Comparing clines on molecular and phenotypic traits in hybrid zones: A window on tension zone models

Evolution

Volumn 62, Issue 11, 2008, Pages 2789-2806

  Gay, Laurène ^a   Crochet, Pierre André ^a   Bell, Douglas A ^b   Lenormand, Thomas ^a  

^a CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^b CALIFORNIA ACADEMY OF SCIENCES   (United States)

Author keywords

Cline; Larus; Moving hybrid zone; Quantitative trait; Tension zone theory

Indexed keywords

DNA; MICROSATELLITE DNA; MITOCHONDRIAL DNA;

CLINE; COMPARATIVE STUDY; DISPERSAL; GENETIC MARKER; HYBRID ZONE; INTROGRESSION; MITOCHONDRIAL DNA; NATURAL SELECTION; PHENOTYPIC PLASTICITY; REPRODUCTIVE ISOLATION; SEABIRD;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CHARADRIIFORMES; CLASSIFICATION; CLIMATE; COLOR; DECISION MAKING; FEATHER; FEMALE; GENE LINKAGE DISEQUILIBRIUM; GENETIC MARKER; GENETICS; MALE; PHENOTYPE; POPULATION DENSITY; REPRODUCTION; SEXUAL BEHAVIOR;

ANIMALS; CHARADRIIFORMES; CHOICE BEHAVIOR; CLIMATE; COLOR; DNA; DNA, MITOCHONDRIAL; FEATHERS; FEMALE; GENETIC MARKERS; LINKAGE DISEQUILIBRIUM; MALE; MICROSATELLITE REPEATS; MODELS, GENETIC; PHENOTYPE; POPULATION DENSITY; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL;

LARUS; LARUS GLAUCESCENS; LARUS OCCIDENTALIS;

EID: 54849418431     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00491.x     Document Type: Article

References (97)

