Population differentiation and restricted gene flow in Spanish crossbills: Not isolation-by-distance but isolation-by-ecology

Journal of Evolutionary Biology

Volumn 25, Issue 3, 2012, Pages 417-430

  Edelaar, P ^a,b   Alonso, D ^c   Lagerveld, S ^d   Senar, J C ^e   Bjorklund M ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^c Aranzadi Sciences Society   (Spain)

^d LEIDEN UNIVERSITY   (Netherlands)

^e Museu de Zoologia   (Spain)

Author keywords

Divergent selection; Ecological speciation; Gene flow; Landscape genetics; Loxia curvirostra; Population divergence; Reproductive isolation; Resource specialization

Indexed keywords

MITOCHONDRIAL DNA;

DIVERGENCE; FUNCTIONAL MORPHOLOGY; GENE FLOW; GENETIC DIFFERENTIATION; LANDSCAPE; LOCAL ADAPTATION; MITOCHONDRIAL DNA; PHENOTYPE; POPULATION STRUCTURE; REPRODUCTIVE ISOLATION; RESOURCE USE; SELECTION; SPECIALIZATION; SPECIATION (BIOLOGY);

ADAPTATION; ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BEAK; DNA SEQUENCE; ECOSYSTEM; GENE FLOW; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; HISTOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYSIOLOGY; POPULATION DYNAMICS; POPULATION GENETICS; SONGBIRD; SPAIN; VOCALIZATION;

ADAPTATION, BIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; BASE SEQUENCE; BEAK; DNA, MITOCHONDRIAL; ECOSYSTEM; GENE FLOW; GENETIC VARIATION; GENETICS, POPULATION; GEOGRAPHY; MOLECULAR SEQUENCE DATA; PASSERIFORMES; PHENOTYPE; POPULATION DYNAMICS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SPAIN; VOCALIZATION, ANIMAL;

SPAIN;

LOXIA; LOXIA CURVIROSTRA;

EID: 84857036858     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02443.x     Document Type: Article

References (87)

