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Genetic panmixia in New Zealand’s Grey-faced Petrel: implications for conservation and restoration

Hayley A. Lawrence A , Phil O’B. Lyver B and Dianne M. Gleeson A C D

A Landcare Research – Manaaki Whenua, Private Bag 92170, Auckland 1142, New Zealand.
B Landcare Research – Manaaki Whenua, PO Box 69040, Lincoln 7640, New Zealand.
C Present address: Institute for Applied Ecology, University of Canberra, Bruce, ACT 2601, Australia.
D Corresponding author. Email: dianne.gleeson@canberra.edu.au

Emu - http://dx.doi.org/10.1071/MU13078
Submitted: 15 August 2013  Accepted: 16 January 2014   Published online: 16 June 2014


 
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Abstract

Seabirds are highly vagile yet many have restricted gene flow owing to physical barriers (e.g. land or ice) or non-physical barriers (e.g. philopatry), which often results in population divergence. Identification of distinct units is important for defining conservation status, guiding restoration of populations and coastal ecosystems, and managing the effect of anthropogenic activities (e.g. fisheries by-catch, customary harvesting). We collected DNA samples from 390 Grey-faced Petrels (Pterodroma macroptera gouldi) at 13 colonies across their New Zealand breeding range to examine population genetic structure. We sequenced part of the mitochondrial control region and genotyped 12 microsatellite DNA loci. We found high diversity in mitochondrial DNA in all colonies. Analyses showed a lack of genetic structure in Grey-faced Petrels that we propose is a result of high levels of gene flow. Although, we found no genetically distinct populations we suggest that any translocations for conservation should be done with caution and with some consideration of the proximity of a restoration site to a natal Grey-faced Petrel colony. Also, the high levels of gene flow we found suggest that the method of using acoustic attraction and natural behaviour to establish new colonies offers a useful addition, or alternative, to translocations of chicks. These results provide a genetic basis for conservation and restoration efforts for the Grey-faced Petrel.

Additional keywords: dispersal, gene flow, population genetic structure, Pterodroma, seabird translocation.


References

Abbott, C. L., Double, M. C., Trueman, J. W. H., Robinson, A., and Cockburn, A. (2005). An unusual source of apparent mitochondrial heteroplasmy: duplicate mitochondrial control regions in Thalassarche albatrosses. Molecular Ecology 14, 3605–3613.
CrossRef | CAS | PubMed |

Abdelkrim, J., Robertson, B. C., Stanton, J.-A. L., and Gemmell, N. J. (2009). Fast, cost-effective development of species-specific microsatellite markers by genomic sequencing. BioTechniques 46, 185–192.
CrossRef | CAS | PubMed |

Atherton, R. A., McComish, B. J., Shepherd, L. D., Berry, L. A., Albert, N. W., and Lockhart, P. J. (2010). Whole genome sequencing of enriched chloroplast DNA using the Illumina GAII platform. Plant Methods 6, 22.
CrossRef | PubMed |

Baker, A. J., and Marshall, H. D. (1997). Mitochondrial control region sequences as tools for understanding evolution. In ‘Avian Molecular Evolution and Systematics’. (Ed. D. P. Mindell.) pp. 51–82. (Academic Press: London.)

Bandelt, H. J., Forster, P., and Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.
CrossRef | CAS | PubMed |

Benjamini, Y., and Yekutieli, D. (2001). The control of false discovery rate under dependancy. Annals of Statistics 29, 1165–1188.

