Contemporary evolution, allelic recycling, and adaptive radiation of the threespine stickleback

Evolutionary Ecology Research

Volumn 15, Issue 4, 2013, Pages 377-411

  Bell, Michael A ^a   Aguirre, Windsor E ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b DEPAUL UNIVERSITY   (United States)

Author keywords

Evolutionary genomics; Gasterosteus aculeatus; Introgression; Invasive species; Parallelism; Recessive allele; Threespine stickleback

Indexed keywords

EID: 84879612427     PISSN: 15220613     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (167)

1. Adachi, T., Ishikawa, A., Mori, S., Makino, W., Kume, M., Kawata, M. et al. 2012. Shifts in morphology and diet of non-native sticklebacks introduced into Japanese crater lakes. Ecol. Evol., 2: 1083-1098.
2. Aguirre, W.E. 2007. The pattern and process of evolutionary diversification: Lessons from a threespine stickleback adaptive radiation. PhD dissertation, Stony Brook University, Stony Brook, NY.
3. Aguirre, W.E. 2009. Microgeographical diversification of threespine stickleback: body shape-habitat correlations in a small, ecologically diverse Alaskan drainage. Biol. J. Linn. Soc., 98: 139-151.
4. Aguirre, W.E. and Bell, M.A. 2012. Twenty years of body shape evolution in a threespine stickleback population adapting to a lake environment. Biol. J. Linn. Soc., 105: 817-831.
5. Aguirre, W.E., Doherty, P.K. and Bell, M.A. 2004. Genetics of lateral plate and gill raker phenotypes in a rapidly evolving population of threespine stickleback. Behaviour, 141: 1465-1483. (Pubitemid 40181208)
6. Aguirre, W.E., Ellis, K.E., Kusenda, M. and Bell, M.A. 2008. Phenotypic variation and sexual dimorphism in anadromous threespine stickleback: implications for postglacial adaptive radiation. Biol. J. Linn. Soc., 95: 465-478.
7. Albert, A.Y.K., Sterling, S., Vines, T.H., Knecht, A.K., Miller, C.T., Summers, B.R. et al. 2007. The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution, 62: 76-85.
8. Applied Biostatistics, Inc. 2002. BIOMstat: Statistical Software for Biologists, version 3.30o.
9. Arif, S., Aguirre, W.E. and Bell, M.A. 2009. Evolutionary diversification of operculum shape in Cook Inlet threespine stickleback. Biol. J. Linn. Soc., 97: 832-844.
10. Baker, J.A., Heins, D.C., King, R.W. and Foster, S.A. 2011. Rapid shifts in multiple life history traits in a population of threespine stickleback. J. Evol. Biol., 24: 863-870.
11. Baker, J.A., Räsänen, K., Moore, J.-S. and Hendry, A.P. 2013. Genetic and plastic contributions to trait divergence between parapatric habitats: female life-history traits in threespine stickleback within the Misty Lake system. Evol. Ecol. Res., 15: 473-487.
12. Bańbura, J. and Bakker, T.C.M. 1995. Lateral plate morph genetics revisited: evidence for a fourth morph in three-spined sticklebacks. Behaviour, 132: 1153-1171.
13. Baquero, B. and Blázquez, J. 1997. Evolution of antibiotic resistance. Trends Ecol. Evol., 12: 482-487. (Pubitemid 28069365)
14. Barrett, R.D.H. 2010. Adaptive evolution of lateral plates in three-spined stickleback Gasterosteus aculeatus: a case study in functional analysis of natural variation. J. Fish Biol., 77: 311-328.
15. Barrett, R.D. and Schluter, D. 2007. Adaptation from standing genetic variation. Trends Ecol. Evol., 23: 38-44.
16. Barrett, R.D.H., Rogers, S.M. and Schluter, D. 2008. Natural selection on a major armor gene in threespine stickleback. Science, 322: 255-257.
17. Barrett, R.D.H., Rogers, S.M. and Schluter, D. 2009. Environment specific pleiotropy facilitates divergence at the ectodysplasin locus in threespine stickleback. Evolution, 63: 2831-2837.
