Natural selection and the genetics of adaptation in threespine stickleback

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1552, 2010, Pages 2479-2486

  Schluter, Dolph ^a   Marchinko, Kerry B ^b   Barrett, R D H ^a   Rogers, Sean M ^c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

Ectodysplasin; Genetics of adaptation; Natural selection; Stickleback

Indexed keywords

ADAPTATION; ALLELE; COLONIZATION; GENOTYPE; NATURAL SELECTION; PHENOTYPIC PLASTICITY; POLYMORPHISM; TELEOST;

GASTEROSTEUS;

ECTODYSPLASIN A;

ADAPTATION; ANIMAL; BIOLOGICAL MODEL; BONE DEVELOPMENT; EVOLUTION; GENETIC SELECTION; GENETICS; GENOTYPE; PHENOTYPE; SMEGMAMORPHA;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; BONE DEVELOPMENT; ECTODYSPLASINS; GENOTYPE; MODELS, GENETIC; PHENOTYPE; SELECTION, GENETIC; SMEGMAMORPHA;

EID: 77956479812     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0036     Document Type: Article

References (64)

1. Albert, A. Y. K., Sawaya, S., Vines, T. H., Knecht, A. K., Miller, C. T., Summers, B. R., Balabhadra, S., Kingsley, D. M. & Schluter, D. 2008 The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution 62, 76-85.
2. Albertson, R. C., Streelman, J. T. & Kocher, T. D. 2003 Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proc. Natl Acad. Sci. USA 100, 5252-5257. (doi:10.1073/pnas.0930235100) (Pubitemid 36542691)
3. Balanya, J., Oller, J. M., Huey, R. B., Gilchrist, G. W. & Serra, L. 2006 Global genetic change tracks global climate warming in Drosophila subobscura. Science 313, 1773-1775. (doi:10.1126/science.1131002) (Pubitemid 44454151)
4. Barrett, R. D. H. & Schluter, D. 2010 Clarifying mechanisms of evolution in stickleback using field studies of natural selection on genes. In In search of the causes of evolution: from field observations to mechanisms (eds P. Grant & R. Grant). Princeton, NJ: Princeton University Press.
5. Barrett, R. D. H., Rogers, S. M. & Schluter, D. 2008 Natural selection on a major armor gene in threespine stickleback. Science 322, 255-257. (doi:10.1126/science.1159978)
6. Baxter, S. W., Papa, R., Chamberlain, N., Humphray, S. J., Joron, M., Morrison, C., ffrench-Constant, R. H., McMillan, W. O. & Jiggins, C. D. 2008 Convergent evolution in the genetic basis of Mullerian mimicry in Heliconius butterflies. Genetics 180, 1567-1577. (doi:10. 1534/genetics.107.082982)
7. Bell, M. A. 2001 Lateral plate evolution in the threespine stickleback: getting nowhere fast. Genetica 112, 445-461. (doi:10.1023/A:1013326024547) (Pubitemid 34119675)
8. Bradshaw, H. D. & Schemske, D. W. 2003 Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426, 176-178. (doi:10.1038/nature02106) (Pubitemid 37442584)
9. Bradshaw, H. D., Otto, K. G., Frewen, B. E., McKay, J. K. & Schemske, D. W. 1998 Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149, 367-382.
10. Chan, Y. F. et al. 2010 Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302-305. (doi:10.1126/science.1182213)
11. Charlesworth, D. & Charlesworth, B. 1975 Theoretical genetics of Batesian mimicry. 3. Evolution of dominance. J. Theor. Biol. 55, 325-337. (doi:10.1016/S0022-5193 (75) 80083-X)
12. Coberly, C. & Rausher, M. 2008 Pleiotropic effects of an allele producing white flowers in Ipomoea purpurea. Evolution 62, 1076-1085. (doi:10.1111/j.1558-5646. 2008.00355.x)
13. Collins, S., de Meaux, J. & Acquisti, C. 2007 Adaptive walks toward a moving optimum. Genetics 176, 1089-1099. (doi:10.1534/genetics.107.072926) (Pubitemid 46961107)
14. Colosimo, P. F. et al. 2005 Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307, 1928-1933. (doi:10.1126/science. 1107239) (Pubitemid 40941876)
15. Derome, N., Duchesne, P. & Bernatchez, L. 2006 Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformis Mitchill) ecotypes. Mol. Ecol. 15, 1239-1249. (doi:10.1111/j.1365-294X. 2005.02968.x)
16. Durinx, M. & Van Dooren, T. J. M. 2009 Assortative mate choice and dominance modification: alternative ways of removing heterozygote disadvantage. Evolution 63, 334-352. (doi:10.1111/j.1558-5646.2008.00578.x)
17. Edelist, C., Lexer, C., Dillmann, C., Sicard, D. & Rieseberg, L. H. 2006 Microsatellite signature of ecological selection for salt tolerance in a wild sunflower hybrid species, Helianthus paradoxus. Mol. Ecol. 15, 4623-4634. (doi:10.1111/j.1365-294X.2006.03112.x) (Pubitemid 44749574)