Bried, J., Dubois, M.-P., Jouventin, P., and Santos, R. S. (2008). Eleven polymorphic microsatellite markers in Cory’s Shearwater, Calonectris diomedea, and cross-species amplification on threatened Procellariiformes. Molecular Ecology Resources 8, 602–604.
CrossRef | CAS | PubMed |

Brownstein, M. J., Carpten, J. D., and Smith, J. R. (1996). Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. BioTechniques 20, 1004–1010.
| CAS | PubMed |

Cornuet, J. M., and Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.
| CAS | PubMed |

Dewoody, J., Nason, J. D., and Hipkins, V. D. (2006). Mitigating scoring errors in microsatellite data from wild populations. Molecular Ecology Notes 6, 951–957.
CrossRef | CAS |

Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T., and Wilson, A. (2012). Geneious version 5.6. (Biomatters: Auckland.) Available at http://www.geneious.com [Verified 1 April 2014].

Dubois, M.-P., Jarne, P., and Jouventin, P. (2005). Ten polymorphic microsatellite markers in the Wandering Albatross Diomedea exulans. Molecular Ecology Notes 5, 905–907.
CrossRef | CAS |

Dunn, R. (2012). The breeding biology of the Grey-faced Petrel Pterodroma macroptera gouldi. M.Sc. Thesis, School of Biological Sciences, University of Auckland.

Earl, D. A., and vonHoldt, B. M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
CrossRef |

Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software structure: a simulation study. Molecular Ecology 14, 2611–2620.
CrossRef | CAS | PubMed |

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. Molecular Ecology Resources 10, 564–567.
CrossRef | PubMed |

Excoffier, L., Smouse, P., and 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.
| CAS | PubMed |

Excoffier, L., Laval, G., and Schneider, S. (2005). ARLEQUIN version 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.
| CAS |

Faircloth, B. C. (2008). MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design. Molecular Ecology Resources 8, 92–94.
CrossRef | CAS | PubMed |

Falush, D., Stephens, M., and Pritchard, J. K. (2003). Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 164, 1567–1587.
| CAS | PubMed |

Friesen, V. L., González, J. A., and Cruz-Delgado, F. (2006). Population genetic structure and conservation of the Galapagos Petrel (Pterodroma phaeopygia). Conservation Genetics 7, 105–115.
CrossRef |

Friesen, V. L., Burg, T. M., and McCoy, K. D. (2007). Mechanisms of population differentiation in seabirds. Molecular Ecology 16, 1765–1785.
CrossRef | CAS | PubMed |

Gill, B. J., Bell, B. D., Chambers, G. K., Medway, D. G., Palma, R. L., Scofield, R. P., Tennyson, A. J. D., and Worthy, T. H. (2010). ‘Checklist of the Birds of New Zealand, Norfolk and Macquarie Islands, and the Ross Dependency, Antarctica’, 4th edn. (Te Papa Press: Wellington, New Zealand.)

Gonzalez, E. G., Genovart, M., Oro, D., Zardoya, R., and Juste, J. (2009). Polymorphic microsatellite markers for the critically endangered Balearic Shearwater, Puffinus mauretanicus. Molecular Ecology Resources 9, 1044–1046.
CrossRef | CAS | PubMed |

González-Jaramillo, M., and Rocha-Olivares, A. (2011). Barriers acting on the genetic structure of a highly aerial seabird: the Magnificent Frigatebird. Biochemical Systematics and Ecology 39, 392–396.
CrossRef |

Guo, S., and Thompson, E. (1992). Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48, 361–372.
CrossRef | CAS | PubMed |

Heather, B. D., and Robertson, H. A. (2005). ‘The Field Guide to the Birds of New Zealand’, revised edn. (Penguin NZ: Auckland.)

Holdaway, R. N. (1989). New Zealand’s pre-human avifauna and its vulnerability. New Zealand Journal of Ecology 12, 11–25.

Holdaway, R. N., Worthy, T. H., and Tennyson, A. J. D. (2001). A working list of breeding bird species of the New Zealand region at first human contact. New Zealand Journal of Zoology 28, 119–187.
CrossRef |

Hubisz, M. J., Falush, D., Stephens, M., and Pritchard, J. K. (2009). Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9, 1322–1332.
CrossRef | PubMed |

Imber, M., Harrison, M., and Harrison, J. (2000). Interactions between petrels, rats and Rabbits on Whale Island and effects of rat and Rabbit eradication. New Zealand Journal of Ecology 24, 153–160.