18. Barrett, R.D.H., Paccard, A., Healy, T.M., Bergek, S., Schulte, P.M., Schluter, D. et al. 2011. Rapid evolution of cold tolerance in stickleback. Proc. R. Soc. Lond. B, 278: 233-238.
19. Baumgartner, J.V. and Bell, M.A. 1984. Lateral plate morph variation in California populations of the threespine stickleback, Gasterosteus aculeatus. Evolution, 38: 665-674.
20. Bell, M.A. 1976. Evolution of phenotypic diversity in the Gasterosteus aculeatus superspecies on the Pacific coast of North America. Syst. Zool., 25: 211-227.
21. Bell, M.A. 1981. Lateral plate polymorphism and ontogeny of the complete plate morph of threespine sticklebacks (Gasterosteus aculeatus). Evolution, 35: 67-74.
22. Bell, M.A. 1984. Evolutionary phenetics and genetics: the threespine stickleback, Gasterosteus aculeatus, and related species. In Evolutionary Genetics of Fishes (B.J. Turner, ed.), pp. 431-528. New York: Plenum.
23. Bell, M.A. 1987. Interacting evolutionary constraints in pelvic reduction of threespine sticklebacks, Gasterosteus aculeatus (Pisces: Gasterosteidae). Biol. J. Linn. Soc., 31: 347-382.
24. Bell, M.A. 1988. Bridging the gap between population biology and paleobiology in stickleback fishes. Trends Ecol. Evol., 3: 320-325.
25. Bell, M.A. 1995. Intraspecific systematics of Gasterosteus aculeatus populations: implications for behavioral ecology. Behaviour, 132: 1131-1152.
26. Bell, M.A. 2001. Lateral plate evolution in the threespine stickleback: getting nowhere fast. Genetica, 112/113: 445-461.
27. Bell, M.A. 2009. Implications of fossil threespine stickleback for Darwinian gradualism. J. Fish Biol., 75: 1977-1999.
28. Bell, M.A. and Foster, S.A. 1994. Introduction to the evolutionary biology of the threespine stickleback. In The Evolutionary Biology of the Threespine Stickleback (M.A. Bell and S.A. Foster, eds.), pp. 1-27. Oxford: Oxford University Press.
29. Bell, M.A. and Ortí, G. 1994. Pelvic reduction in threespine stickleback from Cook Inlet lakes: geographic distribution and intrapopulation variation. Copeia, 1994: 314-325. (Pubitemid 2085267)
30. Bell, M.A. and Reynolds, R.E. 2010. Miocene and Late Pleistocene stickleback spines from the Mojave Desert, California. In Overboard in the Mojave: 20 Million Years of Lakes and Wetlands (R.E. Reynolds and D.M. Miller, eds.), pp. 162-168. Fullerton, CA: Desert Studies, California State University Fullerton.
31. Bell, M.A., Ortí, G., Walker, J.A. and Koenings J.P. 1993. Evolution of pelvic reduction in threespine stickleback fish: a test of competing hypotheses. Evolution, 47: 906-914.
32. Bell, M.A., Aguirre, W.E. and Buck, N.J. 2004. Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution, 58: 814-824. (Pubitemid 38583870)
33. Bell, M.A., Stewart, J.D. and Park, P.J. 2009. The world's oldest fossil threespine stickleback. Copeia, 2009: 256-265.
34. Bell, M.A., Gangavalli, A., Bewick, A. and Aguirre, W.E. 2010. Frequency of Ectodysplasin alleles and limited introgression between sympatric threespine stickleback populations. Environ. Biol. Fish., 89: 189-198.
35. Berner, D., Kaeuffer, R., Grandchamp, A.-C., Raeymaekers, J.A.M., Räsänen, K. and Hendry, A.P. 2011. Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotypic pair: implications for reproductive isolation. J. Evol. Biol., 24: 1975-1983.