18. Eyre-Walker, A. 2006 The genomic rate of adaptive evolution. Trends Ecol. Evol. 21, 569-575. (doi:10.1016/j.tree.2006.06.015) (Pubitemid 44353858)
19. Feldman, C. R., Brodie Jr, E. D., Brodie 3rd, E. D. & Pfrender, M. E. 2009 The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey. Proc. Natl Acad. Sci. USA 106, 13 415-13 420. (doi:10.1073/pnas.0901224106)
20. Fisher, R. A. 1930 The genetical theory of natural selection. Oxford, UK: Oxford University Press.
21. Fishman, L., Kelly, A. & Willis, J. 2002 Minor quantitative trait loci underlie floral traits associated with mating system divergence in Mimulus. Evolution 56, 2138-2155.
22. Fitzpatrick, M. J., Feder, E., Rowe, L. & Sokolowski, M. B. 2007 Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene. Nature 447, 210-215. (doi:10.1038/nature05764) (Pubitemid 46763079)
23. Gratten, J., Wilson, A. J., McRae, A. F., Beraldi, D., Visscher, P. M., Pemberton, J. M. & Slate, J. 2008 A localized negative genetic correlation constrains microevolution of coat color in wild sheep. Science 319, 318-320. (doi:10.1126/science.1151182)
24. Griswold, C. K. & Whitlock, M. C. 2003 The genetics of adaptation: the roles of pleiotropy, stabilizing selection and drift in shaping the distribution of bidirectional fixed mutational effects. Genetics 165, 2181-2192.
25. Gross, J. B., Borowsky, R. & Tabin, C. J. 2009 A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genet. 5, e1000326. (doi:10.1371/journal.pgen. 1000326)
26. Hagen, D. W. & Gilbertson, L. G. 1972 Geographic variation and environmental selection in Gasterosteus aculeatus L. in the Pacific Northwest, America. Evolution 26, 32-51. (doi:10.2307/2406981)
27. Hoekstra, H. E., Hoekstra, J. M., Berrigan, D., Vignieri, S. N., Hoang, A., Hill, C. E., Beerli, P. & Kingsolver, J. G. 2001 Strength and tempo of directional selection in the wild. Proc. Natl Acad. Sci. USA 98, 9157-9160. (doi:10.1073/pnas.161281098) (Pubitemid 32743885)
28. Hutchinson, I., James, T. S., Clague, J. J., Barrie, J. V. & Conway, K. W. 2004 Reconstruction of late Quaternary sea-level change in southwestern British Columbia from sediments in isolation basins. Boreas 33, 183-194. (doi:10.1080/03009480410001299) (Pubitemid 39080991)
29. Jones, C. D. 1998 The genetic basis of Drosophila sechellia's resistance to a host plant toxin. Genetics 149, 1899-1908.
30. Kopp, M. & Hermisson, J. 2007 Adaptation of a quantitative trait to a moving optimum. Genetics 176, 715-719. (doi:10.1534/genetics.106.067215) (Pubitemid 350021059)
31. Kopp, M. & Hermisson, J. 2009 The genetic basis of phenotypic adaptation II: the distribution of adaptive substitutions in the moving optimum model. Genetics 183, 1453-1476. (doi:10.1534/genetics.109.106195)
32. Kryazhimskiy, S., Bazykin, G. A., Plotkin, J. B. & Dushoff, J. 2009 Directionality in the evolution of influenza A haemagglutinin. Proc. R. Soc. B 276, 3035-3035. (doi:10. 1098/rspb.2009.0830)
33. Lewontin, R. C. 1958 A general method for investigating the equilibrium of gene frequency in a population. Genetics 43, 420-434.
34. Lexer, C., Welch, M. E., Durphy, J. L. & Rieseberg, L. H. 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, 1225-1235. (doi:10.1046/j.1365-294X.2003. 01803.x) (Pubitemid 36573124)
35. Linnen, C. R., Kingsley, E. P., Jensen, J. D. & Hoekstra, H. E. 2009 On the origin and spread of an adaptive allele in deer mice. Science 325, 1095-1098. (doi:10.1126/science.1175826)
36. Marchinko, K. B. & Schluter, D. 2007 Parallel evolution by correlated response: lateral plate reduction in threespine stickleback. Evolution 61, 1084-1090. (doi:10.1111/j. 1558-5646.2007.00103.x)
37. Martin, G., Elena, S. F. & Lenormand, T. 2007 Distributions of epistasis in microbes fit predictions from a fitness landscape model. Nat. Genet. 39, 555-560. (doi:10.1038/ng1998) (Pubitemid 46514778)
38. Maynard Smith, J. 1966 Sympatric speciation. Am. Nat. 100, 637-650. (doi:10.1086/282457)
39. McBride, C. S. 2007 Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia. Proc. Natl Acad. Sci. USA 104, 4996-5001. (doi:10.1073/pnas.0608424104) (Pubitemid 47186165)
