Genetic, morphological, and acoustic evidence reveals lack of diversification in the colonization process in an island bird

Evolution

Volumn 68, Issue 8, 2014, Pages 2259-2274

  Illera, Juan Carlos ^a,b   Palmero, Ana M ^a,b   Laiolo, Paola ^a   Rodríguez, Felipe ^c   Moreno, Ángel C ^d   Navascués, Miguel ^e  

^a UNIVERSITY OF OVIEDO   (Spain)

^b INSTITUTO DE PRODUCTOS NATURALES Y AGROBIOLOGÍA   (Spain)

^c Biodiversity Service Canary Government Servicios Múltiples II building   (Spain)

^d Vice Council of Environment Environ Impact Serv Las Palmas de Gran Canaria   (Spain)

^e CENTRE DE BIOLOGIE ET DE GESTION DES POPULATIONS   (France)

Author keywords

Avian evolution; Gene flow; Lack of diversification; Macaronesia; Oceanic islands

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANATOMY AND HISTOLOGY; ANIMAL; CAPE VERDE; DNA SEQUENCE; EVOLUTION; GENE FLOW; GENETICS; ISLAND (GEOLOGICAL); MOLECULAR GENETICS; POPULATION GENETICS; PORTUGAL; SONGBIRD; SPAIN; VOCALIZATION;

ANIMALS; BIOLOGICAL EVOLUTION; CAPE VERDE; DNA, MITOCHONDRIAL; GENE FLOW; GENETICS, POPULATION; ISLANDS; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; PORTUGAL; SEQUENCE ANALYSIS, DNA; SONGBIRDS; SPAIN; VOCALIZATION, ANIMAL;

EID: 84905234284     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12429     Document Type: Article

References (103)

