Advertisement

Marine Biology

, Volume 153, Issue 6, pp 1113–1125 | Cite as

Morphological and molecular variation within an ocean basin in wedge-tailed shearwaters (Puffinus pacificus)

  • Darren R. PeckEmail author
  • Wesley J. Bancroft
  • Bradley C. Congdon
Research Article

Abstract

Micro-evolutionary processes that underpin genetic and morphological variation in highly mobile pelagic vertebrates are virtually unknown. Previous findings preferentially invoke vicariant isolation due to large-scale physical barriers such as continental landmasses, followed by genetic drift. However increasingly, evidence for divergence by non-random processes (e.g. selection, plasticity) is being presented. Wedge-tailed shearwaters are wide-ranging seabirds with breeding colonies located such that they experience a variety of environmental pressures and conditions. Previous work on this species has provided evidence of inter-colony divergence of adult morphology and foraging modes, as well as chick developmental patterns, suggesting that reinforcement among colonies is possible. In order to evaluate the micro-evolutionary processes driving this observed variation, our study compared patterns of gene flow with morphological and environmental variation among four colonies of wedge-tailed shearwater breeding within the Indo-Pacific Ocean basin. Estimates of gene flow differed according to the genetic marker used; most likely, this is a function of different mutation rates. Nuclear introns suggest that gene flow among wedge-tailed shearwater breeding colonies within the Indo-Pacific Ocean basin is substantial, however microsatellite markers imply that gene flow is reduced. In general, levels of genetic divergence were relatively low and did not correlate with geographic distance, morphological distance or environmental differences (sea-surface temperature and chlorophyll a concentration) among colonies. We suggest that genetic drift alone is unlikely to be the major source of morphological variation seen in this species. Instead, we propose that non-random processes (selection, plasticity) underpin morphological diversity seen in this and possibly other seabird species.

Keywords

Gene Flow Markov Chain Monte Carlo Discriminant Function Analysis Breeding Coloni Culmen Length 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

Our sincere thanks to the following people and institutions who provided logistic assistance during this project: Y. Peck, T. Wilson, S. Thompson, I. Hutton, D. Wilcox, C. Bagnato, the staff of the Heron Island Research Station and the Lord Howe Island Board. This research was funded by a James Cook University Merit Research Grant (MRG-02/0026), The Ecological Society of Australia, Reef CRC and Australian Geographic. Work was authorized under New South Wales NPWS License number S10914, QNPWS Permits C6/000175/00/SAA and C6/000195/01/SAA, and James Cook University-Ethics Approval A627_00.