40. Miller, C. T., Beleza, S., Pollen, A. A., Schluter, D., Kittles, R. A., Shriver, M. D. & Kingsley, D. M. 2007 Cisregulatory changes in kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131, 1179-1189. (doi:10.1016/j.cell.2007.10.055) (Pubitemid 350235026)
41. Mitchell-Olds, T., Willis, J. H. & Goldstein, D. B. 2007 Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat. Rev. Genet. 8, 845-856. (doi:10.1038/nrg2207) (Pubitemid 47609091)
42. Nielsen, R. 2005 Molecular signatures of natural selection. Annu. Rev. Genet. 39, 197-218. (doi:10.1146/annurev. genet.39.073003.112420)
43. Nosil, P. 2009 Adaptive population divergence in cryptic color-pattern following a reduction in gene flow. Evolution 63, 1902-1912. (doi:10.1111/j.1558-5646. 2009.00671.x)
44. Orr, H. A. 1998 The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52, 935-949. (doi:10.2307/2411226)
45. Orr, H. A. 1999 The evolutionary genetics of adaptation: a simulation study. Genet. Res. 74, 207-214.
46. Orr, H. A. 2001 The genetics of species differences. Trends Ecol. Evol. 16, 343-350. (doi:10.1016/S0169-5347 (01) 02167-X)
47. Orr, H. A. 2005 The genetic theory of adaptation: a brief history. Nat. Rev. Genet. 6, 119-127. (doi:10.1038/nrg1523) (Pubitemid 40179534)
48. Otto, S. P. & Jones, C. D. 2000 Detecting the undetected: estimating the total number of loci underlying a quantitative trait. Genetics 156, 2093-2107.
49. Reimchen, T. E. 1995 Predator-induced cyclical changes in lateral plate frequencies of Gasterosteus. Behaviour 132, 1079-1094. (doi:10.1163/ 156853995X00469)
50. Reimchen, T. E. 2000 Predator handling failures of lateral plate morphs in Gasterosteus aculeatus: functional implications for the ancestral plate condition. Behaviour 137, 1081-1096. (doi:10.1163/156853900502448)
51. Rieseberg, L. H., Widmer, A., Arntz, A. M. & Burke, J. M. 2002 Directional selection is the primary cause of phenotypic diversification. Proc. Natl Acad. Sci. USA 99, 12 242-12 245. (doi:10.1073/pnas.192360899)
52. Rogers, S. M. & Bernatchez, L. 2007 The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp Salmonidae) species pairs. Mol. Biol. Evol. 24, 1423-1438. (doi:10.1093/molbev/msm066) (Pubitemid 47343948)
53. Sawamura, K., Davis, A. & Wu, C. 2000 Genetic analysis of speciation by means of introgression into Drosophila melanogaster. Proc. Natl Acad. Sci. USA 97, 2652-2655. (doi:10.1073/pnas.050558597) (Pubitemid 30159226)
54. Schluter, D. 1994 Experimental evidence that competition promotes divergence in adaptive radiation. Science 266, 798-801. (doi:10.1126/science. 266.5186.798)
55. Sella, G., Petrov, D. A., Przeworski, M. & Andolfatto, P. 2009 Pervasive natural selection in the Drosophila genome? PLoS Genet. 5, e1000495. (doi:10.1371/journal.pgen. 1000495)
56. Siepielski, A. M., DiBattista, J. D. & Carlson, S. M. 2009 It's about time: the temporal dynamics of phenotypic selection in the wild. Ecol. Lett. 12, 1261-1276. (doi:10. 1111/j.1461-0248.2009.01381.x)
57. Steiner, C. C., Weber, J. N. & Hoekstra, H. E. 2007 Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biol. 5, e219. (doi:10.1371/journal.pbio.0050219) (Pubitemid 47416586)
58. Storz, J. F. 2005 Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol. Ecol. 14, 671-688. (doi:10.1111/j.1365- 294X.2005.02437.x)
59. Subramaniam, B. & Rausher, M. D. 2000 Balancing selection on a floral polymorphism. Evolution 54, 691-695.
60. Taylor, E. B. & McPhail, J. D. 1986 Prolonged and burst swimming in anadromous and freshwater threespine stickleback, Gasterosteus aculeatus. Can. J. Zool. 64, 416-420. (doi:10.1139/z86-064)
61. Vamosi, S. M. 2003 The presence of other fish species affects speciation in threespine sticklebacks. Evol. Ecol. Res. 5, 717-730.
62. Walker, J. A. 1997 Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L (Gasterosteidae) body shape. Biol. J. Linn. Soc. 61, 3-50.
63. Walker, J. A. & Bell, M. A. 2000 Net evolutionary trajectories of body shape evolution within a microgeographic radiation of threespine sticklebacks (Gasterosteus aculeatus). J. Zool. 252, 293-302. (doi:10.1111/j.1469-7998.2000.tb00624.x)
64. Wilson, D. S. & Turelli, M. 1986 Stable underdominance and the evolutionary invasion of empty niches. Am. Nat. 127, 835-850.