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The complete phylogeny of Pseudobulweria, the most endangered seabird genus: systematics, species status and conservation implications

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Abstract

Pseudobulweria is one of the least known and most endangered of all seabird genera. It comprises six taxa, of which two are extinct, three are critically endangered and one is near threatened. Phylogenetic relationships between these taxa and position of the genus in the Order Procellariiformes have never been studied, and the taxonomic status of several taxa remains unsettled. Conservation management of Pseudobulweria taxa will be enhanced if these uncertainties are resolved. We used a multilocus gene tree approach with two mitochondrial DNA markers (cytochrome oxidase subunit 1 and cytochrome b gene) and one nuclear intron (β Fibrinogen intron 7) to investigate phylogenetic relationships within the genus using sequences from all taxa. We combined gene trees to estimate a phylogeny of the genus using a multispecies coalescent methodology. We confirmed the link between Pseudobulweria and a clade comprising Puffinus and Bulweria genera. The Fiji petrel’s status, as belonging to the genus, is confirmed, as is the specific status of newly rediscovered Beck’s petrel. Maintenance of the two sub-species of Tahiti petrel as currently described is not supported. Discovering the breeding grounds of all taxa is the key for their conservation, which is vital to both the marine and fragile insular tropical ecosystems where Pseudobulweria are apical predators.

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References

  • Attié C, Stahl J-C, Bretagnolle V (1997) New data on the endangered mascarene petrel Pseudobulweria aterrima: a third twentieth century specimen and distribution. Colon Waterbirds 20:406–412

    Article  Google Scholar 

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

    Google Scholar 

  • Bowen BW (1999) Preserving genes, species or ecosystems? Healing the fractured foundations of conservation policy. Mol Ecol 8:S5–S10

    Article  PubMed  CAS  Google Scholar 

  • Bretagnolle V (1993) Adaptive significance of seabird colouration: the case of Procellariiforms. Am Nat 142(1):141–173

    Article  PubMed  CAS  Google Scholar 

  • Bretagnolle V (1995) Systematics of the soft-plumaged petrel Pterodroma mollis complex: new insight from vocalizations. Ibis 137:207–218

    Article  Google Scholar 

  • Bretagnolle V, Attié C, Pasquet E (1998) Cytochrome b evidence for validity and phylogenetic relationships of Pseudobulweria and Bulweria. Auk 115(1):188–195

    Google Scholar 

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

    Google Scholar 

  • Buchanan GM, Butchart SHM, Dutson G, Pilgrim JD, Steininger MK, Bishop KD, Mayaux P (2008) Using remote sensing to inform conservation status assessment: estimates of recent deforestation rates on New Britain and the impacts upon endemic birds. Biol Conserv 141:56–66

    Article  Google Scholar 

  • Carstens BC, Knowles LL (2007) Estimating species phylogeny from gene tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Syst Biol 56:400–411

    Article  PubMed  Google Scholar 

  • Collar NJ, Andrew P (1988) Birds to watch. ICBP technical publication No. 8. Cambridge, UK

    Google Scholar 

  • Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 24(6):332–340

    Article  PubMed  Google Scholar 

  • Del Hoyo J, Elliott A, Sargatal J (1992) Handbook of the birds of the world, vol 1. Lynx Edicions, Barcelona

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Drummond SP, Wilson KA, Meijaard E, Watts M, Dennis R, Christy L, Posingham HP (2009) Influence of a threatened-species focus on conservation planning. Conserv Biol 24(2):441–449

    Article  PubMed  Google Scholar 

  • Ebersberger I, Galgoszy P, Taudien S, Taenzer S, Platzer M, von Haeseler A (2007) Mapping human genetic ancestry. Mol Biol Evol 24(10):2266–2276

    Article  PubMed  CAS  Google Scholar 

  • Farrier D, Whelan R, Mooney C (2007) Threatened species listing as a trigger for conservation action. Environ Sci Policy 10(3):219–229

    Article  Google Scholar 

  • Friesen VL, Burg TM, McCoy KD (2007) Mechanisms of population differentiation in seabirds. Mol Ecol 16:1765–1785

    Article  PubMed  CAS  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 

  • Haq BU, Hardenbol J, Vail PR (1987) Chronology of fluctuating sea levels since the triassic. Science 235:1156–1167

    Article  PubMed  CAS  Google Scholar 

  • Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLOS Biol 2(10):e312

    Article  PubMed  Google Scholar 

  • Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27(3):570–580

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Imber MJ (1985) Origins, phylogeny and taxonomy of the gadfly petrels Pterodroma spp. Ibis 127:197–229

    Article  Google Scholar 

  • IUCN (2010) IUCN red list of threatened species. Version 2010.2. www.iucnredlist.org. Downloaded on 26 July 2010

  • Janis CM (1993) Tertiary mammal evolution in the context of changing climates, vegetation and tectonic events. Annu Rev Ecol Syst 24:467–500

    Article  Google Scholar 

  • Jennings WB, Edwards SV (2005) Speciational history of Australian grassfinches (Poephila) inferred from thirty gene trees. Evolution 59:2033–2047