36. Betancur-R, R., Broughton, R.E., Wiley, E.O., Carpenter, K., López, J.A., Li, C. et al. 2013. The tree of life and a new classification of bony fishes. PLOS Currents Tree of Life. Apr 18 [last modified: 2013 Apr 20]. Edition 1 (DOI: 10.1371/currents.tol. 53ba26640df0ccaee75bb165c8c26288).
37. Candolin, U. 2009. Population responses to anthropogenic disturbance: lessons from three-spined sticklebacks Gasterosteus aculeatus in eutrophic habitats. J. Fish Biol., 75: 2108-2121.
38. Chan, Y.F., Marks, M.E., Jones, F.C., Villarreal, G. Jr., Shapiro, M.D., Brady, S.D. et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science, 327: 302-305.
39. Colosimo, P.F., Peichel, C.L., Nereng, K., Blackman, B.K., Shapiro, M.D., Schluter, D. et al. 2004. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol., 2: 635-641.
40. Colosimo, P.F., Hosemann, K.E., Balabhadra, S., Villarreal, G., Dickson, M., Grimwood, J. et al. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science, 307: 1928-1933. (Pubitemid 40404697)
41. Connor, J.K. and Hartl, D.L. 2004. A Primer of Ecological Genetics. Sunderland, MA: Sinauer Associates.
42. Conte, G.L., Arnegard, M.E., Peichel, C.L. and Schluter, D. 2012. The probability of genetic parallelism and convergence in natural populations. Proc. R. Soc. Lond. B, 279: 5039-5047.
43. Cresko, W.A., Amores, A., Wilson, C., Murphy, J., Currey, M., Phillips, P. et al. 2004. The genetic basis of recurrent evolution: armor loss in Alaskan populations of threespine stickleback, Gasterosteus aculeatus. Proc. Natl. Acad. Sci. USA, 101: 6050-6055. (Pubitemid 38520526)
44. Darwin, C.R. 1859. The Origin of Species by Means of Natural Selection, or Preservation of Favoured Races in the Struggle for Life (Avenal 1979 reprint of the first edition.) New York: Avenal Books.
45. Darwin, C.R. 1861/1994. Letter from C.R. Darwin to H. Fawcett, 18 September 1861. In The Complete Correspondence of Charles Darwin, Vol. 9. (F. Burkhardt, J. Harvey, D.M. Porter and M. Richmond, eds.), pp. 269-270. Cambridge: Cambridge University Press.
46. Day, T., Pritchard, J. and Schluter, D. 1994. Ecology and genetics of phenotypic plasticity: a comparison of two sticklebacks. Evolution, 48: 1723-1734.
47. Deagle, B., Jones, F.C., Chan, Y.F., Absher, D.M., Kingsley, D.M. and Reimchen, T.E. 2012. Population genomics of parallel phenotypic evolution in stickleback across stream-lake ecological transitions. Proc. R. Soc. Lond. B, 279: 1277-1286.
48. Deagle, B.E., Jones, F.C., Absher, D.M., Kingsley, D.M. and Reimchen, T.E. 2013. Phylogeography and adaptation genetics of stickleback from the Haida Gwaii archipelago revealed using genomewide single nucleotide polymorphism genotyping. Mol. Ecol., 22: 1917-1932.
49. DeFaveri, J., Shikano, T., Shimada, Y., Goto, A. and Merilä, J. 2011. Global analysis of genes involved in freshwater adaptation in threespine sticklebacks (Gasterosteus aculeatus). Evolution, 65: 1800-1807.
50. Diamond, J.M. 1974. Colonization of exploded volcanic islands by birds: the supertramp strategy. Science, 184: 803-806.
51. Dobzhansky, T. 1970. Genetics of the Evolutionary Process. New York: Columbia University Press.
52. Eldredge, N. and Gould, S.J. 1972. Punctuated equilibria: an alternative to phyletic gradualism. In Models in Paleobiology (T.J.M. Schopf, ed.), pp. 82-115. San Francisco, CA: Freeman Cooper.
53. Endler, J.A. 1986. Natural Selection in the Wild. Princeton, NJ: Princeton University Press.
54. Erwin, D.H. and Anstey, R.L., eds. 1995. New Approaches to Speciation in the Fossil Record. New York: Columbia University Press.
