Cryptic genetic variation and body size evolution in threespine stickleback

Evolution

Volumn 65, Issue 4, 2011, Pages 1203-1211

  Mcguigan, Katrina ^a   Nishimura, Nicole ^b   Currey, Mark ^b   Hurwit, Dan ^b   Cresko, William A ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF OREGON   (United States)

Author keywords

Buffering; Colonization; Gasterosteus aculeatus; Heritability; Salinity

Indexed keywords

FRESH WATER;

BODY SIZE; BUFFERING; COLONIZATION; CRYPSIS; FRESHWATER ENVIRONMENT; GENE EXPRESSION; GENETIC VARIATION; HABITAT TYPE; HERITABILITY; MIMICRY; OBSERVATIONAL METHOD; PHENOTYPE; POPULATION STRUCTURE; SALINITY; SELECTION; TELEOST;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BODY SIZE; BREEDING; ECOSYSTEM; EVOLUTION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; HISTOLOGY; METHODOLOGY; SALINITY; SMEGMAMORPHA; STATISTICAL MODEL; UNITED STATES;

ALASKA; ANALYSIS OF VARIANCE; ANIMALS; BIOLOGICAL EVOLUTION; BODY SIZE; BREEDING; ECOSYSTEM; FRESH WATER; GENETIC VARIATION; MODELS, STATISTICAL; SALINITY; SELECTION, GENETIC; SMEGMAMORPHA;

GASTEROSTEUS; GASTEROSTEUS ACULEATUS;

EID: 79953302401     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2010.01195.x     Document Type: Article

References (92)

