Origin and population history of a recent colonizer, the yellow warbler in Galápagos and Cocos Islands

Journal of Evolutionary Biology

Volumn 25, Issue 3, 2012, Pages 509-521

  Chaves, J A ^a   Parker, P G ^b,c,d   Smith, T B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MISSOURI ST LOUIS   (United States)

^c SAINT LOUIS ZOO   (United States)

^d Charles Darwin Foundation   (Ecuador)

Author keywords

Cocos Island; Colonization route; Divergence estimates; Gal pagos; Gene flow; Geographic isolation; Microsatellites; Yellow warbler

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

COLONIZATION; DISPERSAL; DIVERGENCE; FUNCTIONAL MORPHOLOGY; GENE FLOW; GENETIC ANALYSIS; GENETIC DIFFERENTIATION; GENETIC MARKER; HOMOGENEITY; MITOCHONDRION; POPULATION STRUCTURE; SELECTION; SONGBIRD; TAXONOMY;

ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; BODY SIZE; COMPARATIVE STUDY; COSTA RICA; DNA SEQUENCE; ECUADOR; EVOLUTION; GENE FLOW; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; HISTOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; POPULATION GENETICS; PRINCIPAL COMPONENT ANALYSIS; SEQUENCE ALIGNMENT; SONGBIRD; STATISTICAL MODEL;

ANIMALS; BASE SEQUENCE; BAYES THEOREM; BIOLOGICAL EVOLUTION; BODY SIZE; COSTA RICA; DNA, MITOCHONDRIAL; ECUADOR; GENE FLOW; GENETIC VARIATION; GENETICS, POPULATION; LIKELIHOOD FUNCTIONS; LINEAR MODELS; MICROSATELLITE REPEATS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; PRINCIPAL COMPONENT ANALYSIS; SELECTION, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SONGBIRDS;

COCOS ISLAND; COSTA RICA; ECUADOR; GALAPAGOS ISLANDS;

DENDROICA PETECHIA;

EID: 84857045335     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02447.x     Document Type: Article

References (82)