1. Alonso, D., Arizaga, J., Miranda, R. & Ángeles Hernández, M. 2006. Morphological diversification of Common Crossbill Loxia curvirostra populations within Iberia and the Balearics. Ardea 94: 99-107.
2. Avise, J.C. 2000. Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, MA.
3. Backström, N., Fagerberg, S. & Ellegren, H. 2008. Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Mol. Ecol. 17: 964-980.
4. Badyaev, A.V., Young, R.L., Oh, K.P. & Addison, C. 2008. Evolution on a local scale: developmental, functional, and genetic bases of divergence in bill form and associated changes in song structure between adjacent habitats. Evolution 62: 1951-1964.
5. Bandelt, H.-J., Forster, P. & Röhl, A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16: 37-48.
6. Barbéro, M., Loisel, R., Quézel, P., Richardson, D.M. & Romane, F. 1998. Pines of the Mediterranean Basin. In: Ecology and Biogeography of Pinus (D.M. Richardson, ed.), pp. 153-170. Cambridge University Press, Cambridge, UK.
7. Benkman, C.W. 1993. Adaptation to single resources and the evolution of crossbill (Loxia) diversity. Ecol. Monogr. 63: 305-325.
8. Benkman, C.W. 2003. Divergent selection causes the adaptive radiation of crossbills. Evolution 57: 1176-1181.
9. Benkman, C.W. & Lindholm, A.K. 1991. The advantages and evolution of a morphological novelty. Nature 349: 519-520.
10. Bolnick, D.I. & Fitzpatrick, B.M. 2007. Sympatric speciation: models and empirical evidence. Ann. Rev. Ecol. Evol. Syst. 38: 459-487.
11. Bonnet, E. & Van de Peer, Y. 2002. Zt: a software tool for simple and partial Mantel tests. J. Stat. Softw. 7: 1-12.
12. Borrás, A. & Senar, J.C. 2003. Piquituerto común Loxia curvirostra. In: Atlas de las Aves Reproductoras de España (R. Martí & J.C. Del Moral, eds), pp. 588-589. Dirección General de Conservación de la Naturaleza and Sociedad Española de Ornitología, Madrid, Spain.
13. Borrás, A., Cabrera, A. & Cabrera, J. 1996. Crossbills Loxia curvirostra feeding on cypress seeds. Butll. GCA 13: 53-55.
14. Borrás, A., Cabrera, J. & Senar, J.C. 2008. Local divergence between mediterranean crossbills occurring in two different species of pine. Ardeola 55: 169-177.
15. Borrás, A., Senar, J.C., Cabrera, J., Colomé, X. & Cabrera, T. 2011. Trencapinyes (Loxia curvirostra). In: Atles dels Ocells de Catalunya a l'Hivern 2006-2009 (S. Herrando, L. Brotons, J. Estrada, S. Guallar & M. Anton, eds), pp. 532-533. ICO/Lynx Edicions, Barcelona, Spain. In press.
16. Clouet, M. 2000. The breeding biology of the common Crossbill Loxia curvirostra in the Central Pyrenees. Bird Study 47: 186-194.
17. Clouet, M. 2003. Talle du bec et période de reproduction chez les beccroisés de forêts de pins. Rev. Écol. Terre Vie 58: 419-433.
18. Clouet, M. & Joachim, J. 2008. Sélection des cônes de pins à crochets Pinus uncinata par les beccroisés des sapins Loxia curvirostra dans les Pyrénées. Alauda 76: 223-230.
19. Coyne, J.A. & Orr, H.A. 2004. Speciation. Sinauer and Associates, Sunderland, MA.
20. Cramp, S. & Perrins, C.M. 1994. The Birds of the Western Palearctic. Vol. VIII - Crows to Finches. Oxford University Press, Oxford, UK.
21. De Leon, L.F., Bermingham, E., Podos, J. & Hendry, A.P. 2010. Divergence with gene flow as fascilitated by ecological differences: within-island variation in Darwin's finches. Phil. Trans. R. Soc. B 365: 1041-1052.
22. Dres, M. & Mallet, J. 2002. Host races in plant-feeding insects and their importance in sympatric speciation. Phil. Trans. R. Soc. Lond. B 357: 471-492.
23. Edelaar, P. 2008a. Assortative mating also indicates that common crossbill Loxia curvirostra vocal types are species. J. Avian Biol. 39: 9-12.
24. Edelaar, P. 2008b. Rediscovery of a second kind of crossbill for The Himalayan region, and the hypothesis that ecological opportunity drives crossbill diversification. Ibis 150: 405-408.
25. Edelaar, P. & Björklund, M. 2011. If Fst does not measure neutral genetic differentiation, then comparing it with Qst is misleading. Or is it? Mol. Ecol. 20: 1805-1812.
26. Edelaar, P. & Van Eerde, K. 2010. Non-random infection across individuals and populations supports that parasites can change morphology within an adaptive radiation. J. Zool. 283: 135-142.
27. Edelaar, P., Summers, R. & Iovchenko, N. 2003. The ecology and evolution of crossbills Loxia spp: the need for a fresh look and an international research program. Avian Sci. 3: 85-93.
