Selection and genomic differentiation during ecological speciation: Isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles

Evolution

Volumn 62, Issue 5, 2008, Pages 1162-1181

  Egan, Scott P ^a   Nosil, Patrik ^b   Funk, Daniel J ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

AFLPs; Divergent natural selection; Herbivorous insects; Population divergence; Reproductive isolation; Speciation genetics

Indexed keywords

ADAPTATION; BEETLE; GENETIC DIFFERENTIATION; GENETICS; GENOME; GENOMICS; HOST SPECIFICITY; NATURAL SELECTION; POPULATION GENETICS; REPRODUCTIVE ISOLATION; SPECIATION (BIOLOGY);

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANIMAL; ARTICLE; BEETLE; CLASSIFICATION; ECOSYSTEM; GENE LINKAGE DISEQUILIBRIUM; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GENOME; GENOTYPE; HOST PARASITE INTERACTION; PARASITOLOGY; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION; TREE;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; ANIMALS; BEETLES; ECOSYSTEM; GENETIC SPECIATION; GENOME, INSECT; GENOTYPE; HOST-PARASITE INTERACTIONS; LINKAGE DISEQUILIBRIUM; SELECTION (GENETICS); SPECIES SPECIFICITY; TREES; VARIATION (GENETICS);

ACER; CHRYSOMELIDAE; COLEOPTERA; HEXAPODA; NEOCHLAMISUS BEBBIANAE; SALIX;

EID: 43049109197     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00352.x     Document Type: Article

References (109)