1. Aguirre, W. E., K. E. Ellis, M. Kusenda, and M. A. Bell 2008. Phenotypic variation and sexual dimorphism in anadromous threespine stickleback: implications for postglacial adaptive radiation. Biol. J. Linn. Soc. 95:465-478.
2. Albert, A. Y. K., S. Sawaya, T. H. Vines, A. K. Knecht, C. T. Miller, B. R. Summers, S. Balabhadra, D. M. Kingsley, and D. Schluter 2008. The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution 62:76-85.
3. Arnold, S. J., R. Burger, P. A. Hohenlohe, B. C. Ajie, and A. G. Jones 2008. Understanding the evolution and stability of the G-matrix. Evolution 62:2451-2461.
4. Badyaev, A. V. 2005. Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation. Proc. R. Soc. B Biol. Sci. 272:877-886.
5. Baker, J. A., D. C. Heins, S. A. Foster, and R. W. King 2008. An overview of life-history variation in female threespine stickleback. Behaviour 145:579-602.
6. Barrett, R. D. H., S. M. Rogers, and D. Schluter 2008. Natural selection on a major armor gene in threespine stickleback. Science 322:255-257.
7. Barrett, R. D. H., S. M. Rogers, and D. Schluter 2009. Environment specific pleiotropy facilitates divergence at the Ectodysplasin locus in threespine stickleback. Evolution 63:2831-2837.
8. Barrett, R. D. H., and D. Schluter 2008. Adaptation from standing genetic variation. Trends Ecol. Evol. 23:38-44.
9. Barton, N. H., and M. Turelli 1987. Adaptive landscapes, genetic distance and the evolution of quantitative characters. Gen. Res. 49:157-173.
10. Barton, N. H., and M. Turelli 1989. Evolutionary quantitative genetics: how little do we know? Annu. Rev. Genet. 23:337-370.
11. Bell, M. A. 1981. Lateral plate polymorphism and ontogeny of the complete plate morph of threespone sticklebacks (Gasterosteus aculeatus). Evolution 35:67-74.
12. Bell, M. A. 1994. Paleobiology and evolution of threespine stickleback. Pp. 438-471 in M. A. Bell and S. A. Foster, eds. The evolutionary biology of the threespine stickleback. Oxford Univ. Press, Oxford.
13. Bell, M. A., W. E. Aguirre, and N. J. Buck 2004. Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58:814-824.
14. Bell, M. A., and S. A. Foster 1994. The evolutionary biology of the threespine stickleback. Oxford Univ. Press, Oxford.
15. Bell, M. A., G. Orti, J. A. Walker, and J. P. Koenings 1993. Evolution of pelvic reduction in threespine stickleback: a test of competing hypotheses. Evolution 47:906-914.
16. Blows, M. W., and A. A. Hoffmann 2005. A reassessment of genetic limits to evolutionary change. Ecology 86:1371-1384.
17. Bystrom, P., J. Andersson, A. Kiessling, and L. O. Eriksson 2006. Size and temperature dependent foraging capacities and metabolism: consequences for winter starvation mortality in fish. Oikos 115:43-52.
18. Carlson, S. M., H. B. Rich, and T. P. Quinn 2009. Does variation in selection imposed by bears drive divergence among populations in the size and shape of sockeye salmon? Evolution 63:1244-1261.
19. Charmantier, A., and D. Garant 2005. Environmental quality and evolutionary potential: lessons from wild populations. Proc. R. Soc. B Biol. Sci. 272:1415-1425.
20. 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.
21. Colosimo, P. F., C. L. Peichel, K. Nereng, B. K. Blackman, M. D. Shapiro, D. Schluter, and D. M. Kingsley 2004. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol. 2:635-641.
22. Cresko, W. A. 2008. Armor development and fitness. Science 322:204-206.
23. Cresko, W. A., A. Amores, C. Wilson, J. Murphy, M. Currey, P. Phillips, M. A. Bell, C. B. Kimmel, and J. H. Postlethwait 2004. Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc. Natl. Acad. Sci. USA 101:6050-6055.
24. Cresko, W. A., K. L. McGuigan, P. C. Phillips, and J. H. Postlethwait 2007. Studies of threespine stickleback developmental evolution: progress and promise. Genetica 129:105-126.
25. de Visser, J., J. Hermisson, G. P. Wagner, L. A. Meyers, H. Bagheri-Chaichian, J. L. Blanchard, L. Chao, J. M. Cheverud, S. F. Elena, W. Fontana, et al. 2003. Evolution and detection of genetic robustness. Evolution 57:1959-1972.
26. Estes, S., and S. J. Arnold 2007. Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. Am. Nat. 169:227-244.
27. Eyre-Walker, A. 2010. Genetic architecture of a complex trait and its implications for fitness and genome-wide association studies. Proc. Natl. Acad. Sci. USA 107:1752-1756.
28. Falconer, D. S., and T. F. C. Mackay 1996. Introduction to quantitative genetics. Longman Group Limited, Essex, England.
29. Fear, K. K., and T. Price 1998. The adaptive surface in ecology. Oikos 82:440-448.
30. Flint, J., and T. F. C. Mackay 2009. Genetic architecture of quantitative traits in mice, flies, and humans. Genome Res. 19:723-733.