55. Feulner, P.G.D., Chain, F.J.J., Panchal, M., Eizaguirre, C., Kalbe, M., Lenz, T.L. et al. 2013. Genome-wide patterns of standing genetic variation in a marine population of three-spined sticklebacks. Mol. Ecol., 22: 635-649.
56. Francis, R.C., Havens, A.C. and Bell, M.A. 1985. Unusual lateral plate variation of threespine sticklebacks (Gasterosteus aculeatus) from Knik Lake, Alaska. Copeia, 1985: 619-624.
57. Furin, C.G., von Hippel, F.A. and Bell, M.A. 2012. Partial reproductive isolation of a recently derived resident-freshwater population of threespine stickleback (Gasterosteus aculeatus) from its putative anadromous ancestor. Evolution, 66: 3277-3286.
58. Gelmond, O., von Hippel, F.A. and Christy, M.S. 2009. Rapid ecological speciation in three-spined stickleback from Middleton Island, Alaska: the roles of selection and geographical isolation. J. Fish Biol., 75: 2037-2051.
59. Gienapp, P., Teplitsky, C., Alho, J.S. and Merilä, J. 2008. Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol., 17: 167-178. (Pubitemid 350292455)
60. Gingerich, P.D. 1983. Rates of evolution: effects of time and temporal scaling. Science, 222: 159-161. (Pubitemid 13008788)
61. Gingerich, P.D. 1993. Quantification and comparison of evolutionary rates. Am. J. Sci., 293A: 453-478.
62. Gingerich, P.D. 2001. Rates of evolution on the time scale of the evolutionary process. Genetica, 112/113: 127-144. (Pubitemid 34119657)
63. Gould, F. 2010. Applying evolutionary biology: from retrospective analysis to direct manipulation. In Evolution Since Darwin: The First 150 Years (M.A. Bell, D.J. Futuyma, W.F. Eanes and J.S. Levinton, eds.), pp. 591-621. Sunderland, MA: Sinauer Associates.
64. Gould, S.J. 2002. The Structure of Evolutionary Theory. Cambridge, MA: Harvard University Press.
65. Gregory, R.P.G. and Bradshaw, A.D. 1965. Heavy metal tolerance in populations of Agrostis tenuis Sibth. and other grasses. New Phytol., 64: 131-143.
66. Gross, H.P. and Anderson, J.M. 1984. Geographic variation in the gill rakers and diet of European threespine sticklebacks, Gasterosteus aculeatus. Copeia, 1984: 87-97.
67. Hagen, D.W. 1967. Isolating mechanisms in threespine sticklebacks (Gasterosteus). J. Fish. Res. Board Can., 24: 1637-1692.
68. Hagen, D.W. 1973. Inheritance of numbers of lateral plates and gill rakers in Gasterosteus aculeatus. Heredity, 30: 303-312.
69. Hagen, D.W. and Gilbertson, L.G. 1972. Geographic variation and environmental selection in Gasterosteus aculeatus L. in the Pacific Northwest, America. Evolution, 26: 32-51.
70. Hagen, D.W. and Gilbertson, L.G. 1973a. The genetics of plate morphs in freshwater threeespine sticklebacks. Heredity, 31: 75-84.
71. Hagen, D.W. and Gilbertson, L.G. 1973b. Selective predation and the intensity of selection acting upon the lateral plates of threespine sticklebacks. Heredity, 30: 273-287.
72. Hagen, D.W. and McPhail, J.D. 1970. The species problem within Gasterosteus aculeatus on the Pacific coast of North America. J. Fish. Res. Board Can., 27: 147-155.