1. Baldwin, M. W., H. Winkler, C. L. Organ, and B. Helm . 2010. Wing pointedness associated with migratory distance in common-garden and comparative studies of stonechats (Saxicola torquata). J. Evol. Biol. 23:1050-1063.
2. Beaumont, M. A. 2008. Joint determination of topology, divergence time, and immigration in population trees. Pp. 135-154 in S. Matsumura, P. Forster, and C. Renfrew, eds. Simulation, genetics, and human prehistory. McDonald Institute for Archaeological Research, Cambridge, U.K.
3. Beaumont, M. A., W. Zhang, and D. J. Balding . 2002. Approximate Bayesian computation in population genetics. Genetics 162:2025-2035.
4. BirdLife International. 2012. Species factsheet: Sylvia conspicillata. Available at http://www.birdlife.org. Accessed August 13, 2012.
5. Blackburn, T. M., K. J. Gaston, and N. Loder . 1999. Geographic gradients in body size: a clarification of Bergmann's rule. Divers. Distrib. 5:165-174.
6. Blum, M. G. B., and O. François . 2010. Non-linear regression models for approximate Bayesian computation. Stat. Comput. 20:63-73.
7. Brambilla, M., O. Janni, F. Guidali, and A. Sorace . 2008. Song perception among incipient species as a mechanism for reproductive isolation. J. Evol. Biol. 21:651-657.
8. Chaves, J. A., P. G. Parker, and T. B. Smith . 2012. Origin and population history of a recent colonizer, the yellow warbler in Galápagos and Cocos Islands. J. Evol. Biol. 25:509-521.
9. Cibois, A., J. C. Thibault, and E. Pasquet . 2007. Uniform phenotype conceals double colonization by reed-warblers of a remote Pacific archipelago. J. Biogeogr. 34:1150-1166.
10. Clegg, S. M., and A. B. Phillimore . 2010. The influence of gene flow and drift on genetic and phenotypic divergence in two species of Zosterops in Vanuatu. Philos. Trans. Roy. Soc. B 365:1077-1092.
11. Clegg, S. M., S. M. Degnan, J. Kikkawa, C. Moritz, A. Estoup, and I. P. F. Owens . 2002a. Genetic consequences of sequential founder events by an island-colonizing bird. Proc. Natl. Acad. Sci. USA 99:8127-8132.
12. Clegg, S. M., S. M. Degnan, C. Moritz, A. Estoup, J. Kikkawa, and I. P. F. Owens . 2002b. Microevolution in island forms: the role of drift and directional selection in morphological divergence of a passerine bird. Evolution 56:2090-2099.
13. Cornuet, J.-M., F. Santos, M. A. Beaumont, C. P. Robert, J.-M. Marin, D. J. Balding, T. Guillemaud, and A. Estoup . 2008. Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation. Bioinformatics 24:2713-2719.
14. Cramp, S. 1992. Birds of the Western Paleartic. Vol. 6. Oxford Univ. Press, Oxford. U.K.
15. Crawford, N. G. 2010. SMOGD: software for the measurement of genetic diversity. Mol. Ecol. Resour. 10:556-557.
16. Clement, M., D. Posada, and K. Crandall . 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9:1657-1660.
17. Csilléry, K., O. François, and M. G. B. Blum . 2012. abc: an R package for approximate Bayesian computation (ABC). Methods Ecol. Evol. 3:475-479.
18. Del Hoyo, J., A. Elliot, and D. A. Christie . 2006. Handbook of the birds of the world-volume 11: old world flycatchers to old world warblers. Lynx Editions, Barcelona.
19. Dennison, M. D., and A. J. Baker . 1991. Morphometric variability in continental and Atlantic island populations of chaffinches (Fringilla coelebs). Evolution 45:29-39.
20. Dietzen, C., E. Garcia, G. Delgado, and M. Wink . 2008. Phylogenetic differentiation of Sylvia species (Aves: Passeriformes) of the Atlantic islands (Macaronesia) based on mitochondrial DNA sequence data and morphometrics. Biol. J. Linn. Soc. 95:157-174.
21. Earl, D. A., and B. M. vonHoldt . 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Gen. Resour. 4:359-361.
22. Edwards, S. V., P. Arctander, and A. C. Wilson . 1991. Mitochondrial resolution of a deep branch in the genealogical tree for perching birds. Proc. R. Soc. Lond. B 243:99-107.
23. Edwards, S. V., S. B. Kingan, J. D. Calkins, C. N. Balakrishnan, W. B. Jennings, W. J. Swanson, and M. D. Sorenson . 2005. Speciation in birds: genes, geography, and sexual selection. Proc. Natl. Acad. Sci. USA 102:6550-6557.
24. Emerson, B. C. 2002. Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol. Ecol. 11:951-966.