1. Achere, V., J. M. Favre, G. Besnard, and S. Jeandroz. 2005. Genomic organization of molecular differentiation in Norway spruce (Picea abies). Mol. Ecol. 14 : 3191 3201.
2. Balloux, F., and N. Lugon-Moulin. 2002. The estimation of population differentiation with microsatellite markers. Mol. Ecol. 11 : 155 165.
3. Beaumont, M. A., and R. A. Nichols. 1996. Evaluating loci for use in the genetic analysis of population structure. Proc. R. Soc. Lond. B 263 : 1619 1626.
4. ST tell us? Trends Ecol. Evol. 20 : 435 440.
5. Beaumont, M. A., and D. J. Balding. 2004. Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 13 : 969 980.
6. Berlocher, S. H., and J. L. Feder. 2002. Sympatric speciation in phytophagous insects: moving beyond controversy? Annu. Rev. Entomol. 47 : 773 815.
7. Bernays, E. A., and R. F. Chapman. 1994. Host-plant selection by phytophagous insects. Chapman & Hall, New York.
8. Black, W. C., C. F. Baer, M. F. Antolin, and N. M. DuTeau. 2001. Population genomics: genome-wide sampling of insect populations. Annu. Rev. Entomol. 46 : 441 469.
9. Bonin, A., E. Bellemain, P. B. Eidesen, F. Pompanon, C. Brochmann, and P. Taberlet. 2004. How to track and assess genotyping errors in population genetics studies. Mol. Ecol. 13 : 3261 3273.
10. Bonin, A., P. Taberlet, C. Miaud, and F. Pompanon. 2006. Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Mol. Biol. Evol. 23 : 773 783.
11. Bonin, A., D. Ehrich, and S. Manel. 2007. Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Mol. Ecol. 16 : 3737 3758.
12. Boughman, J. W. 2001. Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411 : 944 948.
13. Bradshaw, H. D., and D. W. Schemske. 2003. Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426 : 176 178.
14. Burke, J. M., S. J. Knapp, and L. H. Rieseberg. 2005. Genetic consequences of selection during the evolution of cultivated sunflower. Genetics 171 : 1933 1940.
15. Campbell, D., and L. Bernatchez. 2004. Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol. Biol. Evol. 21 : 945 956.
16. Colosimo, P. F., K. E. Hosemann, S. Balabhadra, G. Villarreal, M. Dickson, J. Grimwood, J. Schmutz, R. M. Myers, D. Schluter, and D. M. Kingsley. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307 : 1928 1933.
17. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer Associates, Sunderland, MA.
18. Craig, T. P., J. K. Itami, W. G. Abrahamson, and J. D. Horner. 1993. Behavioral evidence for host-race formation in Eurosta solidaginis. Evolution 47 : 1696 1710.
19. Darwin, C. 1859. On the origin of species by means of natural selection or the preservation of favored races in the struggle for life. J. Murray, London.
20. Dasmahapatra, K. K., M. J. Blum, A. Aiello, S. Hackwell, N. Davies, E. P. Bermingham, and J. Mallet. 2002. Inferences from a rapidly moving hybrid zone. Evolution 56 : 741 753.
21. Dieckmann, U., and M. Doebeli. 1999. On the origin of species by sympatric speciation. Nature 400 : 354 357.
22. Dumolin-Lapegue, S., M.-H. Pemonge, and R. J. Petit. 1997. An enlarged set of consensus primers for the study of organelle DNA in plants. Mol. Ecol. 6 : 393 397.
23. Egan, S. P., and D. J. Funk. 2006. Individual advantages to ecological specialization: insights on cognitive constraints from three conspecific taxa. Proc. R. Soc. Lond. B. 273 : 843848.
24. Emelianov, I., F. Marec, and J. Mallet. 2003. Genomic evidence for divergence with gene flow in host races of the larch budmoth. Proc. R. Soc. Lond. B 271 : 97 105.
25. Endler, J. A. 1986. Natural selection in the wild. Princeton Univ. Press, Princeton, NJ.
26. Feder, J. L., S. B. Opp, B. Wlazlo, K. Reynolds, W. Go, and S. Spisak. 1994. Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. Proc. Natl. Acad. Sci. USA 91 : 7990 7994.
27. Feder, J. L., S. H. Berlocher, and S. B. Opp. 1998. Sympatric host-race formation and speciation in Rhagoletis (Diptera: Tephritidae): a tale of two species for Charles D. Pp. 408 441 in S. Mopper, and S. Strauss, eds. Genetic structure and local adaptation in natural insect populations: effects of ecology, life history, and behavior. Chapman & Hall, New York.
28. Feder, J. L., F. B. Roethele, K. Filchak, J. Niedbalski, and J. Romero-Severson. 2003. Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly, Rhagoletis pomonella. Genetics 163 : 939 953.
29. Felsenstein, J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35 : 124 138.
30. Felsenstein, J. 2004. PHYLIP. Distributed by the author, Department of Genome Sciences, Univ. of Washington, Seattle.
31. Fisher, R. A. 1930. The genetical theory of natural selection. Clarendon Press, Oxford.
32. Funk, D. J. 1996. The evolution of reproductive isolation in Neochlamisus leaf beetles: a role for selection. PhD Dissertation., State Univ. of New York, Stony Brook, NY.
33. Funk, D. J. 1998. Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 52 : 1744 1759.
34. Funk, D. J. 1999. Molecular systematics of cytochrome oxidase I and 16S from Neochlamisus leaf beetles and the importance of sampling. Mol. Biol. Evol. 16 : 67 82.
35. Funk, D. J., and P. Nosil. 2008. Comparative analyses and ecological speciation in herbivorous insects. Pp. 117 135 in K. Tilmon, ed. Ecology and evolution of herbivorous insects. University of California Press, Berkeley, CA.
