldon, D. S., Van Dijken, S., Bury, S. and Phillips, R. A. (2008b) Foraging ecology of the Cook’s petrel Pterodroma cookii during the austral breeding season: a comparison of its two populations. Mar. Ecol. Progr. Ser. 370: 271–284.CrossRefGoogle Scholar
Rayner, M. J., Hauber, M. E., Steeves, T. E., Lawrence, H. A., Thompson, D. R., Sagar, P. M., Bury, S. J., Landers, T. J., Phillips, R. A., Ranjard, L. and Shaffer, S. A. (2011) Contemporary and historic separation of transhemispheric migration between two genetically distinct seabird populations. Nature Communications 2: 332.CrossRefGoogle Scholar
Rayner, M. J., Taylor, G., Gummer, H., Phillips, R. A., Sagar, P. M., Shaffer, S. A. and Thompson, D. R. (2012) Breeding cycle, year round distribution and activity patterns of the endangered Chatham petrel (Pterodroma axillaris). Emu 112: 107–116.CrossRefGoogle Scholar
Robertson, B. C., Stephenson, B. M. and Goldstien, S. J. (2011) When rediscovery is not enough: Taxonomic uncertainty hinders conservation of a critically endangered bird. Mol. Phylogenet. Evol. 61: 949–952.CrossRefGoogle Scholar
Rohland, N. and Hofreiter, M. (2007) Ancient DNA extraction from bones and teeth. Nat. Protoc. 2: 1756–1762.CrossRefGoogle ScholarPubMed
Russello, M. A., Poulakakis, N., Gibbs, J. P., Tapia, W., Benavides, E., Powell, J. R. and Caccone, A. (2010) DNA from the past informs ex situ conservation for the future: An "extinct" species of Galápagos tortoise identified in captivity. PLoS ONE 5: e8683.CrossRefGoogle ScholarPubMed
Shapiro, B. and Hofreiter, M. (2012) Ancient DNA: Methods and protocols. Humana Press Incorporated.CrossRefGoogle Scholar
Shepherd, L. and Lambert, D. (2008) Ancient DNA and conservation: lessons from the endangered kiwi of New Zealand. Mol. Ecol. 17: 2174–2184.CrossRefGoogle ScholarPubMed
Shepherd, L. D., Worthy, T. H., Tennyson, A. J. D., Scofield, R. P., Ramstad, K. M. and Lambert, D. M. (2012) Ancient DNA analyses reveal contrasting phylogeographic patterns amongst Kiwi (Apteryx spp.) and a recently extinct lineage of Spotted Kiwi. PLoS ONE 7: e42384.CrossRefGoogle Scholar
Spurgin, L. G., Wright, D. J., van der Velde, M., Collar, N. J., Komdeur, J., Burke, T. and Richardson, D. S. (2014), Museum DNA reveals the demographic history of the endangered Seychelles warbler. Evol. Applic. 7: 1134–1143.CrossRefGoogle ScholarPubMed
Steeves, T. E., Holdaway, R. N., Hale, M. L., McLay, E., McAllan, I. A. W., Christian, M., Hauber, M. E. and Bunce, M. (2010) Merging ancient and modern DNA: extinct seabird taxon rediscovered in the North Tasman Sea. Biol. Lett. 6: 94–97.CrossRefGoogle ScholarPubMed
Stephens, M. and Donnelly, P. (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am. J. Hum. Genet. 73: 1162–1169.CrossRefGoogle ScholarPubMed
Stephens, M., Smith, N. J. and Donnelly, P. (2001) A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68: 978–989.CrossRefGoogle ScholarPubMed
Toews, D. P. L. and Brelsford, A. (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol. Ecol. 21: 3907–3930.CrossRefGoogle ScholarPubMed
Towns, D. (2018) Ecological restoration on New Zealand islands: a history of shifting scales and paradigms. In: Moro, D., Ball, D. and Bryant, S., eds. Australian Island Arks: conservation management and opportunities. Clayton, Australia: CSIRO Publishing.Google Scholar
Valentine, K., Duffield, D. A., Patrick, L. E., Hatch, D. R., Butler, V. L., Hall, R. L. and Lehman, N. (2007) Ancient DNA reveals genotypic relationships among Oregon populations of the sea otter (Enhydra lutris). Conserv. Genet. 9: 933–938.CrossRefGoogle Scholar
Welch, A. J., Fleischer, R. C., James, H. F., Wiley, A. E., Ostrom, P. H., Adams, J., Duvall, F., Holmes, N., Hu, D., Penniman, J. and Swindle, K. A. (2012a) Population divergence and gene flow in an endangered and highly mobile seabird. Heredity 109: 19–28.CrossRefGoogle Scholar
Welch, A. J., Wiley, A. E., James, H. F., Ostrom, P. H., Stafford, T. W. Jr. and Fleischer, R. C. (2012b) Ancient DNA reveals genetic stability despite demographic decline: 3,000 years of population history in the endemic Hawaiian petrel. Mol. Biol. Evol. 29: 3729–3740.CrossRefGoogle Scholar
White, N. E., Dawson, R., Coghlan, M. L., Tridico, S. R., Mawson, P. R., Haile, J. and Bunce, M. (2012) Application of STR markers in wildlife forensic casework involving Australian black-cockatoos (Calyptorhynchus spp.). Forensic Sci. Int. Genet. 6: 664–670.CrossRefGoogle Scholar
Willerslev, E. and Cooper, A. (2005) Ancient DNA. Proc. Roy. Soc. B: Biol. Sci. 272: 3.CrossRefGoogle ScholarPubMed
Wilmshurst, J. M., Hunt, T. L., Lipo, C. P. and Anderson, A. J. (2011) High-precision radiocarbon dating shows recent and rapid initial human colonization of East Polynesia. Proc. Natl. Ac. Sci. 108: 1815.CrossRefGoogle ScholarPubMed
Worthy, T. H. and Holdaway, R. N. (2002) The lost world of the moa: Prehistoric life of New Zealand. Christchurch: Canterbury University Press.Google Scholar
Zink, R. M. and Barrowclough, G. F. (2008) Mitochondrial DNA under siege in avian phylogeography. Molec. Ecol. 17: 2107–2121.CrossRefGoogle ScholarPubMed
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