Imber, M. J., Harrison, M., Wood, S. E., and Cotter, R. N. (2003). An estimate of numbers of Grey-faced Petrels (Pterodroma macroptera gouldi) breeding on Moutohorā (Whale Island), Bay of Plenty, New Zealand, during 1998–2000. Notornis 50, 23–26.

Jones, H. P., and Kress, S. W. (2012). A review of the world’s active seabirds restoration projects. Journal of Wildlife Management 76, 2–9.
CrossRef |

Jones, C. J., Clifford, H., Fletcher, D., Cuming, P., and Lyver, P. O’B. (2011). Survival and age-at-first-return estimates for Grey-faced Petrels (Pterodroma macroptera gouldi) breeding on Mauao and Motuotau Island in the Bay of Plenty, New Zealand. Notornis 58, 71–80.

Küpper, C., Horsburgh, G. J., Dawson, D. A., French-Constant, R., Szekely, T., and Burke, T. (2007). Characterization of 36 polymorphic microsatellite loci in the Kentish Plover (Charadrius alexandrinus) including two sex-linked loci and their amplification in four other Charadrius species. Molecular Ecology Notes 7, 35–39.
CrossRef |

Kuro-o, M., Yonekawa, H., Saito, S., Eda, M., Higuchi, H., Koike, H., and Hasegawa, H. (2010). Unexpectedly high genetic diversity of mtDNA control region through severe bottleneck in vulnerable albatross Phoebastria albatrus. Conservation Genetics 11, 127–137.
CrossRef | CAS |

Lawrence, H. A., Taylor, G. A., Millar, C. D., and Lambert, D. M. (2008a). High mitochondrial and nuclear genetic diversity in one of the world’s most endangered seabirds, the Chatham Island Taiko (Pterodroma magentae). Conservation Genetics 9, 1293–1301.
CrossRef |

Lawrence, H. A., Taylor, G. A., Crockett, D. E., Millar, C. D., and Lambert, D. M. (2008b). New genetic approach to detecting individuals of rare and endangered species. Conservation Biology 22, 1267–1276.
CrossRef | PubMed |

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

Longmire, J. L., Lewis, A. K., Brown, N. C., Buckingham, J. M., Clark, L. M., Jones, M. D., Meincke, L. J., Meyne, J., Ratliff, R. L., Ray, F. A., Wagner, R. P., and Moyzis, R. K. (1988). Isolation and molecular characterization of a highly polymorphic centromeric tandem repeat in the family Falconidae. Genomics 2, 14–24.
CrossRef | CAS | PubMed |

Lyver, P. O’B., David, J., Ngamane, L., Anderson, A., and Clarkin, P. (2008). Hauraki Māori Mātauranga for the conservation and harvest of Tītī, Pterodroma macroptera gouldi. Papers and Proceedings of the Royal Society of Tasmania 142, 149–160.
CrossRef |

MacLeod, C. J., Adams, J., and Lyver, P. O’B. (2008). At-sea distribution of satellite-tracked Grey-faced Petrels, Pterodroma macroptera gouldi, captured on the Ruamaahua (Alderman) Islands, New Zealand. Papers and Proceedings of the Royal Society of Tasmania 142, 73–88.
CrossRef |

Marko, P. B., and Hart, M. W. (2011). The complex analytical landscape of gene flow inference. Trends in Ecology & Evolution 26, 448–456.
CrossRef |

Markwell, T. J., and Daugherty, C. H. (2002). Invertebrate and lizard abundance is greater on seabird-inhabited islands than on seabird-free islands in the Marlborough Sounds, New Zealand. Ecoscience 9, 293–299.

Millener, P. R. (1981). The Quaternary avifauna of the North Island, New Zealand. Ph.D. Thesis, Geology Department, University of Auckland.