36. Funk, D. J., K. E. Filchak, and J. L. Feder. 2002. Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 116 : 251 267.
37. Funk, D. J., P. Nosil, and W. Etges. 2006. Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc. Natl. Acad. Sci. USA 103 : 3209 3213.
38. Gavrilets, S. 2004. Fitness landscapes and the origin of species. Princeton Univ. Press, Princeton, NJ.
39. Gompert, Z., J. A. Fordyce, M. L. Forister, A. M. Shapiro, and C. C. Nice. 2006. Homoploid hybrid speciation in an extreme habitat. Science 314 : 1923 1925.
40. Grant, P. R., B. R. Grant, and K. Petren. 2005. Hybridization in the Recent Past. Am. Nat. 166 : 56 67.
41. Hartl, D. L., and A. G. Clark. 1997. Principles of population genetics. Sinauer Associates, Sunderland, MA.
42. Haubold, B., and Hudson, R. R. 2000. LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics 16 : 847 848.
43. Hawthorne, D. J., and S. Via. 2001. Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412 : 904 907.
44. Hedrick, P. W. 2005. A standardized genetic differentiation measure. Evolution 59 : 1633 1638.
45. Hill, W. G. 1974. Estimation of linkage disequilibrium in randomly mating populations. Heredity 33 : 229 239.
46. Hoekstra, H. E., R. J. Hirschmann, R. A. Bundey, P. A. Insel, and J. P. Crossland. 2006. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313 : 101 104.
47. Jiggins, C. D., R. E. Naisbit, R. L. Coe, and J. M. Mallet. 2001. Reproductive isolation caused by colour pattern mimicry. Nature 411 : 302 305.
48. Joron, M., R. Papa, M. Beltran, N. Chamberlain, J. Mavarez, S. Baxter, M. Abanto, E. Bermingham, S. J. Humphray, J. Rogers, et al. 2006. A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLOS Biol. 4 : 1831 1840.
49. Jump, A. S., J.M Hunt, J.A Martinez-Izquirdo, and J. Penuelas. 2006. Natural selection and climate change: temperature-linked spatial and temporal trends in gene frequency in Fagus sylvatica. Mol. Ecol. 15 : 3469 3480.
50. Karren, J. B. 1972. A revision of the subfamily Chlamisinae of America north of Mexico (Coleoptera: Chrysomelidae). Univ. Kansas Sci. Bull. 49 : 875 988.
51. Kimura, M. 1968. Evolutionary rate at the molecular level. Nature 217 : 624 626.
52. Kimura, M. 1986. DNA and the neutral theory. Philos. Trans. R. Soc. Lond. B 312 : 343 354.
53. King, J. L., and T. H. Jukes. 1969. Non-Darwinian evolution. Science 164 : 788 798.
54. Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri, C. E. Hill, A. Hoang, P. Gilbert, and P. Beerli. 2001. The strength of phenotypic selection in natural populations. Am. Nat. 157 : 245 261.
55. Kondrashov, A. S., and F. A. Kondrashov. 1999. Interactions among quantitative traits in the course of sympatric speciation. Nature 400 : 351 354.
56. Langerhans, R. B., M. E. Gifford, and E. O. Joseph. 2007. Ecological speciation in Gambusia fishes. Evolution 61 : 2056 2074.
57. Lexer, C., M. E. Welch, J. L. Durphy, and L. H. Rieseberg. 2003. Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. Mol. Ecol. 12 : 1255 1235.
58. Lexer, C., Z. Lai, and L. H. Rieseberg. 2004. Candidate gene polymorphisms associated with salt tolerance in wild sunflower hybrids: implication for the origin of Helianthus paradoxus, a diploid hybrid species. New Phytol. 161 : 225 233.
59. Mallet, J., N. Barton, G. Lamas, C. Jose Santisteban, M., Muedas, 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.
60. Manly, B. F. J. 1997. Randomization, bootstrap and Monte Carlo methods in biology. Chapman and Hall, London.
61. Maynard Smith, J. 1966. Sympatric speciation. Am. Nat. 100 : 637 650.
62. Mayr, E. 1942. Systematics and the origin of species. Columbia Univ. Press, New York.
63. Mayr, E. 1947. Ecological factors in speciation. Evolution 1 : 263 288.
64. Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge.
65. Muller, H. J. 1942. Isolating mechanisms, evolution and temperature. Biol. Symp. 6 : 71 125.
66. Murray, M. C., and M. P. Hare. 2006. A genomic scan for divergent selection in a secondary contact zone between Atlantic and Gulf of Mexico oysters, Crassostrea virginica. Mol. Ecol. 15 : 4229 4242.
67. Nachman, M. W., H. E. Hoekstra, and S. L. D'Agostino. 2003. The genetic basis of adaptive melanism in pocket mice. Proc. Natl. Acad. Sci. USA 100 : 5268 5273.
68. Nielsen, R. 2005. Molecular signatures of natural selection. Annu. Rev. Genet. 39 : 197 218.
69. Noor, M. A. F., and J. L. Feder. 2006. Speciation genetics: evolving approaches. Nat. Rev. Genet. 7 : 851 861.
70. Noor, M. A. F., K. L. Grams, L. A. Bertucci, and J. Reiland. 2001. Chromosomal inversions and the reproductive isolation of species. Proc. Natl. Acad. Sci. USA 98 : 12084 12088.
71. Nosil, P. 2004. Reproductive isolation caused by visual predation on migrants between divergent environments. Proc. R. Soc. Lond. B 271 : 1521 1528.
72. Nosil, P. 2007. Divergent host-plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking-sticks. Am. Nat. 169 : 151 162.
73. Nosil, P., and B. J. Crespi. 2006. Experimental evidence that predation promotes divergence during adaptive radiation. Proc. Natl. Acad. Sci. USA 103 : 9090 9095.