1. Abbott, I. & Abbott, L.K. 1978. Multivariate study of morphological variation in Galápagos and Ecuadorean mockingbirds. Condor 80: 301-308.
2. Alderson, G., Gibbs, H. & Sealy, S. 1999. Parentage and kinship studies in an obligate brood parasitic bird, the brown-headed cowbird (Molothrus ater), using microsatellite DNA markers. J. Hered. 90: 182-190.
3. Arbogast, B.S., Drovetski, S.V., Curry, R.L., Boag, P.T., Seutin, G., Grant, P.G. et al. 2006. The origin and diversification of Galápagos mockingbirds. Evolution 60: 370-382.
4. Barker, F.K., Cibois, A., Schikler, P., Feinstein, J. & Cracraft, J. 2004. Phylogeny and diversification of the largest avian radiation. Proc. Natl Acad. Sci. USA 101: 11040-11045.
5. Beerli, P. & Felsenstein, J. 1999. Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152: 763-773.
6. Benavides, E., Baum, R.B., Snell, H.M., Snell, H.L. & Sites, J.W. Jr 2009. Island biogeography of Galápagos lava lizards (Thropiduridae: Microlophus): species diversity and colonization of the archipelago. Evolution 63: 1606-1626.
7. Bollmer, J.L., Sanchez, T., Donaghy Cannon, M., Sanchez, D., Cannon, B., Bednarz, J.C. et al. 2003. Variation in morphology and mating system among island populations of Galápagos hawks. Condor 105: 425-438.
8. Bollmer, J.L., Kimball, R.T., Whiteman, N.K., Sarasola, J.H. & Parker, P.G. 2006. Phylogeography of the Galápagos hawk (Buteo galapagoensis): a recent arrival to the Galápagos Islands. Mol. Phylogen. Evol. 39: 237-247.
9. Browne, R.A., Collins, E. & Anderson, D.J. 2008. Genetic structure of Galápagos populations of yellow warbler. Condor 110: 549-553.
10. Browning, M.R. 1994. A taxonomic review of Dendroica petechia (Yellow Warbler; Aves: Parulinae). Proc. Biol. Soc. Washington 107: 27-51.
11. Burnham, K.P. & Anderson, D.R. 2002. Model Selection and Multimodel Inference: A Practical Information-theoretic Approach. Springer-Verlag, New York.
12. Burns, K.J., Hackett, S.J. & Klein, N.K. 2002. Phylogenetic relationships and morphological diversity in Darwin's finches and their relatives. Evolution 56: 1240-1252.
13. Caccone, A., Gibbs, J.P., Ketmaier, V., Suatoni, E. & Powell, J.R. 1999. Origin and evolutionary relationships of giant Galápagos tortoises. Proc. Natl Acad. Sci. USA 96: 13223-13228.
14. Caccone, A., Gentile, G., Gibbs, J.P., Fritts, T.H., Snell, H., Betts, J. et al. 2002. Phylogeography and history of giant Galápagos tortoises. Evolution 56: 2052-2066.
15. Chaves, J.A. & Smith, T.B. 2011. Evolutionary patterns of diversification in the Andean hummingbird genus Adelomyia. Mol. Phylogen. Evol. 60: 207-218.
16. Clegg, S.M., Degnan, S.M., Kikkawa, J., Moritz, C., Estoup, A. & Owens, I.P.F. 2002a. Genetic consequences of sequential founder events by an island-colonizing bird. Proc. Natl Acad. Sci. USA 99: 8127-8132.
17. Clegg, S.M., Degnan, S.M., Moritz, C., Kikkawa, J., Estoup, A. & Owens, I.P.F. 2002b. Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a passerine bird. Evolution 56: 2090-2099.
18. Clegg, S.M., Kelly, J.F., Kimura, M. & Smith, T.B. 2003. Combining genetic markers and stable isotopes to reveal population connectivity and migration patterns in a Neotropical migrant, Wilson's warbler (Wilsonia pusilla). Mol. Ecol. 12: 819-830.
19. Clegg, S.M., Frentiu, F.D., Kikkawa, J., Tavecchia, G. & Owens, P.F. 2008. 4000years of phenotypic change in an island bird: heterogeneity of selection over three microevolutionary timescales. Evolution 62: 2393-2410.
20. Colinvaux, P.A. 1984. The Galápagos climate: past and present. In: Galápagos (Perry. R, ed), pp. 55-69. Pergamon. Oxford, U.K.
21. Darwin, C.R. 1836 [1963]. Darwin's ornithological notes. (ed. Barlow. NP ) Bull. Brit. Mus. Nat. Hist. Ser 2: 201-278.
22. Dawson, R.J.G., Gibbs, H.L., Hobson, K.A. & Yezerinac, S.M. 1997. Isolation of microsatellite DNA markers from a passerine bird, Dendroica petechia (the yellow warbler), and their use in population studies. Heredity 79: 506-514.
23. Drummond, A.J. & Rambaut, A. 2006. BEAST v1.4. Available from:
24. Emerson, B.C. 2002. Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol. Ecol. 11: 951-966.
25. Endler, J.A. 1977. Geographic Variation, Speciation, and Clines. Princeton University Press, Princeton, NJ.