    PubMed  CAS  Google Scholar 

  • Jesus J, Menezes D, Gomes S, Oliveira P, Nogales M, Brehm A (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 19:1–16

    Article  Google Scholar 

  • Johnsen A, Rindal E, Ericson PGP, Zuccon D, Kerr KCR, Stoeckle MY, Lifjeld JT (2010) DNA barcoding of Scandinavian birds reveals divergent lineages in trans-Atlantic species. J Ornithol. doi:10.1007/s10336-009-0490-3

  • Jouanin C, Mougin JL (1979) Order Procellariiformes. In: Mayr E, Cottrell GW (eds) Checklist of birds of the world, vol 1, 2nd edn. Museum of Comparative Zoology, Cambridge, pp 48–121

    Google Scholar 

  • Kennedy M, Page RDM (2002) Seabird supertrees: combining partial estimates of Procellariiform phylogeny. Auk 119(1):88–108

    Article  Google Scholar 

  • Kerr KCR, Stoeckle MY, Dove CJ, Weigt LA, Francis CM, Hebert PDN (2007) Comprehensive DNA barcode coverage of North American birds. Mol Ecol Notes 7:535–543

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Le Corre M, Ghestemme T, Salamolard M, Couzi F-X (2003) Rescue of the mascarene petrel, a critically endangered seabird of Reunion Island, Indian Ocean. Condor 105:387–391

    Article  Google Scholar 

  • LeCorre M, Ollivier A, Ribes S, Jouventin P (2002) Light-induced mortality of petrels: a 4 year study from Reunion Island (Indian Ocean). Biol Conserv 105:93–102

    Article  Google Scholar 

  • Lewis AR et al (2008) Mid-miocene cooling and the extinction of tundra in continental Antarctica. Proc Natl Acad Sci USA 105(31):10676–10680

    Article  PubMed  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Yu L, Kubatko L, Pearl DK, Edwards SV (2009a) Coalescent methods for estimating phylogenetic trees. Mol Phylogenetic Evol 53(1):320–328

    Article  CAS  Google Scholar 

  • Liu L, Yu L, Pearl DK, Edwards SV (2009b) Estimating species phylogenies using coalescence times among sequences. Syst Biol 58:468–477

    Article  PubMed  CAS  Google Scholar 

  • Mathews GM (1936) A note on the black Fiji petrel. Ibis 6:309

    Google Scholar 

  • Mayr G (2009) Notes on the osteology and phylogenetic affinities of the oligocene Diomedeoididae (Aves, Procellariiformes). Fossil Rec 12(2):133–140

    Article  Google Scholar 

  • Miller KG, Fairbanks RG (1983) Evidence for oligocene—middle miocene abyssal circulation changes in the western North Atlantic. Nature 306(5940):250–253

    Article  CAS  Google Scholar 

  • Mundy NI (2005) A window on the genetics of evolution: MC1R and plumage colouration in birds. Proc R Soc B 272:1633–1640

    Article  PubMed  CAS  Google Scholar 

  • Murphy RC (1928) Birds collected during the Whitney South Sea Expedition. IV. American Museum Novitates 322

  • Nichols R (2001) Gene trees and species trees are not the same. Trends Ecol Evol 16(7):358–364

    Article  PubMed  Google Scholar 

  • Nunn GB, Stanley SE (1998) Body size effects and rates of cytochrome b evolution in tube-nosed seabirds. Mol Biol Evol 15:1360–1371

    PubMed  CAS  Google Scholar 

  • O’Meara BC (2010) New heuristic methods for joint species delimitation and species tree inference. Syst Biol 59(1):59–73

    Article  PubMed  Google Scholar 

  • Olson SL (1975) Remarks on the generic characters of Bulweria. Ibis 117:111–113

    Article  Google Scholar 

  • Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5(5):568–583

    PubMed  CAS  Google Scholar 

  • Penhallurick J, Wink M (2004) Analysis of the taxonomy and nomenclature of the Procellariiformes based on complete nucleotide sequences of the mitochondrial cytochrome b gene. Emu 104:125–147

    Article  CAS  Google Scholar 

  • Pereira SL, Baker AJ (2006) A mitogenomic timescale for birds detects variable phylogenetic rates of molecular evolution and refutes the standard molecular clock. Mol Biol Evol 23(9):1731–1740

    Article  PubMed  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Posigham HP, Andelman SJ, Burgman MA, Medellin RA, Master LL, Keith DA (2002) Limits to the use of threatened species lists. Trends Ecol Evol 17(11):503–507

    Article  Google Scholar 

  • Priddel D, Carlile N, Moce K, Watling D (2008) A review of records and recovery actions for the critically endangered Fiji petrel Pseudobulweria macgillivrayi. Bird Conserv Int 18:381–393

    Article  Google Scholar 

  • Prychitko TM, Moore WS (1997) The utility of DNA sequences of an intron from the β-fibrinogen gene in phylogenetic analysis of woodpeckers (Aves: Picidae). Mol Phylogenetic Evol 8:193–204