73. Hagen, D.W. and Moodie, G.E.E. 1982. Polymorphism for plate morphs in Gasterosteus aculeatus on the east coast of Canada and an hypothesis for their global distribution. Can. J. Zool., 60: 1032-1042. (Pubitemid 13282105)
74. Haldane, J.B.S. 1949. Suggestions as to quantitative measurement of rates of evolution. Evolution, 3: 51-56.
75. Haldane, J.B.S. 1957. The cost of natural selection. Genetics, 55: 511-524.
76. Hansen, N.R. 1969. Perception and Discovery. San Francisco, CA: Freeman, Cooper.
77. Hay, D.E. and McPhail, J.D. 1975. Mate selection in three-spine sticklebacks. Can. J. Zool., 53: 441-450.
78. Hendry, A.P. and Kinnison, M.T. 1999. The pace of modern life: measuring rates of contemporary microevolution. Evolution, 53: 1637-1653. (Pubitemid 30044800)
79. Hendry, A.P., Farrugia, T.J. and Kinnison, M.T. 2008. Human influences on rates of phenotypic change in wild animal populations. Mol. Ecol., 17: 20-29. (Pubitemid 350292459)
80. Hendry, A.P., Hendry, A.S. and Hendry, C.A. 2013a. Hendry Vineyard stickleback: testing for contemporary lake-stream divergence. Evol. Ecol. Res., 15: 343-359.
81. Hendry, A.P., Peichel, C.L., Matthews, B., Boughman, J.W. and Nosil, P. 2013b. Stickleback research: the now and the next. Evol. Ecol. Res., 15: 111-141.
82. Hermida, M., Fernández, C., Amaro, R. and San Miguel, E. 2002. Heritability and 'evolvability' of meristic characters in a natural population of Gasterosteus aculeatus. Can. J. Zool., 80: 532-541. (Pubitemid 34519716)
83. Heuts, M.J. 1947a. The phenotypical variability of Gasterosteus aculeatus (L.) populations in Belgium: its bearing on the general geographical variation of the species. Verh. K. Vlaam. Acad. Wet. Lett. Schone Kunsten Belgie Kl. Wet., 9: 1-63.
84. Heuts, M.J. 1947b. Experimental studies on adaptive evolution in Gasterosteus aculeatus L. Evolution, 1: 89-102.
85. Hohenlohe, P.A., Bassham, S., Etter, P.D., Stiffler, N., Johnson, E.A. and Cresko, W.A. 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Gene, 6: e1000862.
86. Hohenlohe, P.A., Bassham, S., Currey, M. and Cresko, W.A. 2012. Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes. Phil. Trans. R. Soc. Lond. B, 367: 395-408.
87. Hunt, G., Bell, M.A. and Travis, M.P. 2008. Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage. Evolution, 62: 700-710. (Pubitemid 351348254)
88. Ishikawa, M. and Mori, S. 2000. Mating success and male courtship behaviors in three populations of the threespine stickleback. Behaviour, 137: 1065-1080.
89. Jones, F., Brown, C., Pemberton, J. and Braithwaite, V. 2006. Reproductive isolation in a threespine stickleback hybrid zone. J. Evol. Biol., 19: 1531-1544.
90. Jones, F.C., Chan, Y.F., Schmutx, J., Grimwood, J., Brady, S.D., Southwick, A.M. et al. 2012a. A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Curr. Biol., 22: 83-90.
91. Jones, F.C., Grabherr, M.G., Chan, Y.F., Russell, P., Mauceli, E., Johnson, J. et al. 2012b. The genomic basis of adaptive evolution in threespine sticklebacks. Nature, 484: 55-61.
92. Karve, A.D., von Hippel, F.A. and Bell, M.A. 2007. Isolation between sympatric anadromous and resident threespine stickleback species in Mud Lake, Alaska. Environ. Biol. Fish., 81: 287-296.
93. Kawahara, R., Miya, M., Mabuchi, K., Near, T.J. and Nishida, M. 2009. Stickleback phylogenies resolved: evidence from mitochondrial genomes and 11 nuclear genes. Mol. Phylogenet. Evol., 50: 401-404.
94. Kettlewell, H.B.D. 1973. The Evolution of Melanism. Oxford: Clarendon Press.
95. Kirkpatrick, M. 2010. Rates of adaptation: why is Darwin's machine so slow? In Evolution Since Darwin: The First 150 Years (M.A. Bell, D.J. Futuyma, W.F. Eanes and J.S. Levinton, eds.), pp. 177-195. Sunderland, MA: Sinauer Associates.