Milot, E., Weimerskirch, H., and Bernatchez, L. (2008). The seabird paradox: dispersal, genetic structure and population dynamics in a highly mobile, but philopatric albatross species. Molecular Ecology 17, 1658–1673.
CrossRef | CAS | PubMed |

Miskelly, C. M., and Taylor, G. A. (2004). Establishment of a colony of Common Diving Petrels (Pelecanoides urinatrix) by chick transfers and acoustic attraction. Emu 104, 205–211.
CrossRef |

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). Biological Conservation 142, 1965–1980.
CrossRef |

Moller, H. (2006). Are current harvests of seabirds sustainable? Acta Zoologica Sinica 52, 649–652.

Morris-Pocock, J. A., Taylor, S. A., Birt, T. P., Damus, M., Piatt, J. F., Warheit, K. I., and Friesen, V. L. (2008). Population genetic structure in Atlantic and Pacific Ocean Common Murres (Uria aalge): natural replicate tests of post-Pleistocene evolution. Molecular Ecology 17, 4859–4873.
CrossRef | CAS | PubMed |

Morris-Pocock, J. A., Taylor, S. A., Birt, T. P., and Friesen, V. L. (2010). Concerted evolution of duplicated mitochondrial control regions in three related seabird species. BMC Evolutionary Biology 10, 14.
CrossRef | PubMed |

Narum, S. R. (2006). Beyond Bonferroni: less conservative analyses for conservation genetics. Conservation Genetics 7, 783–787.
CrossRef | CAS |

Nei, M. (1987). ‘Molecular Evolutionary Genetics.’ (Columbia University Press: New York.)

Palsbøll, P. J., Bérubé, M., and Allendorf, F. W. (2007). Identification of management units using population genetic data. Trends in Ecology & Evolution 22, 11–16.
CrossRef |

Peakall, R., and Smouse, P. E. (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
CrossRef |

Posada, D., and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
CrossRef | CAS | PubMed |

Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| CAS | PubMed |

Ramos-Onsins, S. E., and Rozas, J. (2002). Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19, 2092–2100.
CrossRef | CAS | PubMed |

Rayner, M. J., Carraher, C. J. F., Clout, M. N., and Hauber, M. E. (2010). Mitochondrial DNA analysis reveals genetic structure in two New Zealand Cook’s Petrel (Pterodroma cookii) populations. Conservation Genetics 11, 2073–2077.
CrossRef |

Rayner, M. J., Hauber, M. E., Steeves, T. E., Lawrence, H. A., Thompson, D. R., Sagar, P. M., Bury, S. J., Landers, T. J., Philips, R. A., Ranjard, L., and Shaffer, S. A. (2011). Contemporary and historical separation of transequatorial migration between genetically distinct seabird populations. Nature Communications 2, 332.
CrossRef | PubMed |

Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43, 223–225.
CrossRef |

Rozen, S., and Skaletsky, H. (2000). PRIMER 3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics Methods and Protocols: Methods in Molecular Biology’. (Eds S. Krawetz and S. Misener.) pp. 365–386. (Humana Press: Totowa, NJ.)

Ryman, N., and Palm, S. (2006). POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Molecular Ecology Resources 6, 600–602.
CrossRef |

Sawyer, S. L., and Fogle, S. R. (2010). Acoustic attraction of Grey-faced Petrels (Pterodroma macroptera gouldi) and Fluttering Shearwaters (Puffinus gavia) to Young Nick’s Head, New Zealand. Notornis 57, 166–168.