28. Edelaar, P., Siepielski, A.M. & Clobert, J. 2008. Perspective: matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology. Evolution 62: 2462-2472.
29. Edelaar, P., Burraco, P. & Gomez-Mestre, I. 2011. Comparisons between Qst and Fst - how wrong have we been? Molecular Ecology 20: 4830-4839.
30. Evans, K.L., Gaston, K.J., Frantz, A.C., Simeoni, M., Sharp, S.P., McGowan, A. et al. 2009. Independent colonization of multiple urban centres by a formerly forest specialist bird species. Proc. R. Soc. B Biol. Sci. 276: 2403-2410.
31. Excoffier, L. & Slatkin, M. 1995. Maximum-likelihood estimation of molecular haplotype frequencies in a diploid population. Mol. Biol. Evol. 12: 921-927.
32. Excoffier, L., Laval, G. & Schneider, S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1: 47-50.
33. Farjon, A. 2005. Pines. Drawings and Descriptions of the Genus Pinus. Brill, Leiden, The Netherlands.
34. Gavrilets, S. 2004. Fitness Landscapes and the Origin of Species. Princeton University Press, Princeton, NJ.
35. Génard, M. & Lescourret, F. 1987. The common crossbill Loxia curvirostra in the Pyrenees: some observations on its habitats and on its relations with conifer seeds. Bird Study 34: 52-63.
36. Gómez, A., Vendramin, G.G., González-Martínez, S.C. & Alía, R. 2005. Genetic diversity and differentiation of two Mediterranean pines (Pinus halepensis Mill. and Pinus pinaster Ait.) along a latitudinal cline using chloroplast microsatellite markers. Div. Distr. 11: 257-263.
37. Grapputo, A., Pilastro, A. & Marin, G. 1998. Genetic variation and bill size dimorphism in a passerine bird, the reed bunting Emberiza schoeniclus. Mol. Ecol. 7: 1173-1182.
38. Grivet, D., Sebastiani, F., González-Martínez, S.C. & Vendramin, G.G. 2009. Patterns of polymorphism resulting from long-range colonization in the Mediterranean conifer Aleppo pine. New Phytol. 184: 1016-1028.
39. Groth, J.G. 1993a. Evolutionary Differentiation in Morphology, Vocalisations, and Allozymes among Nomadic Sibling Species in the North American Red Crossbill (Loxia curvirostra) Complex. University of California Publications in Zoology 127. Berkeley, CA, USA.
40. Groth, J.G. 1993b. Call matching and positive assortative mating in red crossbills. Auk 110: 398-401.
41. Hall, T.A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuclic Acids Symp. Ser. 41: 95-98.
42. Hendry, A.P., Day, T. & Taylor, E.B. 2001. Population mixing and the adaptive divergence of quantitative traits in discrete populations: a theoretical framework for empirical tests. Evolution 55: 459-466.
43. Jensen, J.L., Bohonak, A.J. & Kelley, S.T. 2005. Isolation by distance, web service. BMC Genet. 6: 13.
44. Jost, L. 2008. Gst and its relatives do not measure differentiation. Mol. Ecol. 17: 4015-4026.
45. Keenan, P.C. & Benkman, C.W. 2008. Call imitation and call modification in Red Crossbills. Condor 110: 93-101.
46. Kronholm, I., Loudet, O. & De Meaux, J. 2010. Influence of mutation rate on estimators of genetic differentiation - lessons from Arabidopsis thaliana. BMC Genet. 11: 33.
47. Maniatis, T., Fritsch, E.F. & Sambrook, J. 1982. Molecular Cloning, a Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
48. Marquiss, M., Hobson, K.A. & Newton, I. 2008. Stable isotope evidence for different regional source areas of common crossbill Loxia curvirostra irruptions into Britain. J. Avian Biol. 39: 30-34.
49. Massa, B. 1987. Variations in Mediterranean crossbills Loxia curvirostra. Bull. Brit. Ornithol. Club 107: 118-129.
50. Meirmans, P.G. 2006. Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60: 2399-2402.
51. Mezquida, E.T. & Benkman, C.W. 2005. The geographic selection mosaic for squirrels, crossbills and Aleppo pine. J. Evol. Biol. 18: 348-357.
52. Mezquida, E.T. & Benkman, C.W. 2010. Habitat area and structure affect the impact of seed predators and the potential for coevolutionary arms races. Ecology 91: 802-814.
53. Newton, I. 2006. Movement patterns of common crossbills Loxia curvirostra in Europe. Ibis 148: 782-788.
54. Nosil, P. 2008. Speciation with gene flow could be common. Mol. Ecol. 17: 2103-2106.
55. Nosil, P., Egan, S.P. & Funk, D.J. 2008. Heterogeneous genomic differentiation between walking-stick ecotypes: 'isolation-by-adaptation' and multiple roles for divergent selection. Evolution 62: 316-336.
56. Nosil, P., Funk, D.J. & Ortiz-Barrientos, D. 2009. Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18: 375-402.