References

  1. Ashmole NP, Ashmole MJ (1967) Comparative feeding of seabirds of a tropical oceanic island. Peabody Museum of Natural History 24:1–131Google Scholar
  2. Avise JC, Alisauskas RT, Nelson WS, Ankney CD (1992) Matriarchal population genetic structure in an avian species with female natal philopatry. Evolution 46:1084–1096CrossRefGoogle Scholar
  3. Bancroft WJ, Garkaklis MJ, Roberts JD (2004) Continued expansion of the Wedge-tailed Shearwater, Puffinus pacificus, nesting colonies on Rottnest Island, Western Australia. Emu 104:79–82CrossRefGoogle Scholar
  4. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedGoogle Scholar
  5. Banke S, MCDonald BA (2005) Migration patterns among global populations of the pathogenic fungus Mycosphaerella graminicola. Mol Ecol 14:1881–1896PubMedCrossRefGoogle Scholar
  6. Barbraud C, Weimerskirch H, Robertson G, Jouventin P (1999) Size-related life history traits: insights from a studyof snow petrels (Pagodroma nivea). J Avian Biol 68:1179–1182Google Scholar
  7. Barrowclough GF (1983) Biochemical studies of microevolutionary preocesses. In: Brush AH, Clark JGA (eds) Perspectives in ornithology. University of Cambridge Press, Cambridge, pp. 223–261Google Scholar
  8. Beaumont MA (2001) Conservation Genetics. In: Balding DJ, Bishop M, Cannings C (eds) Handbook of statistical genetics. Wiley, New YorkGoogle Scholar
  9. Beerli P (1998) Estimation of migration rates and population sizes in geographically structured populations. In: Carvalho G (ed) Advances in molecular ecology. IOS Press, AmsterdamGoogle Scholar
  10. Beerli P (2002) MIGRATE documentation. Version 1.6. http://evolution.genetics.washington.edu/lamarc/migrate.html
  11. Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773PubMedGoogle Scholar
  12. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568PubMedCrossRefGoogle Scholar
  13. Bittner TD, King RB (2003) Gene flow and melanism in garter snakes revisited: a comparison of molecular markers and island vs. coalescent models. Biol J Linnean Soc 79:389–399CrossRefGoogle Scholar
  14. Bohonak AJ (2002) Software for reduced major axis regression V 1.2. San Diego State UniversityGoogle Scholar
  15. Bosch E, Calafell F, Santos FR et al (1999) Variation in short tandem repeats is deeply structured by genetic background on the human Y chromosome. Am J Human Genet 65:1623–1638CrossRefGoogle Scholar
  16. Bruen TC, Philippe H, Bryant D (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172:2665–2681PubMedCrossRefGoogle Scholar
  17. Campbell NA, Atchley WR (1981) The geometry of canonical variate analysis. Syst Zool 30:268–280CrossRefGoogle Scholar
  18. Chan Y, Arcese P (2003) Morphological and microsatellite differentiation in Melospiza melodia (Aves) at a microgeographic scale. J Evol Biol 16:939–947PubMedCrossRefGoogle Scholar
  19. Ciofi C, Beaumont MA, Swingland IR, Bruford MW (1999) Genetic divergence and units for conservation in the Komodo dragon Varanus komodoensis. Proc R Soc B 266:2269–2274CrossRefGoogle Scholar
  20. Clegg SM, Degnan SM, Moritz C et al (2002) Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a Passerine bird. Evolution 56:2090–2099PubMedGoogle Scholar
  21. Congdon BC, Krockenberger AK, Smithers BV (2005) Dual foraging strategy in a tropical Procellariid, the wedge-tailed shearwater. Mar Ecol Progr Ser 301:293–301CrossRefGoogle Scholar
  22. Congdon BC, Piatt JF, Martin K, Friesen VL (2000) Mechanisms of population differentiation in marbled murrelets: historical versus contemporary processes. Evolution 54:974–986PubMedGoogle Scholar
  23. Cornuet JM, Luikart G, (1997) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014Google Scholar
  24. Dearborn DC, Anders AD, Schreiber EA, Adams RMM, Mueller UG (2003) Inter-island movements and population differentiationin a pelagic seabird. Mol Ecol 12:2835–2843PubMedCrossRefGoogle Scholar
  25. Dyer PK, Hill GJE, Barnes A (1995) Three decades of burrow estimates for wedge-tailed shearwaters on the Capricorn Group. EMU 95:272–279CrossRefGoogle Scholar
  26. Dyer PK (1999) Wedge-tailed shearwaters at Raine Island, Great Barrier Reef: population estimate and breeding status. Corella 23:1–6Google Scholar
  27. Dyer PK (2002) Burrow occupancy by wedge-tailed shearwaters and flesh-footed shearwaters on Lord Howe Island. Corella 26:38–40Google Scholar
  28. Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton, NJGoogle Scholar
  29. Filatov DA (2002) ProSeq: a software for preparation and evolutionary analysis of DNA sequence data sets. Mol Ecol Notes 2:621–624CrossRefGoogle Scholar
  30. Friesen VL, Congdon BC, Walsh HE, Birt TP (1997) Intron variation in marbled murrelets detected using analyses of single-stranded conformational polymorphisms. Mol Ecol 6:1047–1058PubMedCrossRefGoogle Scholar
  31. Friesen VL, Montevecchi WA, Baker AJ, Barretts RT, Davidson WS (1996) Population differentiation and evolution in the common guillemot Uria aalge. Mol Ecol 5:793–805PubMedGoogle Scholar
  32. Fullard KJ, Early G, Heide-Jorgensen MP et al (2000) Population structure of long-finned pilot whales in the north Atlantic: a correlation with sea surface temperature? Mol Ecol 9:949–958PubMedCrossRefGoogle Scholar
  33. Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372PubMedCrossRefGoogle Scholar
  34. Haldane JB (1954) An exact test for randomness of mating. J Genet 52:631–635Google Scholar
  35. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evolut 23:254–267CrossRefGoogle Scholar
  36. Jarne P, Lagoda JL (1996) Microsatellites, form molecules to populations and back. TREE 11:424–429Google Scholar
  37. Jolley KA, Feil EJ, Chan MS, Maiden MC (2001) Sequence type analysis and recombinational tests (START). Bioinformatics 17:1230–1231PubMedCrossRefGoogle Scholar