74. Nosil, P., B. J. Crespi, and C. P. Sandoval. 2002. Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417 : 440 443.
75. Nosil, P., T. H. Vines, and D. J. Funk. 2005. Perspective : Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59 : 705 719.
76. Nosil, P., S. P. Egan, and D. J. Funk. 2008. Heterogeneous genomic differentiation between walking-stick ecotypes: 'isolation by adaptation' and multiple roles for divergent selection. Evolution 62 : 316 336.
77. Ohta, T. 1992. The nearly neutral theory of molecular evolution. Annu. Rev. Ecol. Syst. 23 : 263 286.
78. Ohta, T. 2002. Near-neutrality in evolution of genes and gene regulation. Proc. Natl. Acad. Sci. USA 99 : 16134 16137.
79. Peterson, M. A., and R. F. Denno. 1998. Life-history strategies and the genetic structure of phytophagous insect populations. Pp. 263 322 in S. Mopper, and S. Strauss, eds. Genetic structure and local adaptation in natural insect populations: effects of ecology, life history, and behavior. Chapman & Hall, New York.
80. Pompanon, F., A. Bonin, E. Bellemain, and P. Taberlet. 2005. Genotyping errors: causes, consequences and solutions. Nat. Rev. Genet. 6 : 847 859.
81. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155 : 945 959.
82. Rieseberg, L. H. 2001. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16 : 351 358.
83. Rogers, S. M., N. Isabel, and L. Bernatchez. 2007. Linkage maps of the dwarf and normal lake whitefish (Coregonus clupeaformis) species complex and their hybrids reveal the genetic architecture of population divergence. Genetics 175 : 375 398.
84. Rundle, H. D. 2002. A test of ecologically dependent post-mating isolation between sympatric sticklebacks. Evolution 56 : 322 329.
85. Rundle, H., and P. Nosil. 2005. Ecological speciation. Ecol. Letters 8 : 336 352.
86. Rundle, H. D., L. Nagel, J. W. Boughman, and D. Schluter. 2000. Natural selection and parallel speciation in sympatric sticklebacks. Science 287 : 306 308.
87. Savolainen, V., M. C. Anstett, C. Lexer, I. Hutton, J. J. Clarkson, M. V. Norup, M. P. Powell, D. Springate, N. Salamin, and W. J. Baker. 2006. Sympatric speciation in palms on an oceanic island. Nature 441 : 210 213.
88. Schluter, D. 2000. The ecology of adaptive radiation. Oxford Univ. Press, Oxford.
89. Schluter, D. 2001. Ecology and the origin of species. Trends Ecol. Evol. 16 : 372 380.
90. Schluter, D., and L. M. Nagel. 1995. Parallel speciation by natural selection. Am. Nat. 146 : 292 301.
91. Scotti-Saintagne, C., S. Mariette, I. Porth, P. G. Goicoechea, T. Barreneche, K. Bodenes, K. Burg, and A. Kremer. 2004. Genome scanning for interspecific differentiation between two closely related oak species (Quercus robur L. and Q. petraea (Matt.) Liebl.). Genetics 168 : 1615 1626.
92. Stinchcombe, J. R., and H. E. Hoekstra. 2008. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100 : 158 170.
93. Storz, J. F. 2005. Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol. Ecol. 14 : 671 688.
94. Szymura, J. M., and N. H. 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.
95. Taberlet, P., L. Gielly, G. Pautou, and J. Bouvet. 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol. Biol. 17 : 1105 1109.
96. Vasemagi, A., and C. R. Primmer. 2005. Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies. Mol. Ecol. 14 : 3623 3642.
97. Vasemagi, A., J. Nilsson, and C. R. Primmer. 2005. Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic salmon (Salmo salar L.). Mol. Biol. Evol. 22 : 1067 1076.
98. Vekemans, X., T. Beauwens, M. Lemaire, and I. Roldan-Ruiz. 2002. Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol. Ecol. 11 : 139 151.
99. Via, S. 1999. Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53 : 1446 1457.
100. Via, S., A. C. Bouck, and S. Skillman. 2000. Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments. Evolution 54 : 1626 1637.
101. Vines, T. H., and D. Schluter. 2006. Strong assortative mating between allopatric sticklebacks as a by-product of adaptation to different environments. Proc. R. Soc. Lond. B 273 : 911 916.
102. Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. Vandelee, M. Hornes, A. Fritjers, J. Pot, J. Peleman, M. Kuiper, et al. 1995. AFLP - a new technique for DNA-fingerprinting. Nucl. Acids Res. 23 : 4407 4414.
103. Wilding, C. S., R. K. Butlin, and J. Grahame. 2001. Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J. Evol. Biol. 14 : 611 619.
104. Winkler, I. S., and C. Mitter. 2008. The phylogenetic dimension of insect/plant assemblages: a review of recent evidence. Pp. 240 263 in K. Tilmon, ed. Ecology and evolution of herbivorous insects. University of California Press, Berkeley, CA.
105. Wood, T. K., and M. C. Keese. 1990. Host-plant-induced assortative mating in Enchenopa treehoppers. Evolution 44 : 619 628.
106. Yatabe, Y., N. C. Kane, C. Scotti-Saintagne, and L. H. Rieseberg. 2007. Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175 : 1883 1893.
107. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16 : 97 159.
108. Wright, S. 1943. Isolation by distance. Genetics 28 : 114 138.
109. Zhivotovsky, L. A. 1999. Estimating population structure in diploids with multilocus dominant DNA markers. Mol. Ecol. 8 : 907 913.