57. Orr, M.R. & Smith, T.B. 1998. Ecology and speciation. Trends Ecol. Evol. 13: 502-506.
58. Parchman, T.L., Benkman, C.W. & Britch, S.C. 2006. Patterns of genetic variation in the adaptive radiation of New World crossbills (Aves: Loxia). Mol. Ecol. 15: 1873-1887.
59. Piertney, S.B., Summers, R. & Marquiss, M. 2001. Mitochondrial and microsatellite DNA homogeneity among phenotypically diverse crossbill taxa in the UK. Proc. R. Soc. Lond. B 268: 1511-1516.
60. Questiau, S., Gielly, L., Clouet, M. & Taberlet, P. 1999. Phylogeographical evidence of gene flow among common crossbill (Loxia curvirostra, Aves, Fringillidae) populations at the continental level. Heredity 83: 196-205.
61. Räsänen, K. & Hendry, A.P. 2008. Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification. Ecol. Lett. 11: 624-636.
62. Raymond, M. & Rousset, F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Heredity 86: 248-249.
63. Rolshausen, G., Segelbacher, G., Hobson, K. & Schaefer, H.M. 2009. Contemporary evolution of reproductive isolation and phenotypic divergence in sympatry along a migratory divide. Curr. Biol. 19: 2097-2101.
64. Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219-1228.
65. Rousset, F. 2008. Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Res. 8: 103-106.
66. Rubiales, J.M., García-Amorena, I., Hernández, L., Génova, M., Martínez, F., Gómez Manzaneque, F. et al. 2010. Late Quaternary dynamics of pinewoods in the Iberian Mountains. Rev. Palaeobot. Palynol. 162: 476-491.
67. Rundle, H. & Nosil, P. 2005. Ecological speciation. Ecol. Lett. 8: 336-352.
68. Ryan, P.G., Bloomer, P., Moloney, C.L., Grant, T.J. & Delport, W. 2007. Ecological speciation in South Atlantic Island finches. Science 315: 1420-1423.
69. Schluter, D. 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford, UK.
70. Senar, J.C., Borrás, A., Cabrera, T. & Cabrera, J. 1993. Testing for the relationship between coniferous crop stability and Common Crosbill residence. J. Field Ornithol. 64: 464-469.
71. Senar, J.C., Borrás, A., Cabrera, A., Cabrera, J. & Björklund, M. 2006. Local differentiation in the presence of gene flow in the citril finch Serinus citronella. Biol. Lett. 2: 85-87.
72. Sewall, K.B. 2009. Limited adult vocal learning maintains call dialects but permits pair-distinctive calls in red crossbills. Anim. Behav. 77: 1303-1311.
73. Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236: 787-792.
74. Smith, J.W. & Benkman, C.W. 2007. A coevolutionary arms race causes ecological speciation in crossbills. Am. Nat. 169: 455-465.
75. Smith, L.M. & Burgoyne, L.A. 2004. Collecting, archiving and processing DNA from wildlife samples using FTA databasing paper. BMC Ecol. 4: 4.
76. Snowberg, L.K. & Benkman, C.W. 2007. The role of marker traits in the assortative mating within red crossbills, Loxia curvirostra complex. J. Evol. Biol. 20: 1924-1932.
77. Snowberg, L.K. & Benkman, C.W. 2009. Mate choice based on a key ecological performance trait. J. Evol. Biol. 22: 762-769.
78. Soto, A., Robledo-Arnuncio, J.J., González-Martínez, S.C., Smouse, P.E. & Alía, R. 2010. Climatic niche and neutral genetic diversity of the six Iberian pine species: a retrospective and prospective view. Mol. Ecol. 19: 1396-1409.
79. Summers, R.W., Dawson, R.J.G. & Phillips, R.E. 2007. Assortative mating and patterns of inheritance indicate that the three crossbill taxa in Scotland are species. J. Avian Biol. 38: 153-162.
80. Svensson, L. 1992. Identification Guide to European Passerines. Svensson, Stockholm, Sweden.
81. Tar, C.L. 1995. Primers for amplification and determination of mitochondrial control region in oscine passerines. Mol. Ecol. 4: 527-552.
82. Tellería, J.L., Asensio, B. & Díaz, M. 1999. Aves Ibéricas II. Passeriformes. J.M. Reyero, Madrid, Spain.
83. Thibert-Plante, X. & Hendry, A.P. 2010. When can ecological speciation be detected with neutral loci? Mol. Ecol. 19: 2301-2314.
84. Van Doorn, G.S., Edelaar, P. & Weissing, F.J. 2009. On the origin of species by natural and sexual selection. Science 326: 1704-1707.
85. Weissing, F.J., Van Doorn, G.J. & Edelaar, P. 2011. Adaptive speciation theory: a conceptual review. Behav. Ecol. Sociobiol. 65: 461-480.
86. Whitlock, M.C. 2005. Combining probability from independent tests: the weighted Z-method is superior to Fisher's approach. J. Evol. Biol. 18: 1368-1373.
87. Whitlock, M.C. 2011. G′st and D do not replace Fst. Mol. Ecol. 20: 1083-1091.