96. Kitano, J., Bolnick, D.I., Beauchamp, D.A., Mazur, M.M., Mori, S., Nakano, T. et al. 2008. Reverse evolution of armor plates in the threespine stickleback. Curr. Biol., 18: 769-774.
97. Kitano, J., Lema, S.C., Luckenbach, J.A., Mori, S., Yui, K., Swanson, P. et al. 2010. Adaptive divergence of the thyroid hormone signaling pathway in the stickleback radiation. Curr. Biol., 20: 2124-2130.
98. Klepaker, T. 1993. Morphological changes in a marine population of threespined stickleback, Gasterosteus aculeatus, recently isolated in fresh water. Can. J. Zool., 71: 1231-1258.
99. Klepaker, T. 1996. Lateral plate polymorphism in marine and estuarine populations of the threespine stickleback (Gasterosteus aculeatus) along the coast of Norway. Copeia, 14: 120-127.
100. Klepaker, T., Østbye, K. and Bell, M.A. 2013. Regressive evolution of the pelvic complex in stickleback fishes: a study of convergent evolution. Evol. Ecol. Res., 15: 413-435.
101. Kraak, S.B.M., Mundwiler, B. and Hart, P.J.B. 2001. Increased number of hybrids between benthic and limnetic three-spined sticklebacks in Enos Lake, Canada: the collapse of a species pair? J. Fish Biol., 58: 1458-1464. (Pubitemid 32546023)
102. Kristjánsson, B.K. 2005. Rapid morphological changes in threespine stickleback, Gasterosteus aculeatus, in freshwater. Environ. Biol. Fish., 74: 357-363. (Pubitemid 41740009)
103. Kristjánsson, B.K., Skúlason, S. and Noakes, D.L.G. 2002. Rapid divergence in a recently isolated population of threespine stickleback (Gasterosteus aculeatus L.). Evol. Ecol. Res., 4: 1-14.
104. Kristjánsson, B.K., Skúlason, S. and Noakes, D.L.G. 2004. Unusual number of pectoral fin rays in an Icelandic population of threespine stickleback (Gasterosteus aculeatus) recently isolated in freshwater. Evol. Ecol., 18: 379-384. (Pubitemid 40607589)
105. Lavin, P.A. and McPhail, J.D. 1985. The evolution of freshwater diversity in threespine stickleback (Gasterosteus aculeatus): site-specific differentiation of trophic morphology. Can. J. Zool., 63: 2632-2638. (Pubitemid 17247291)
106. Leaver, S.D. and Reimchen, T.E. 2012. Abrupt changes in defense and trophic morphology of the giant threespine stickleback (Gasterosteus sp.) following colonization of a vacant habitat. Biol. J. Linn. Soc., 107: 494-509.
107. Leinonen, T., Cano, J.M., Mäkinen, H. and Merilä, J. 2006. Contrasting patterns of body shape and neutral genetic divergence in marine and lake populations of threespine sticklebacks. J. Evol. Biol., 19: 1803-1812. (Pubitemid 44571619)
108. Leinonen, T., McCairns, R.J.S., Herczeg, G. and Merilä, J. 2012. Decreased lateral plate coverage in freshwater threespine sticklebacks. Evolution, 66: 3866-3875.
109. Le Rouzic, A., Østbye, K., Klepaker, T.O., Hansen, T.F., Bernatchez, L., Schluter, D. et al. 2011. Strong and consistent natural selection associated with armor reduction in sticklebacks. Mol. Ecol., 20: 2483-2493.
110. Lind, E.E. and Grahn, M. 2011. Directional genetic selection by pulp mill effluent on multiple natural populations of three-spined stickleback (Gasterosteus aculeatus) Ecotoxicology, 20: 503-512.
111. Lindsey, C.C. 1962. Experimental study of meristic variation in a population of threespine stickleback, Gasterosteus aculeatus. Can. J. Zool., 40: 271-312.