31. Futuyma, D. J. 2010. Evolutionary constraint and ecological consequences. Evolution 64:1865-1884.
32. Gelmond, O., F. A. von Hippel, and M. S. Christy 2009. Rapid ecological speciation in three-spined stickleback Gasterosteus aculeatus from Middleton Island, Alaska: the roles of selection and geographic isolation. J. Fish Biol. 75:2037-2051.
33. Ghalambor, C. K., J. K. McKay, S. P. Carroll, and D. N. Reznick 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21:394-407.
34. Gibson, G., and I. Dworkin 2004. Uncovering cryptic genetic variation. Nat. Rev. Genet. 5:681-690.
35. Giles, N. 1983. The possible role of environmental calcium levels during hte evolution of phenotypic diversity in outer-Hebridean populations of the three-spined stickleback, Gasterosteus aculeatus. J. Zool. 199:535-544.
36. Grant, P. R., and B. R. Grant 1995. Predicting microevolutionary responses to directional selection on heritable variation. Evolution 49:241-251.
37. Hadfield, J. D. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33:1-22.
38. Hagen, D. W. 1973. Inheritance of numbers of lateral plates and gill rakers in Gasterosteus aculeatus. Heredity 30:303-312.
39. Haldane, J. B. S. 1927. A mathematical theory of natural and artificial selection, Part V: selection and mutation. Proc. Camb. Philol. Soc. 23:838-844.
40. Hansen, T. F., and D. Houle 2008. Measuring and comparing evolvability and constraint in multivariate characters. J. Evol. Biol. 21:1201-1219.
41. Herczeg, G., A. Gonda, and J. Merila 2009. Evolution of gigantism in nine-spined sticklbacks. Evolution 63:3190-3200.
42. Hill, W. G. 2010. Understanding and using quantitative genetic variation. Phil. Trans. R. Soc. Lond. B Biol. Sci. 365:73-85.
43. Hoffmann, A. A., and J. Merila 1999. Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol. Evol. 14:96-101.
44. Hohenlohe, P. A., S. Bassham, P. Etter, N. Stiffler, E. Johnson, and W. A. Cresko 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genetics 6:e1000862.
45. Houle, D. 2010. Numbering the hairs on our heads: the shared challenge and promise of phenomics. Proc. Natl. Acad. Sci. USA 107:1793-1799.
46. Hunt, J., M. W. Blows, F. Zajitschek, M. D. Jennions, and R. Brooks 2007. Reconciling strong stabilizing selection with the maintenance of genetic variation in a natural population of black field crickets (Teleogryllus commodus). Genetics 177:875-880.
47. Hunt, J., C. J. Breuker, J. A. Sadowski, and A. J. Moore 2009. Male-male competition, female mate choice and their interaction: determining total sexual selection. J. Evol. Biol. 22:13-26.
48. Ishikawa, M., and S. Mori 2000. Mating success and male courtship behaviors in three populations of the threespine stickleback. Behaviour 137:1065-1080.
49. Johnson, T., and N. Barton 2005. Theoretical models of selection and mutation on quantitative traits. Phil. Trans. R. Soc. Lond. B Biol. Sci. 360:1411-1425.
50. Kellermann, V. M., B. van Heerwaarden, A. A. Hoffmann, and C. M. Sgro 2006. Very low additive genetic variance and evolutionary potential in multiple populations of two rainforest Drosophila species. Evolution 60:1104-1108.
51. Kingsolver, J. G., and D. W. Pfennig 2004. Individual-level selection as a cause of Cope's rule of phyletic size increase. Evolution 58:1608-1612.
52. Kirkpatrick, M. 1982. Quantum evolution and punctuated equilibria in continuous genetic characters. Am. Nat. 119:833-848.
53. Kitano, J., J. A. Ross, S. Mori, M. Kume, F. C. Jones, Y. F. Chan, D. M. Absher, J. Grimwood, J. Schmutz, R. M. Myers, et al. 2009. A role for a neo-sex chromosome in stickleback speciation. Nature 461:1079-1083.
54. Kristjansson, B. K. 2005. Rapid morphological changes in threespine stickleback, Gasterosteus aculeatus, in freshwater. Environ. Biol. Fish. 74:357-363.
55. Lande, R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 33:402-416.
56. Lynch, M., and B. Walsh 1998. Genetics and analysis of quantitative traits. Sinauer Associates Inc., Sunderland, MA.
57. Marchinko, K. B. 2009. Predation's role in repeated phenotypic and genetic divergence of armor in threespine stickleback. Evolution 63:127-138.
58. Marchinko, K. B., and D. Schluter 2007. Parallel evolution by correlated response: lateral plate reduction in threespine stickleback. Evolution 61:1084-1090.
59. Masel, J., and M. L. Siegal 2009. Robustness: mechanisms and consequences. Trends Genet. 25:395-403.
60. McCairns, R. J. S., and L. Bernatchez 2010. Adaptive divergence between freshwater and marine sticklebacks: insights into the role of phenotypic plasticity from an integrated analysis of candidate gene expression. Evolution 64:1029-1047.