Seutin, G., White, B. N., and Boag, P. T. (1991). Preservation of avian blood and tissue samples for DNA analysis. Canadian Journal of Zoology 69, 82–90.
CrossRef | CAS |

Shaffer, S. A., Tremblay, Y., Weimerskirch, H., Scott, D., Thompson, D. R., Sagar, P. M., Moller, H., Taylor, G. A., Foley, D. G., Block, B. A., and Costa, D. P. (2006). Migratory shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer. Proceedings of the National Academy of Sciences of the United States of America 103, 12799–12802.
CrossRef | CAS | PubMed |

Steeves, T. E., Anderson, D. J., and Friesen, V. L. (2005). A role for nonphysical barriers to gene flow in the diversification of a highly vagile seabird, the Masked Booby (Sula dactylatra). Molecular Ecology 14, 3877–3887.
CrossRef | CAS | PubMed |

Stow, A. J., and Magnusson, W. E. (2012). Genetically defining populations is of limited use for evaluating and managing human impacts on gene flow. Wildlife Research 39, 290–294.

Tajima, F. (1983). Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460.
| CAS | PubMed |

Tamura, K., and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.
| CAS | PubMed |

Taylor, G. A. (2000). Action plan for seabird conservation in New Zealand. Part B: Non-threatened seabirds. Threatened Species Occasional Publication 17. Department of Conservation, Wellington.

Taylor, S. A., and Friesen, V. L. (2012). Use of molecular genetics for understanding seabird evolution, ecology and conservation. Marine Ecology Progress Series 451, 285–304.
CrossRef |

Techow, N. M. S. M., and O’Ryan, C. (2004). Characterization of microsatellite loci in White-chinned Petrel (Procellaria aequinoctialis) and cross-amplification in six other procellariiform species. Molecular Ecology Notes 4, 33–35.
CrossRef | CAS |

Towns, D. R., Wardle, D. A., Mulder, C. P. H., Yeates, G. W., Fitzgerald, B. M., Parrish, G. R., Bellingham, P. J., and Bonner, K. I. (2009). Predation of seabirds by invasive rats: multiple indirect consequences for invertebrate communities. Oikos 118, 420–430.
CrossRef |

van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
CrossRef | CAS |

Warham, J. (1996). ‘The Behaviour, Population Biology and Physiology of the Petrels.’ (Academic Press: London.)

Welch, A. J., Wiley, A. E., James, H. F., Ostrom, P. H., Stafford, T. W., and Fleischer, R. C. (2012a). Ancient DNA reveals genetic stability despite demographic decline: 3,000 years of population history in the endemic Hawaiian Petrel. Molecular Biology and Evolution 29, 3729–3740.
CrossRef | CAS | PubMed |

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. (2012b). Population divergence and gene flow in an endangered and highly mobile seabird. Heredity 109, 19–28.
CrossRef | CAS | PubMed |

Whitehead, A. L., Lyver, P. O’B., Jones, C., Macleod, C. J., Bellingham, P. J., Coleman, M., Karl, B. J., Drew, K., Pairman, D., Gormley, A. M., and Duncan, R. P. (2014). Establishing accurate baseline estimates of breeding populations of a burrowing seabird, the Grey-faced Petrel (Pterodroma macroptera gouldi) in New Zealand. Biological Conservation 169, 109–116.
CrossRef |

Wiley, A. E., Welch, A. J., Ostrom, P. H., James, H. F., Stricker, C. A., Fleischer, R. C., Gandhi, H., Adams, J., Ainley, D. G., Duvall, F., Holmes, N., Hu, D., Judge, S., Penniman, J., and Swindle, K. A. (2012). Foraging segregation and genetic divergence between geographically proximate colonies of a highly mobile seabird. Oecologia 168, 119–130.
CrossRef | PubMed |

Williams, M., Gummer, H., Powlesland, R., Robertson, H., and Taylor, G. (2006). ‘Migrations and Movements of Birds to New Zealand and Surrounding Seas.’ (Department of Conservation Science & Technical Publishing: Wellington.)

Young, L. C. (2010). Inferring colonization history and dispersal patterns of a long-lived seabird by combining genetic and empirical data. Journal of Zoology 281, 232–240.

Zink, R. M., and Barrowclough, G. F. (2008). Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology 17, 2107–2121.
CrossRef | CAS | PubMed |


   
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