25. Emerson, B. C., and P. Oromí . 2005. Diversification of the forest beetle genus Tarphius on the Canary Islands, and the evolutionary origins of island endemics. Evolution 59:586-598.
26. Evanno, G., S. Regnaut, and J. Goudet . 2005. Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol. Ecol. 14:2611-2620.
27. Excoffier, L., and H. E. L. Lischer . 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.
28. Goldstein, D. B., A. R. Linares, L. L. Cavalli-Sforza, and M. W. Feldman . 1995. Genetic absolute dating based on microsatellites and the origin of modern humans. Proc. Natl. Acad. Sci. USA 92:6723-6727.
29. Goudet, J. 2002. FSTAT version 2.9.3.2, a program to estimate and test gene diversities and differentiation statistics from codominant genetic markers. Available at http://www2.unil.ch/popgen/softwares/fstat.htm.
30. Grant, B. R., and P. R. Grant . 2010. Songs of Darwin's finches diverge when a new species enters the community. Proc. Natl. Acad. Sci. USA 107:20156-20163.
31. Grant, P. R., and B. R. Grant . 1997. Mating patterns of Darwin's finch hybrids determined by song and morphology. Biol. J. Linn. Soc. 60:317-343.
32. Grant, P. R., and B. R. Grant . 2008. How and why species multiply. The radiation of Darwin's finches. Princeton Univ. Press, Princeton, NJ. 218 p.
33. Griffiths, R., M. C. Double, K. Orr, and R. J. G. Dawson . 1998. A DNA test to sex most birds. Mol. Ecol. 7:1071-1075.
34. Hall, M. L., S. A. Kingma, and A. Peters . 2013. Male songbird indicates body size with low-pitched advertising songs. PLoS One 8:e56717.
35. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
36. Harshman, J. 1996. Phylogeny, evolutionary rates, and ducks. Ph.D. diss., University of Chicago, Chicago.
37. Hazevoet, C. J. 1995. The birds of the Cape Verde Islands. B.O.U. Check-list No. 13. The British Ornithologist's Union, Tring, U.K. 192 p.
38. Hoeck, P. E. A., J. L. Bollmer, P. G. Parker, and L. F. Keller . 2010. Differentiation with drift: a spatio-temporal genetic analysis of Galápagos mockingbird populations (Mimus spp.). Philos. Trans. Roy. Soc. B 365:1127-1138.
39. Holleley, C. E., and P. G. Geerts . 2009. Multiplex Manager 1.0: a crossplatform computer program that plans and optimizes multiplex PCR. BioTechniques 46:511-517.
40. Hudson, R. R. 2002. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18:337-338.
41. Illera, J. C., M. Díaz, and M. Nogales . 2006. Ecological traits influence the current distribution and range of an island endemic bird. J. Biogeogr. 33:1192-1201.
42. Illera, J. C., B. C. Emerson, and D. S. Richardson . 2007. Population history of Berthelot's pipit: colonization, gene flow and morphological divergence in Macaronesia. Mol. Ecol. 16:4599-4612.
43. Illera, J. C., D. S. Richardson, B. Helm, J. C. Atienza, and B. C. Emerson . 2008. Phylogenetic relationships, biogeography and speciation in the avian genus Saxicola. Mol. Phylogenet. Evol. 48:1145-1154.
44. Illera, J. C., K. Koivula, J. Broggi, M. Päckert, J. Martens, and L. Kvist . 2011. A multi-gene approach reveals a complex evolutionary history in the Cyanistes species group. Mol. Ecol. 20:4123-4139.
45. Illera, J. C., J. C. Rando, D. S. Richardson, and B. C. Emerson . 2012. Age, origin and extinctions of the avifauna of Macaronesia: a synthesis of phylogenetic and fossil information. Quat. Sci. Rev. 50:14-22.
46. Irwin, D. E., S. Bensch, and T. D. Price . 2001. Speciation in a ring. Nature 409:333-337.
47. Jombart, T., S. Devillard, and F. Balloux . 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 11:94.
48. Jønsson, K. A., M. Irestedt, L. Christidis, S. M. Clegg, B. G. Holt, and J. Fjeldså . 2014. Evidence of taxon cycles in an Indo-Pacific passerine bird radiation (Aves: Pachycephala). Proc. R. Soc. Lond. B 281:20131727.
49. Jost, L. 2008. GST and its relatives do not measure differentiation. Mol. Ecol. 17:4015-4026.
50. Kenta, T., J. Gratten, N. S. Haigh, G. N. Hinten, J. Slate, R. K. Butlin, and T. Burke . 2008. Multiplex SNP-SCALE: a cost-effective medium-throughput single nucleotide polymorphism genotyping method. Mol. Ecol. Resour. 8:1230-1238.
51. Kirchman, J. J. 2009. Genetic tests of rapid parallel speciation of flightless birds from an extant volant ancestor. Biol. J. Linn. Soc. 96:601-616.