1. Akaike, H. 1973. Information theory and an extension of the maximum likelihood principle. International symposium on information theory, Akadémiai Kiadi, Budapest, Hungary. 267 281.
2. Alexandrino, J., S. J. E. Baird, L. Lawson, J. R. Macey, C. Moritz, and D. B. Wake. 2005. Strong selection against hybrids at a hybrid zone in the Ensatina ring species complex and its evolutionary implications. Evolution 59 : 1334 1347.
3. AOU. 1998. Check list of North American Birds. 7th ed. American Ornithologists' Union, Washington, DC.
4. Arnold, M. L. 1992. Natural hybridization as an evolutionary process. Annu. Rev. Ecol. Syst. 23 : 237 261.
5. Arnold, M. L. 1992. On the spread of new gene combinations in the 3rd phase of Wright shifting-balance. Evolution 46 : 551 557.
6. Arnold, M. L. 2000. Estimating multilocus linkage disequilibria. Heredity 84 : 373 389.
7. Barton, N. H., and K. S. Gale. 1993. Genetic analysis of hybrid zones. Pp. 13 45 in R. G. Harrison, ed. Hybrid zones and the evolutionary process. Oxford Univ. Press, Oxford, UK.
8. Barton, N. H., and G. M. Hewitt. 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16 : 113 148.
9. Barton, N. H., and G. M. Hewitt. 1989. Adaptation, speciation and hybrid zones. Nature 341 : 497 503.
10. Belkhir, K., P. Borsa, J. Goudet, L. Chikhi, and F. Bonhomme. 1998. GENETIX, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome et Populations, CNRS UPR 9060, Université de Montpellier II, Montpellier, France.
11. Bell, D. A. 1996. Genetic differentiation, geographic variation and hybridization in gulls of the Larus-glaucescens-occidentalis complex. Condor 98 : 527 546.
12. Bell, D. A. 1997. Hybridization and reproductive performance in gulls of the Larus glaucescens-occidentalis complex. Condor 99 : 585 594.
13. Bierne, N., P. Borsa, C. Daguin, D. Jollivet, F. Viard, F. Bonhomme, and P. David. 2003. Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M-galloprovincialis. Mol. Ecol. 12 : 447 461.
14. Blum, M. J. 2002. Rapid movement of a Heliconius hybrid zone: evidence for phase III of Wright's shifting balance theory Evolution 56 : 1992 1998.
15. Bozikova, E., P. Munclinger, K. C. Teeter, P. K. Tucker, M. Macholan, and J. Pialek. 2005. Mitochondrial DNA in the hybrid zone between Mus musculus musculus and Mus musculus domesticus: a comparison of two transects. Biol. J. Linn. Soc. 84 : 363 378.
16. Bridle, J. R., and R. K. Butlin. 2002. Mating signal variation and bimodality in a mosaic hybrid zone between Chorthippus grasshopper species. Evolution 56 : 1184 1198.
17. Bridle, J. R., S. J. E. Baird, and R. K. Butlin. 2001. Spatial structure and habitat variation in a grasshopper hybrid zone. Evolution 55 : 1832 1843.
18. Bridle, J. R., C. I. Saldamando, W. Koning, and R. K. Butlin. 2006. Assortative preferences and discrimination by females against hybrid male song in the grasshoppers Chorthippus brunneus and Chorthippus jacobsi (Orthoptera: Acrididae). J. Evol. Biol. 19 : 1248 1256.
19. Britch, S. C., M. L. Cain, and D. J. Howard. 2001. Spatio-temporal dynamics of the Allonemobius fasciatus-A. socius mosaic hybrid zone: a 14-year perspective. Mol. Ecol. 10 : 627 638.
20. Bronson, C. L., T. C. Grubb, G. D. Sattler, and M. J. Braun. 2003. Mate preference: a possible causal mechanism for a moving hybrid zone. Anim. Behav. 65 : 489 500.
21. Brumfield, R. T., R. W. Jernigan, D. B. McDonald, and M. J. Braun. 2001. Evolutionary implications of divergent clines in an avian (Manacus: Aves) hybrid zone. Evolution 55 : 2070 2087.
22. Buggs, R. J. A. 2007. Empirical study of hybrid zone movement. Heredity 99 : 301 312.
23. Buggs, R. J. A., and J. R. Pannell. 2006. Rapid displacement of a monoecious plant lineage is due to pollen swamping by a dioecious relative. Curr. Biol. 16 : 996 1000.
24. Carney, S. E., K. A. Gardner, and L. H. Rieseberg. 2000. Evolutionary changes over the fifty-year history of a hybrid population of sunflowers (Heliantus). Evolution 54 : 462 474.
25. Coulson, J. C. 1991. The population dynamics of culling herring gulls and lesser black-backed gulls. Pp. 479 497 in C. M. Perrins, J. D. Lebreton and G. J. M. Hirons, eds. Bird population studies. Oxford Univ. Press, Oxford.