  38. Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795CrossRefGoogle Scholar
  39. Kirkpatrick M, Ravigne V (2002) Speciation by natural and sexual selection: models and experiments. Am Natur 159:S22–S35CrossRefPubMedGoogle Scholar
  40. Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on coalescent. Genetics 149:429–434PubMedGoogle Scholar
  41. Mantel N (1967) the detection of disease clustering and a generalised regression approach. Canc Res 27:209–220Google Scholar
  42. Marshall JL, Arnold ML, Howard DJ (2002) Reinforcement: the road not taken. Trends Ecol Evol 17:558–563CrossRefGoogle Scholar
  43. Marchant S, Higgins PJ, (1990) Handbook of Australian, New Zealand & Antarctic birds. Oxford University Press, MelbourneGoogle Scholar
  44. Mayr E (1942) Systematics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  45. Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge, MAGoogle Scholar
  46. Miller KJ, Benzie JAH (1997) No clear genetic distinction between morphological species within the coral genus platygyra. Bull Mar Sci 61:907–917Google Scholar
  47. Monteiro LR, Furness RW (1998) Speciation through temporal segregation of Madeiran storm petrel (Oceanodroma castro) populations in the Azores? Philos Tran R Soc Lond B 353:945–953CrossRefGoogle Scholar
  48. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  49. Palumbi SR (2003) Population genetics, demographic connectivity and the design of marine protected areas. Ecol Appl 13:S146–S158CrossRefGoogle Scholar
  50. Palumbi SR, Baker CS (1994) Contrasting population structure from nuclear intron sequences and mtDNA of Humpback Whales. Mol Biol Evol 11:426–435PubMedGoogle Scholar
  51. Pearson D, Shine R, How R (2002) Sex-specific niche partitioning and sexual size dimorphism in Australian pythons (Morelia spilota imbricata). Biol J Linn Soc 77:113–125CrossRefGoogle Scholar
  52. Peck DR, Congdon BC (2004) Reconciling historical processes and population structure in the sooty tern Sterna fuscata. J Avian Biol 35:327–335CrossRefGoogle Scholar
  53. Peck DR, Congdon BC (2005) Colony-specific foraging behaviour and co-ordinated divergence of chick development in the wedge-tailed shearwater Puffinus pacificus. Mar Ecol Progr Ser 299:289–296CrossRefGoogle Scholar
  54. Peck DR, Smithers BV, Krockenberger A, Congdon BC (2004) Sea surface temperature constrains wedge-tailed shearwater foraging success within breeding seasons. Mar Ecol Progr Ser 281:259–266CrossRefGoogle Scholar
  55. Peck DR, Congdon BC (2006) Sex-specific chick provisioning and diving behaviour in the wedge-tailed shearwater. J Avian Biol 37:1–7CrossRefGoogle Scholar
  56. Pennycuick CJ (1989) Bird flight performance: a practical calculation manual. Oxford University Press, OxfordGoogle Scholar
  57. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 98:13757–13762PubMedCrossRefGoogle Scholar
  58. Posada D (2002) Evaluation of methods for detecting recombination from DNA sequences: empirical data. Mol Biol Evol 19:708–717PubMedGoogle Scholar
  59. Quinn GP, Keough MJ (2003) Experimental design and data analysis for biologists. Cambridge University Press, MelbourneGoogle Scholar
  60. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  61. Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103PubMedGoogle Scholar
  62. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  63. Rice WR, Hostert EE (1993) Laboratory experiments on speciation: What have we learned in 40 years? Evolution 47:1637–1653CrossRefGoogle Scholar
  64. Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538PubMedGoogle Scholar
  65. Schneider S, Kueffer JM, Roessli D, Excoffier L (1997) Arlequin: a sofware for population genetic data analysis. Genetics and Biometry Laboratory, Department of Antropology, University of Geneva, Geneva, SwitzerlandGoogle Scholar
  66. Seutin G, White BN, Boag PT (1991) Preservation of avian blood sample tissue for DNA analysis. Can J Zool, vol 69Google Scholar
  67. Smith TB, Wayne RK, Girman J, Bruford MW (1997) A role for ecotones in generating rainforest biodiversity. Science 276:1855–1857CrossRefGoogle Scholar
  68. Sokal RR, Rohlf FJ (1995) Biometry. W. H. Freeman, New YorkGoogle Scholar
  69. Steeves TE, Anderson DJ, Friesen VL (2005) A role for nonphysical barriers to gene flow in the diversification of a highly vagile seabird, the masked booby (Sula dactylatra). Mol Ecol 14:3877–3887PubMedCrossRefGoogle Scholar
  70. Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Human Genet 73:1162–1169CrossRefGoogle Scholar
  71. Stephens M, Smith N, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Human Genet 68:978–989CrossRefGoogle Scholar
  72. Techow NMSM, O’Ryan C (2004) Characterisation of microsatellite loci in White-chinned Petrel (Procellaria aequinoctialis) and cross-amplification in six other procellariiform species. Mol Ecol Notes 4:33–35CrossRefGoogle Scholar
  73. Waugh SM, Weimerskirch H (2003) Environmental heterogeneity and the evolution of foraging behaviour in long ranging greater albatrosses. OIKOS 103:374–384CrossRefGoogle Scholar
  74. Waugh SM, Weimerskirch H, Cherel Y, Prince PA (2000) Contrasting strategies of provisioning and chick growth in two sympatrically breeding albatrosses at Cambell Island, New Zealand. The Condor 102:804–813CrossRefGoogle Scholar
  75. Wright S (1931) Evolution in mendelian populations. Genetics 16:97–159PubMedGoogle Scholar
  76. Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Darren R. Peck
    • 1
    • 3
    Email author
  • Wesley J. Bancroft
    • 2
  • Bradley C. Congdon
    • 1
  1. 1.School of Tropical BiologyJames Cook UniversityCairnsAustralia
  2. 2.School of Animal BiologyUniversity of Western AustraliaCrawleyAustralia
  3. 3.CSIRO EntomologyCanberraAustralia

Personalised recommendations