61. McGuigan, K., N. Nishimura, M. Currey, D. Hurwit, and W. A. Cresko 2010. Quantitative genetic variation in static allometry in the threespine stickleback Integr. Comp. Biol. 50:1067-1080.
62. McGuigan, K., and C. M. Sgro 2009. Evolutionary consequences of cryptic genetic variation. Trends Ecol. Evol. 24:305-311.
63. McKinnon, J. S., S. Mori, B. K. Blackman, L. David, D. M. Kingsley, L. Jamieson, J. Chou, and D. Schluter 2004. Evidence for ecology's role in speciation. Nature 429:294-298.
64. McPhail, J. D. 1977. Inherited interpopulation differences in size at first reproductionin threspine stickleback, Gasterosteus aculeatus L. Heredity 38:53-60.
65. Moen, D. S., and J. J. Wiens 2009. Phylogenetic evidence for competitively driven divergence: body size evolution in Caribbean treefrogs (Hylidae: Osteopilus). Evolution 63:195-214.
66. Mori, S. 1990. Two morphological types in the reproductive stock of three-spined stickleback, Gasterosteus aculeatus, in Lake Harutori, Hokkaido Island. Environ. Biol. Fish. 27:21-31.
67. Nagel, L., and D. Schluter 1998. Body size, natural selection, and speciation in sticklebacks. Evolution 52:209-218.
68. Pfennig, D. W., M. A. Wund, E. C. Snell-Rood, T. Cruickshank, C. D. Schlichting, and A. P. Moczek 2010. Phenotypic plasticity's impacts on diversification and speciation. Trends Ecol. Evol. 25:459-467.
69. Pigliucci, M., and C. J. Murren 2003. Genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution 57:1455-1464.
70. Potthoff, T. 1984. Clearing and staining techniques. Pp. 35-37 in H. G. Moser, W. J. Richards, D. M. Cohen, M. P. Fahay, A. W. J. Kendall, and S. L. Richardson, eds. Ontogeny and Systematics of Fish. Allen Press, Lawrence, KS.
71. Price, T. D., A. Qvarnstrom, and D. E. Irwin 2003. The role of phenotypic plasticity in driving genetic evolution. Proc. R. Soc. Lond. B. 270:1433-1440.
72. Reeve, J. P. 2000. Predicting long-term response to selection. Gen. Res. 75:83-94.
73. Rohlf, F. J. 1999. Shape statistics: procrustes superimpositions and tangent spaces. J. Classification. 16:197-223.
74. Rohlf, F. J. 2005. tps Morphometric Software. Available at Dept. of Ecology and Evolution, State Univ. of New York, Stony Brook, NY.
75. Rutherford, S. L., and S. Lindquist 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336-342.
76. Schlichting, C. D. 2008. Hidden reaction norms, cryptic genetic variation, and evolvability. Ann. N. Y. Acad. Sci. 1133:187-203.
77. Schluter, D. 1993. Adaptive radiation in sticklebacks: size shape and habitat use efficiency. Ecology 74:699-709.
78. Scoville, A. G., and M. E. Pfrender 2010. Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc. Natl. Acad. Sci. USA 107:4260-4263.
79. Slice, D. E. 1998. Morpheus et al. Dept. of Ecology and Evolution, State Univ. of New York, Stony Brook, NY.
80. Snyder, R. J. 1991. Migration and life histories of the threespine stickleback: evidence for adaptive variation in growth rate between populations. Environ. Biol. Fish. 31:381-388.
81. Snyder, R. J., and H. Dingle 1989. Adaptive, genetically based differences in life history between estuary and freshwater threespine sticklebacks (Gasterosteus aculeatus L). Can. J. Zool. 67:2448-2454.
82. Steppan, S. J., P. C. Phillips, and D. Houle 2002. Comparative quantitative genetics: evolution of the G matrix. Trends Ecol. Evol. 17:320-327.
83. Taylor, E. B., and J. D. McPhail 2000. Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc. R. Soc. B Biol. Sci. 267:2375-2384.
84. Thomas, G. H., S. Meiri, and A. B. Phillimore 2009. Body size diversification in Anolis: novel environment and island effects. Evolution 63:2017-2030.
85. Turelli, M. 1988. Phenotypic evolution, constant covariances, and the maintenance of additive variances. Evolution 42:1342-1347.
86. Waddington, C. H. 1957. The strategy of the genes. Macmillan, New York.
87. Wagner, A. 2005. Robustness, evolvability, and neutrality. FEBS Lett. 579:1772-1778.
88. Walker, J. A., and M. A. Bell 2000. Net evolutionary trajectories of body shape evolution within a microgeographic radiation of threespine sticklebacks (Gasterosteus aculeatus). J. Zool. 252:293-302.
89. Walsh, B., and M. W. Blows 2009. Abundant genetic variation + strong selection = multivariate genetic constraints: a geometric view of adaptation. Annu. Rev. Ecol. Evol. Syst. 40:41-59.
90. Wilson, A. J. 2008. Why h(2) does not always equal V-A/V-P? J. Evol. Biol. 21:647-650.
91. Wootton, R. J. 2009. The Darwinian stickleback Gasterosteus aculeatus: a history of evolutionary studies. J. Fish Biol. 75:1919-1942.
92. Wright, H. A., R. J. Wootton, and I. Barber 2004. Interpopulation variation in early growth of threespine sticklebacks (Gasterosteus aculeatus) under laboratory conditions. Can. J. Fish. Aquat. Sci. 61:1832-1838.