26. Coyne, J. A., N. H. Barton, and M. Turelli. 2000. Is Wright's shifting balance process important in evolution Evolution 54 : 306 317
27. Cramps, S., and K. E. L. Simmons. 1983. Handbook of the birds of Europe the Middle East and North Africa. The birds of the Western Palearctic. Oxford Univ. Press, Oxford, UK.
28. Crochet, P. A. 1996. Can measures of gene flow help to evaluate bird dispersal Acta Oecologica 17 : 459 474.
29. Crochet, P. A., J. D. Lebreton, and F. Bonhomme. 2002. Systematics of large white-headed gulls: patterns of mitochondrial DNA variation in western European taxa. Auk 119 : 603 620.
30. Crochet, P. A., J. J. Z. Chen, J. M. Pons, J. D. Lebreton, P. D. N. Hebert, and F. Bonhomme. 2003. Genetic differentiation at nuclear and mitochondrial loci among large white-headed gulls: sex-biased interspecific gene flow Evolution 57 : 2865 2878.
31. Daguin, C., F. Bonhomme, and P. Borsa. 2001. The zone of sympatry and hybridization of Mytilus edulis and M. galloprovincialis, as described by intron length polymorphism at locus mac-1. Heredity 86 : 342 354.
32. Dasmahapatra, K. K., M. J. Blum, A. Aiello, S. Hackwell, N. Davies, E. P. Bermingham, and T. Mallett. 2002. Inferences from a rapidly moving hybrid zone. Evolution 56 : 741 753.
33. Dawson, W. L. 1908. The bird colonies of the Olympiads. Auk 25 : 153 163.
34. Dod, B., L. S. Jermiin, P. Boursot, V. H. Chapman, J. T. Nielsen, and F. Bonhomme. 1993. Counterselection on sex-chromosomes in the Mus musculus European hybrid zone. J. Evol. Biol. 6 : 529 546.
35. Endler, J. A. 1977. Geographic variation, speciation and clines. Princeton Univ. Press, Princeton, NJ.
36. Gay, L., D. A. Bell, and P. A. Crochet. 2005. Additional data on mitochondrial DNA of North American large gull taxa. Auk 122 : 684 688.
37. Gay, L., G. Neubauer, M. Zagalska-Neubauer, C. Debain, J. M. Pons, P. David, and P. A. Crochet. 2007. Molecular and morphological patterns of introgression between two large white-headed gull species in a zone of recent secondary contact. Mol. Ecol. 16 : 3215 3227.
38. Good, T. P. 2002. Breeding success in the western gull × glaucous-winged gull complex: the influence of habitat and nest site characteristics. Condor 104 : 353 365.
39. Good, T. P., J. C. Ellis, C. A. Annett, and R. Pierotti. 2000. Bounded hybrid superiority in an avian hybrid zone: effects of mate, diet, and habitat choice. Evolution 54 : 1774 1783.
40. Goodisman, M. A. D., D. D. Shoemaker, and M. A. Asmussen. 1998. Cytonuclear theory for haplodiploid species and X-linked genes. II. Stepping-stone models of gene flow and application to a fire ant hybrid zone. Evolution 52 : 1423 1440.
41. Goodman, S. J., N. H. Barton, G. Swanson, K. Abernethy, and J. M. Pemberton. 1999. Introgression through rare hybridization: a genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland. Genetics 152 : 355 371.
42. Grahame, J. W., C. S. Wilding, and R. K. Butlin. 2006. Adaptation to a steep environmental gradient and an associated barrier to gene exchange in Littorina saxatilis. Evolution 60 : 268 278.
43. Hafner, M. S., J. W. Demastes, D. J. Hafner, T. A. Spradling, P. D. Sudman, and S. A. Nadler. 1998. Age and movement of a hybrid zone: implications for dispersal distance in pocket gophers and their chewing lice. Evolution 52 : 278 282.
44. Hare, M. P., and J. C. Avise. 1996. Molecular genetic analysis of a stepped multilocus cline in the American oyster (Crassostrea virginica). Evolution 50 : 2305 2315.
45. Hoffman, W., J. A. Wiens, and J. M. Scott. 1978. Hybridization between gulls (Larus glaucescens and L. occidentalis) in Pacific Northwest. Auk 95 : 441 458.
46. Jiggins, C. D., and J. Mallet. 2000. Bimodal hybrid zones and speciation. Trends Ecol. Evol. 15 : 250 255.
47. Jones, J. S., S. H. Bryant, R. C. Lewontin, J. A. Moore, and T. Prout. 1981. Gene flow and the geographical distribution of a molecular polymorphism in Drosophila pseudoobscura. Genetics 98 : 157 178.
48. Klingenberg, C. P., J. R. Spence, and C. K. Mirth. 2000. Introgressive hybridization between two species of waterstriders (Hemiptera: Gerridae: Limnoporus): geographical structure and temporal change of a hybrid zone. J. Evol. Biol. 13 : 756 765.
49. Kohlmann, B., and D. Shaw. 1991. The effect of a partial barrier on the movement of a hybrid zone. Evolution 45 : 1606 1617.