26. Ericson, P.G.P. & Johansson, U.S. 2003. Phylogeny of Passerida (Aves: Passeriformes) based on nuclear and mitochondrial sequence data. Mol. Phylogen. Evol. 29: 126-138.
27. 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.
28. Excoffier, L., Laval, G. & Schneider, S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinf. Online 1: 47-50.
29. Faircloth, B.C. 2008. MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design. Mol. Ecol. Resour. 8: 92-94.
30. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
31. Geist, D.J. 1992. Pyroclastic rocks as paleoclimate indicators, Galápagos Islands. In: Abstracts and Program, Chapman Conference on Climate, Volcanism and Global Change (Turco. RP, ed), p. 18. American Geophysical Union, Washington, DC.
32. Gibbs, H.L., Dawson, R.J.G. & Hobson, K.A. 2000. Limited differentiation in microsatellite DNA variation among northern populations of the yellow warbler: evidence for male-biased gene flow? Mol. Ecol. 9: 2137-2147.
33. Goudet, J. 2001. FSTAT (version 2.9.3.): A Program for Windows to Estimate and Test Gene Diversity and Fixation Indices. Institut d'Écologie, Université de Lausanne, Lausanne, Switzerland.
34. Grant, P.R. & Grant, B.R. 2002. Unpredictable evolution in a 30-year study of Darwin's finches. Science 296: 707-711.
35. Grant, P.R. & Grant, B.R. 2008. How and Why Species multiply: the Radiation of Darwin's Finches. Princeton University Press, Princeton, NJ.
36. Grant, P.R., Abbott, I., Schluter, D., Curry, R.L. & Abbott, L.K. 1985. Variation in the size and shape of Darwin's finches. Biol. J. Linn. Soc. 25: 1-39.
37. Hailer, F., Schreiber, E.A., Miller, J.M., Levin, I.I., Parker, P.G., Chesser, R.T. et al. 2010. Long-term isolation of a highly mobile seabird on the Galapagos. Proc. R. Soc. B 278: 817-825.
38. Hendry, A.P., Grant, P.R., Grant, R.B., Ford, H.A., Brewer, M.J. & Podos, J. 2006. Possible human impacts on adaptive radiation: beak size bimodality in Darwin's finches. Proc. R. Soc. B 273: 1887-1894.
39. Hendry, A.P., Huber, S.K., de Leon, L.F., Herrel, A. & Podos, J. 2009. Disruptive selection in a bimodal population of Darwin's finches. Proc. R. Soc. B 276: 753-759.
40. Hubisz, M.J., Falush, D., Stephens, M. & Pritchard, J.K. 2009. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9: 1322-1332.
41. Illera, J.C., Emerson, B.C. & Richardson, D.S. 2007. Population history of Berthelot's pipit: colonization, gene flow and morphological divergence in Macaronesia. Mol. Ecol. 16: 4599-4612.
42. Irwin, D.E., Alström, P., Olsson, U. & Benowitz-Fredericks, Z. 2001. Cryptic species in the genus Phylloscopus (Old World leaf warblers). Ibis 143: 233-247.
43. Klein, N.K. & Brown, W.M. 1994. Intraspecific molecular phylogeny in the Yellow Warbler (Dendroica petechia) and implications for avian biogeography in the West Indies. Evolution 48: 1914-1932.
44. Klicka, J., Johnson, K.P. & Lanyon, S.M. 2000. New World nine-primaried oscine relationships: constructing a mitochondrial DNA framework. Auk 117: 321-336.
45. Lack, D. 1947. Darwin's Finches. Cambridge University Press, Cambridge.
46. Langerhans, R.B., Layman, C.A., Langerhans, A.K. & Dewitt, T.J. 2003. Habitat- associated morphological divergence in two Neotropical fish species. Biol. J. Linn. Soc. 80: 689-698.
47. Lovette, I.J. 2004. Molecular phylogeny and plumage signal evolution in a trans Andean and circum Amazonian avian species complex. Mol. Phylogen. Evol. 32: 512-523.
48. Lovette, I.J., Bermingham, E. & Ricklefs, R.E. 2002. Clade-specific morphological diversification and adaptive radiation in Hawaiian songbirds. Proc. R. Soc. B 296: 37-42.
49. McCormack, J.E. & Smith, T.B. 2008. Niche expansion leads to small-scale adaptive divergence along an elevational gradient in a medium-sized passerine bird. Proc. R. Soc. B 275: 2155-2164.
50. Milá, B., Wareen, B.H., Heeb, P. & Thébaud, C. 2010. The geographic scale of diversification on islands: genetic and morphological divergence at a very small spatial scale in the Mascarene grey white-eye (Aves: Zosterops borbonicus). BMC Evol. Biol. 10: 158.
51. Milot, E., Gibbs, H.L. & Hobson, K.A. 2000. Phylogeography and genetic structure of northern populations of the Yellow Warbler (Dendroica petechia). Mol. Ecol. 5: 667-681.