52. Kirschel, A. N. G., D. T. Blumstein, and T. B. Smith . 2009. Character displacement of song and morphology in African tinkerbirds. Proc. Natl. Acad. Sci. USA 106:8256-8261.
53. Kocher, T. D., W. K. Thomas, A. Meyer, S. V. Edwards, S. Pääbo, F. X. Villablanca, and A. C. Wilson . 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 86:6196-6200.
54. Kuhner, M. K. 2009. Coalescent genealogy samplers: windows into population history. Trends Ecol. Evol. 24:86-93.
55. Laiolo, P. 2012. Interspecific interactions drive cultural co-evolution and acoustic convergence in syntopic species. J. Anim. Ecol. 81:594-604.
56. Laiolo, P., and A. Rolando . 2003. The evolution of vocalisations in the genus Corvus: effects of phylogeny, morphology and habitat. Evol. Ecol. 17:111-123.
57. Lapiedra, O., D. Sol, S. Carranza, and J. M. Beaulieu . 2013. Behavioural changes and the adaptive diversification of pigeons and doves. Proc. R. Soc. Lond. B 280:1471-2954.
58. Lerner, H. R. L., M. Meyer, H. F. Jmes, M. Hofreiter, and R. C. Fleischer . 2011. Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Curr. Biol. 21:1838-1844.
59. Librado, P., and J. Rozas . 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
60. Losos, J. B. 2009. Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press, Berkeley and Los Angeles, CA.
61. Marie Curie SPECIATION network. 2012. What do we need to know about speciation? Trends Ecol. Evol. 27:27-39.
62. Marler, P., and H. Slabbekoorn . 2004. Nature's music: the science of birdsong. Elservier Academic Press, San Diego, CA.
63. Martín, A., and J. A. Lorenzo . 2001. Aves del Archipiélago Canario. Lemus Editor, La Laguna.
64. Mayr, E., and J. M. Diamond . 2001. The birds of Northern Melanesia: speciation, ecology, and biogeography. Oxford Univ. Press, New York.
65. Medina, I., and C. C. Francis . 2012. Environmental variability and acoustic signals: a multi-level approach in songbirds. Biol. Lett. 8:928-931.
66. Melo, M., B. H. Warren, and P. J. Jones . 2011. Rapid parallel evolution of aberrant traits in the diversification of the Gulf of Guinea white-eyes (Aves, Zosteropidae). Mol. Ecol. 20:4953-4967.
67. Milá, B., B. H. Warren, P. Heeb, and C. Thébaud . 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.
68. Monceau, K., F. Cézilly, J. Moreau, S. Motreuil, and R. Wattier . 2013. Colonisation and diversification of the zenaida dove (Zenaida aurita) in the Antilles: phylogeography, contemporary gene flow and morphological divergence. PLoS ONE 8:e82189.
69. Nei, M. 1987. Molecular evolutionary genetics. Columbia Univ. Press, New York.
70. Nicholls, J. A., J. J. Austin, C. Moritz, and A. W. Goldizen . 2006. Genetic population structure and call variation in a passerine bird, the satin bowerbird, Ptilonorhynchus violaceus. Evolution 60:1279-1290.
71. Orsini, L., J. Vanoverbeke, I. Swillen, J. Mergeay, and L. De Meester . 2013. Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Mol. Ecol. 22:5983-5999.
72. Palmero, A. M., J. C. Illera, and P. Laiolo . 2012. Song characterization in the spectacled warbler (Sylvia conspicillata): a circum-Mediterranean species with a complex song structure. Bioacoustics 21:175-191.
73. Palmero, A. M., J. Espelosín, P. Laiolo, and J. C. Illera . 2014. Information theory reveals that individual birds do not change song complexity when varying its length. Anim. Behav. 87:153-163.
74. Papadopulos, A. S. T., W. J. Baker, D. Crayn, R. K. Butlin, I. A. Kynast, and V. Savolainen . 2011. Speciation with gene flow on Lord Howe Island. Proc. Natl. Acad. Sci. USA 108:13188-13193.
75. Parker, K. A., M. J. Anderson, P. F. Jenkins, and D. H. Brunton . 2012. The effects of translocation-induced isolation and fragmentation on the cultural evolution of bird song. Ecol. Lett. 15:778-785.
76. Pérez-Tris, J., and J. L. Tellería . 2001. Age-related variation in wing shape of migratory and sedentary Blackcaps Sylvia atricapilla. J. Avian Biol. 32:207-213.
77. Pérez-Tris, J., S. Bensch, R. Carbonell, A. J. Helbig, and J. L. Telleria . 2004. Historical diversification of migration patterns in a passerine bird. Evolution 58:1819-1832.
78. Pinho, C., and J. Hey . 2010. Divergence with gene flow: models and data. Annu. Rev. Ecol. Syst. 41:215-230.