50. Kondrashov, A. S. 1992. The 3rd phase of Wright shifting - balance - a simple analysis of the extreme case. Evolution 46 : 1972 1975.
51. Kristiansen, K. O., J. O. Bustnes, I. Folstad, and M. Helberg. 2006. Carotenoid coloration in great black-backed gull Larus marinus reflects individual quality. J. Avian Biol. 37 : 6 12.
52. Kruuk, L. E. B., S. J. E. Baird, K. S. Gale, and N. H. Barton. 1999. A comparison of multilocus clines maintained by environmental adaptation or by selection against hybrids. Genetics 153 : 1959 1971.
53. Leache, A. D., and C. J. Cole. 2007. Hybridization between multiple fence lizard lineages in an ecotone: locally discordant variation in mitochondrial DNA, chromosomes, and morphology. Mol. Ecol. 16 : 1035 1054.
54. Lebreton, J. D., K. P. Burnham, J. Clobert, and D. R. Anderson. 1992. Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol. Monogr. 62 : 67 118.
55. MacCallum, C. J., B. Nurnberger, N. H. Barton, and J. M. Szymura. 1998. Habitat preference in the Bombina hybrid zone in Croatia. Evolution 52 : 227 239.
56. Majerus, M. E. N., and N. I. Mundy. 2003. Mammalian melanism: natural selection in black and white. Trends Genet. 19 : 585 588.
57. Mallet, J., N. Barton, L. M. Gerardo, S. C. Jose, M. M. Manuel, and H. Eeley. 1990. Estimates of selection and gene flow from measures of cline width and linkage disequilibrium in Heliconius hybrid zones. Genetics 124 : 921 936.
58. Marshall, J. C., and J. W. Sites. 2001. A comparison of nuclear and mitochondrial cline shapes in a hybrid zone in the Sceloporus grammicus complex (Squamata: Phrynosomatidae). Mol. Ecol. 10 : 435 449.
59. McDonnell, L. J., D. F. Gartside, and M. J. Littlejohn. 1978. Analysis of a narrow hybrid zone between two species of Pseudophryne (Anura- Leptodactylidae) in southeastern Australia. Evolution 32 : 602 612.
60. Migot, P. 1992. Demographic changes in French herring gull Larus argentatus populations - a modeling approach and hypotheses concerning the regulation of numbers. Ardea 80 : 161 169.
61. Moore, W. S., and D. B. Buchanan. 1985. Stability of the northern flicker hybrid zone in historical times - implications for adaptive speciation theory. Evolution 39 : 135 151.
62. Moore, W. S., and R. A. Dolbeer. 1989. The use of banding recovery data to estimate dispersal rates and gene flow in avian species - case studies in the red-winged blackbird and common grackle. Condor 91 : 242 253.
63. Munsell. 1968. Dominant wavelength and excitation purity for designated Munsell color notations. Munsell Color Co., Macbeth Kollmorgen, Baltimore, MD.
64. Munsell. 1971. Munsell neutral value scale. Glossy. 37-step scale. Munsell Color Co., Macbeth Kollmorgen, Baltimore, MD.
65. Munsell. 1976. Munsell book of color. Munsell Color Co., Macbeth Kollmorgen, Baltimore, MD.
66. Nagylaki, T. 1993. The evolution of multilocus systems under weak selection. Genetics 134 : 627 647.
67. Nürnberger, B., N. Barton, C. MacCallum, J. Gilchrist, and M. Appleby. 1995. Natural selection on quantitative traits in the Bombina hybrid zone. Evolution 49 : 1224 1238.
68. Oro, D., and R. Pradel. 1999. Recruitment of Audouin's gull to the Ebro Delta colony at metapopulation level in the western Mediterranean. Marine Ecol. 180 : 267 273.
69. Parsons, T. J., S. L. Olson, and M. J. Braun. 1993. Unidirectional spread of secondary sexual plumage traits across an avian hybrid zone. Science 260 : 1643 1646.
70. Pearse, T. 1946. Nesting of the western gull off the coast of Vancouver Island, British Columbia, and possible hybridization with the glaucous-winged gull. Murrelet 27 : 39 40.
71. Perry, W. L., J. L. Feder, G. Dwyer, and D. M. Lodge. 2001. Hybrid zone dynamics and species replacement between Orconectes crayfishes in a northern Wisconsin lake. Evolution 55 : 1153 1166.
72. Phillips, B. L., S. J. E. Baird, and C. Moritz. 2004. When vicars meet: a narrow contact zone between morphologically cryptic phylogeographic lineages of the rainforest skink, Carlia rubrigularis. Evolution 58 : 1536 1548.
73. Pierotti, R. 1987. Isolating mechanisms in seabirds. Evolution 41 : 559 570.
74. Porter, A. H., R. Wenger, H. Geiger, A. Scholl, and A. M. Shapiro. 1997. The Pontia daplidice-edusa hybrid zone in northwestern Italy. Evolution 51 : 1561 1573.