    Article  CAS  Google Scholar 

  • Rheindt FE, Austin JJ (2005) Major analytical and conceptual shortcomings in a recent taxonomic revision of the Procellariiformes—a reply to Penhallurick and Wink (2004). Emu 105:181–186

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP, Van der Mark P (2005) MrBayes 3.1 Manual. http://mrbayes.csit.fsu.edu/. Accessed March 2010

  • Shevenell AE, Kennett JP, Lea DW (2004) Middle miocene Southern ocean cooling and Antarctic cryosphere expansion. Science 305:1766–1770

    Article  PubMed  CAS  Google Scholar 

  • Shirihai H (2008) Rediscovery of beck’s petrel Pseudobulweria becki, and other observations of tubenoses from the bismarck archipelago, papua new Guinea. Bull Br Ornithol Club 128:3–16

    Google Scholar 

  • Shirihai H, Pym T, Kretzschmar J, Moce K, Taukei A, Watling D (2009) First observation of Fiji petrel Pseudobulweria macgillivrayi at sea: off Gau island, Fiji, in May 2009. Bull Br Ornithol Club 129:129–148

    Google Scholar 

  • Sibley CG, Monroe BL (1990) Distribution and taxonomy of birds of the world. Yale University Press, New Haven

    Google Scholar 

  • Sullivan J, Joyce P (2005) Model selection in phylogenetics. Annu Rev Ecol Evol Syst 36:445–466

    Article  Google Scholar 

  • Syring J, Farrell K, Businsky R, Cronn R, Liston A (2007) Widespread genealogical non-monophyly in species of Pinus subgenus Strobus. Syst Biol 56:163–181

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Villard P, Dano S, Bretagnolle V (2006) First data on the breeding biology of the Tahiti petrel Pseudobulweria rostrata. Ibis 148:285–291

    Article  Google Scholar 

  • Warham J (1990) The petrels: their ecology and breeding systems. Academic Press, London

    Google Scholar 

  • Warheit KI (1992) A review of the fossil seabirds from the tertiary of the North Pacific: plate tectonics, paleoceanography, and faunal change. Paleobiology 18(4):401–424

    Google Scholar 

  • Warheit KI (2002) The seabird fossil record and the role of paleontology in understanding seabird community structure. In: Schreiber, Burger (eds) Biology of marine birds. CRC Press, Boca Raton

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Worthy TH, Tennyson AJD (2004). Avifaunal assemblages from the Nenega-Iti and Onemea sites. In: Conte E, Vinton Kirch P (eds) Archaeological Investigations in the Mangareva Islands (Gambier Archipelago), French Polynesia, Chapter 6. Archaeological Research Facility Contributions No. 62. University of California, Berkeley

  • Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39(3):306–314

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Rannala B (2010) Bayesian species delimitations using multilocus sequence data. PNAS 107(20):9264–9269

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the “Consortium National de Recherche en Génomique”, and the “Service de Systématique Moléculaire” of the Muséum National d’Histoire Naturelle (CNRS UMS 2700). It is part of the agreement No. 2005/67 between the Genoscope and the Muséum National d’Histoire Naturelle on the project “Macrophylogeny of life” directed by Guillaume Lecointre. We are deeply indebted to Joel Cracraft, Curator, Paul Sweet, Collection Manager, and Margaret Hart at the American Museum of Natural History (AMNH) for giving us access to the collections and providing samples from Pseudobulweria becki type specimens. BG also acknowledges receipt of a Collection Study Grant from the AMNH. We thank Alice Cibois for providing us samples from P. rostrata rostrata from Marquesas. Many thanks also to T. Steeves and P. Pelser for useful comments that improved an early draft of the manuscript and to two anonymous referees whose comments greatly improved the manuscript.

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Authors and Affiliations

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

    Benoit Gangloff & Vincent Bretagnolle

  2. c/o Ausserdorfstraße 6, 8052, Zurich, Switzerland

    Hadoram Shirihai

  3. NatureFiji-MareqetiViti, Box 2041, Government Buildings, Suva, Fiji. 259 Prince’s Road, Tamavua, Suva, Fiji

    Dick Watling

  4. Génoscope. Centre National de Séquençage, 2, rue Gaston Crémieux, CP5706, 91057, Evry Cedex, France

    Corinne Cruaud & Arnaud Couloux

  5. Département Systématique et Evolution, Museum National d’Histoire Naturelle, UMR7205 Origine, Structure et Evolution de la Biodiversité, 55 rue Buffon, Paris, France

    Annie Tillier & Eric Pasquet

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  1. Benoit Gangloff
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Correspondence to Benoit Gangloff.

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Gangloff, B., Shirihai, H., Watling, D. et al. The complete phylogeny of Pseudobulweria, the most endangered seabird genus: systematics, species status and conservation implications. Conserv Genet 13, 39–52 (2012). https://doi.org/10.1007/s10592-011-0261-6

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