79. Podos, J. 2010 Acoustic discrimination of sympatric morphs in Darwin's finches: a behavioural mechanism for assortative mating? Philos. Trans. R. Soc. B 365:1031-1039.
80. Podos, J., J. A. Southall, and M. R. Rossi-Santos . 2004. Vocal mechanics in Darwin's finches: correlation of beak gape and song frequency. J. Exp. Biol. 207:607-619.
81. Price, T. 2008. Speciation in birds. Roberts and Company Publishers, Greenwood Village, CO.
82. Pritchard, J. K., M. Stephens, and P. J. Donnelly . 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
83. R Development Core Team. 2010. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.r-project.org/.
84. Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolating by distance. Genetics 145:1219-1228.
85. Sætre, G. P., and S. A. Sæther . 2010. Ecology and genetics of speciation in Ficedula flycatchers. Mol. Ecol. 19:1091-1106.
86. Seddon, N., and J. A. Tobias . 2010. Character displacement from the receiver's perspective: species and mate recognition despite convergent signals in suboscine birds. Evolution 277:2475-2483.
87. Seddon, N., C. A. Botero, J. A. Tobias, P. O. Dunn, H. E. A. MacGregor, D. R. Rubenstein, J. A. C. Uy, J. T. Weir, L. A. Whittingham, and R. J. Safran . 2013. Sexual selection accelerates signal evolution during speciation in birds. Proc. R. Soc. Lond. B 280:20131065.
88. Shuker, D. M., K. Underwood, T. M. King, and R. K. Butlin . 2005. Pattern of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection. Proc. R. Soc. Lond. B 272:2491-2497.
89. Spurgin, L. G., J. C. Illera, T. H. Jorgensen, D. A. Dawson, and D. S. Richardson . 2014. Genetic and phenotypic divergence in an island bird: isolation by distance, by colonisation or by adaptation? Mol. Ecol. 23:1028-1039.
90. Tajima, F. 1996. The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 143:1457-1465.
91. Tellería, J. L., B. Asensio, and M. Díaz . 1999. Aves lbericas II. Paseriformes. Reyero, Madrid.
92. Tietze, D. T., J. Martens, Y. H. Sun, L. Severinghaus, and M. Päckert . 2011. Song evolution in the coal tit Parus ater. J. Avian Biol. 42:214-230.
93. Tobias, J. A., and N. Seddon . 2009. Signal design and perception in Hypocnemis antbirds: evidence of convergent evolution via social selection. Evolution 63:3168-3189.
94. Tobias, J. A., J. Aben, R. T. Brumfield, E. P. Derryberry, W. Halfwerk, H. Slabbekoorn, and N. Seddon . 2010. Song divergence by sensory drive in Amazonian birds. Evolution 64:2820-2839.
95. Toews, D. P. L., and D. E. Irwin . 2008. Cryptic speciation in a Holarctic passerine revealed by genetic and bioacoustic analyses. Mol. Ecol. 17:2691-2705.
96. Trujillo, D. 2007. Curruca Tomillera (Sylvia conspicillata). Pp. 344-347 in J. A. Lorenzo, ed. Atlas de las aves nidificantes en el archipiélago Canario. Dirección General de Conservación de la Naturaleza-Sociedad Española de Ornitología, Organismo Autónomo de Parques Nacionales, Madrid.
97. Turelli, M., N. H. Barton, and J. A. Coyne . 2001. Theory and speciation. Trends Ecol. Evol. 16:330-343.
98. Uy, J. A. C., R. G. Moyle, C. E. Filardi, and Z. A. Cheviron . 2009. Difference in plumage color used in species recognition between incipient species is linked to a single amino acid substitution in the melanocortin-1 receptor. Am. Nat. 174:244-254.
99. Warren, B. H., E. Bermingham, R. P. Prys-Jones, and C. Thebaud . 2005. Tracking island colonization history and phenotypic shifts in Indian Ocean bulbuls (Hypsipetes: Pycnonotidae). Biol. J. Linn. Soc. 85:271-287.
100. Warren, B. H., E. Bermingham, Y. Bourgeois, L. K. Estep, R. P. Prys-Jones, D. Strasberg, and C. Thébaud . 2012. Hybridization and barriers to gene flow in an island bird radiation. Evolution 66:1490-1505.
101. Weir, J. T., D. J. Wheatcroft, and T. D. Price . 2012. The role of ecological constraint in driving the evolution of avian song frequency across a latitudinal gradient. Evolution 66:2773-2783.
102. Wiley, C., A. Qvarnström, G. Andersson, T. Borge, and G.-P. Sætre 2009. Postzygotic isolation over multiple generations of hybrid descendents in a natural hybrid zone: how well do single-generation estimates reflect reproductive isolation? Evolution 63:1731-1739.
103. Wilkins, M. R., N. Seddon, and R. J. Safran 2013. Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol. Evol. 28:156-166.