75. Raufaste, N., A. Orth, K. Belkhir, D. Senet, C. Smadja, S. J. E. Baird, F. Bonhomme, B. Dod, and P. Boursot. 2005. Inferences of selection and migration in the Danish house mouse hybrid zone. Biol. J. Linn. Soc. 84 : 593 616.
76. Rohwer, S., E. Bermingham, and C. Wood. 2001. Plumage and mitochondrial DNA haplotype variation across a moving hybrid zone. Evolution 55 : 405 422.
77. Rouhani, S., and N. Barton. 1987. Speciation and the shifting balance in a continuous population. Theor. Popul. Biol. 31 : 465 492.
78. Rousset, F. 2004. Genetic structure and selection in subdivided populations. Monographs in Population Biology, Princeton Univ. Press, Princeton, NJ.
79. Sanderson, N., J. M. Szymura, and N. H. Barton. 1992. Variation in mating call across the hybrid zone between the fire-bellied toads Bombina bombina and B. variegata. Evolution 46 : 595 607.
80. Scott, J. M. 1971. Interbreeding of the glaucous-winged gull and western gull in the Pacific northwest. Californian Birds 2 : 129 133.
81. Sequeira, F., J. Alexandrino, S. Rocha, J. W. Arntzen, and N. Ferrand. 2005. Genetic exchange across a hybrid zone within the Iberian endemic golden-striped salamander, Chioglossa lusitanica. Mol. Ecol. 14 : 245 254.
82. Slatkin, M. 1973. Gene flow and selection in a cline. Genetics 75 : 733 756.
83. Sotka, E. E., and S. R. Palumbi. 2006. The use of genetic clines to estimate dispersal distances of marine larvae. Ecology 87 : 1094 1103.
84. Steinmetz, R., J. Johannesen, and A. Seitz. 2004. Clinal genetic variation and the 'rare allele phenomenon' in random mating populations of Urophora cardui (Diptera: Tephritidae). Genetica 122 : 277 290.
85. Szymura, J., and N. Barton. 1986. Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and Bombina variegata, near Cracow in southern Poland. Evolution 40 : 1141 1159.
86. Szymura, J., and N. Barton. 1991. The genetic structure of the hybrid zone between the fire-bellied toads Bombina bombina and B. variegata - Comparisons between transects and between loci. Evolution 45 : 237 261.
87. Takami, Y., and H. Suzuki. 2005. Morphological, genetic and behavioural analyses of a hybrid zone between the ground beetles Carabus lewisianus and C. albrechti (Coleoptera, Carabidae): asymmetrical introgression caused by movement of the zone Biol. J. Linn. Soc. 86 : 79 94.
88. Theron, E., K. Hawkins, E. Bermingham, R. E. Ricklefs, and N. I. Mundy. 2001. The molecular basis of an avian plumage polymorphism in the wild: a melanocortin-1-receptor point mutation is perfectly associated with the melanic plumage morph of the bananaquit, Coereba flaveola. Curr. Biol. 11 : 550 557.
89. Thioulouse, J., D. Chessel, S. Dolédec, and J. M. Olivier. 1997. ADE-4: a multivariate analysis and graphical display software. Statistics and Computing 7 : 75 83.
90. Tirard, C., F. Helfenstein, and E. Danchin. 2002. Polymorphic microsatellites in the black-legged kittiwake Rissa tridactyla. Mol. Ecol. Notes 2 : 431 433.
91. Urbanelli, S., F. Silvestrini, W. K. Reisen, E. DeVito, and L. Bullini. 1997. Californian hybrid zone between Culex pipiens pipiens and C. p. quinquefasciatus revisited (Diptera: Culicidae). J. Med. Entomol. 34 : 116 127.
92. Walsh, P. S., D. A. Metzger, and R. Higuchi. 1991. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10 : 506 513.
93. Weber, J. W. 1981. The Larus gulls of the Pacific northwest's interior, with taxonomic comments on several forms (Part II - conclusions). Continental Birdlife 2 : 74 91.
94. Weir, B. S., and C. C. Cockerham. 1984. Estimating F-Statistics fo the analysis of population structure. Evolution 38 : 1358 70.
95. Woodruff, D. S., and S. J. Gould. 1987. 50 years of interspecific hybridization - genetics and morphometrics of a controlled experiment on the land snail cerion in the Florida keys. Evolution 41 : 1022 1045.
96. Wright, S. 1982. The shifting balance theory and macroevolution. Annu. Rev. Genet. 16 : 1 19.
97. Yanchukov, A., S. Hofman, J. M. Szymura, and S. V. Mezhzherin. 2006. Hybridization of Bombina bombina and B-variegata (Anura, Discoglossidae) at a sharp ecotone in western Ukraine: comparisons across transects and over time. Evolution 60 : 583 600.