52. Nei, M. 1972. Genetic distance between populations. Am. Nat. 106: 283-292.
53. Nylander, J.A.A., Wilgenbusch, J.C., Warren, D.L. & Swofford, D.L. 2008. AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. Bioinformatics 24: 581-583.
54. Olson, S.L. 1980. Geographic variation in the yellow warblers (Dendroica petechia: Parulidae) of the Pacific coast of Middle and South America. Proc. Biol. Soc. Wash. 93: 473-480.
55. Paradis, E. 2010. Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26: 419-420.
56. Petren, K. 1998. Microsatellite primers from Geospiza fortis and cross-species amplification in Darwin's finches. Mol. Ecol. 7: 782-1784.
57. Petren, K., Grant, B.R. & Grant, P.R. 1999. A phylogeny of Darwin's finches based on microsatellite DNA length variation. Proc. R. Soc. Lond. B 266: 321-329.
58. Phillimore, A.B., Owens, I.P.F., Black, R.A., Chittock, J., Burke, T. & Clegg, S.M. 2008. Complex patterns of genetic and phenotypic divergence in an island bird and the consequences for delimiting conservation units. Mol. Ecol. 17: 2839-2853.
59. Posada, D. 2008. jModelTest: phylogenetic Model Averaging. Mol. Biol. Evol. 25: 1253-1256.
60. Power, D.M. 1975. Similarity among avifaunas of the Galápagos Islands. Ecology 56: 616-626.
61. Price, T. 1991. Morphology and ecology of breeding warblers along an altitudinal gradient in Kashmir, India. J. Anim. Ecol. 60: 643-664.
62. Pritchard, J.K., Stephens, M. & Donnelly, P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
63. R Development Core Team 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria,
64. Rambaut, A. & Drummond, A.J. 2007. Tracer v.1.4, Available from
65. Raymond, M. & Rousset, F. 1995. Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249 (available from: ).
66. Rice, W.R. 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.
67. Ricklefs, R.E. & Bermingham, E. 2007. The causes of evolutionary radiations in archipelagoes: passerine birds in the Lesser Antilles. Am. Nat. 169: 285-297.
68. Ronquist, F. & Huelsenbeck, J.P. 2003. MRBAYES 3.1.2: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
69. Rozen, S. & Skaletsky, H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132: 365-386.
70. Ruokonen, M. & Kvist, L. 2002. Structure and evolution of the avian mitochondrial control region. Mol. Phylogen. Evol. 23: 422-432.
71. Santiago-Alarcón, D., Tanksley, S.M. & Parker, P.G. 2006. Morphological variation and genetic structure of Galápagos dove (Zenaida galapagoensis) populations: issues in conservation for the Galápagos bird fauna. Wilson J. Ornithol. 118: 194-207.
72. Schluter, D. & Grant, P.R. 1984. Determinants of morphological patterns in communities of Darwin's finches. Am. Nat. 123: 175-196.
73. Schneider, C. & Moritz, C. 1999. Rainforest refugia and evolution in Australia's wet tropics. Proc. R. Soc. B 266: 191-196.
74. Schreiber, R.W. & Schreiber, E.A. 1984. Central Pacific Seabirds and the El Niño Southern Oscillation: 1982 to 1983 perspectives. Science 17: 713-716.
75. Smith, T.B., Wayne, R.K., Girman, D.J. & Bruford, M.W. 1997. A role for ecotones in generating rainforest biodiversity. Science 276: 1855-1857.
76. Soobramoney, S., Downs, C.T. & Adams, N.J. 2005. Morphological variation in the common fiscal (Lanius collaris) along an altitudinal gradient in southern Africa. Ostrich 76: 130-141.
77. Sulloway, F.J. 1982. Darwin's conversion: the Beagle voyage and its aftermath. J. Hist. Biol. 15: 325-396.
78. * and Other Methods) Ver 4.0b4a. Sinauer Associates, Sunderland.
79. Templeton, A.R., Crandall, K.A. & Sing, C.F. 1992. A cladistic analysis of phenotypic association with haplotypes inferred from restriction endonuclease mapping and DNAsequence data. III. Cladogram estimation. Genetics 132: 619-635.
80. Warren, B.H., Bermingham, E., Prys-Jones, R.P. & Thébaud, C. 2006. Immigration, species radiation and extinction in a highly diverse lineage: white-eyes on Indian Ocean islands. Mol. Ecol. 15: 3769-3786.
81. Weir, B.S. & Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
82. Weir, J.T. & Schluter, D. 2008. Calibrating the avian molecular clock. Mol. Ecol. 17: 2321-2328.