112. Lucek, K., Haesler, M.P. and Sivasundar, A. 2012. When phenotypes do not match genotypes - unexpected phenotypic diversity and potential environmental constraints in Icelandic stickleback. J. Hered., 103: 579-584.
113. Majerus, M.E.N. 1998. Melanism: Evolution in Action. Oxford: Oxford University Press.
114. Majerus, M.E.N. 2009. Industrial melanism in the peppered moth, Biston betularia: an excellent teaching example of Darwinian evolution in action. Evol. Educ. Outreach, 2: 63-74.
115. Mäkinen, H.S., Cano, J.M. and Merilä, J. 2006. Genetic relationships among marine and freshwater populations of the European three-spined stickleback (Gasterosteus aculeatus) revealed by microsatellites. Mol. Ecol., 15: 1519-1534.
116. McGuigan, K., Nishimura, N., Currey, M., Hurwit, D. and Cresko, W.A. 2010. Cryptic genetic variation and body size evolution in threespine stickleback. Evolution, 65: 1203-1211.
117. McKinnon, J.S., Mori, S., Blackman, B.K., David, L., Kingsley, D.M., Jamieson, L. et al. 2004. Evidence for ecology's role in speciation. Nature, 429: 294-298. (Pubitemid 38691086)
118. McNeilly, T. 1968. Evolution in closely adjacent plant populations. III. Agrostis tenuis on a small copper mine. Heredity, 23: 99-108.
119. McPhail, J.D. 1994. Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of south-western British Columbia. In The Evolutionary Biology of the Threespine Stickleback (M.A. Bell and S.A. Foster, eds.), pp. 1-27. Oxford: Oxford University Press.
120. McPhail, J.D. and Lindsey, C.C. 1970. Freshwater fishes of northwestern Canada and Alaska. Bull. Fish. Res. Board Can., 173: 1-381.
121. Michel, A.P., Sim, S., Powell, T.H.Q., Taylor, M.S., Nosil, P. and Feder, J.L. 2010. Widespread genomic divergence during sympatric speciation. Proc. Natl. Acad. Sci. USA, 107: 9724-9729.
122. Miller, C.T., Beleza, S., Pollen, A.A., Schluter, D., Kittles, R.A., Shriver, M.D. et al. 2007. cis-Regulatory changes in Kit Ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell, 131: 1179-1189. (Pubitemid 350235026)
123. Miller, R.R. and Hubbs, C.L. 1969. Systematics of Gasterosteus aculeatus, with particular reference to intergradation and introgression along the Pacific coast of North America: a commentary on a recent contribution. Copeia, 1969: 52-69.
124. Moodie, G.E.E. and Reimchen, T.E. 1976. Phenotypic variation and habitat differences in Gasterosteus populations of the Queen Charlotte Islands. Syst. Zool., 25: 49-61.
125. Münzing, J. 1963. The evolution of variation and distributional patterns in European populations of the three-spined stickleback, Gasterosteus aculeatus. Evolution, 17: 320-332.
126. Nagel, L. and Schluter, D. 1998. Body size, natural selection, and speciation in sticklebacks. Evolution, 52: 209-218. (Pubitemid 28195160)
127. Nosil, P. and Feder, J.L. 2012. Genomic divergence during speciation: causes and consequences. Phil. Trans. R. Soc. Lond. B, 367: 332-342.
128. Olafsdóttir, G.A. 2004. Population divergence and speciation in Icelandic threespine stickleback (Gasterosteus aculeatus). PhD thesis, University of St. Andrews, St. Andrews, UK. [Not seen, cited in Kristjánsson, B.K. (2005).]
129. Otto, S.P. and Whitlock, M.C. 1997. The probability of fixation in populations of changing size. Genetics, 146: 723-733. (Pubitemid 27251408)
130. Pigliucci, M. and Preston, K.A. 2004. Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes. New York: Oxford University Press.
131. Ravinet, M., Prodöhl, P.A. and Harrod, C. 2013. On Irish sticklebacks: morphological diversification in a secondary contact zone. Evol. Ecol. Res., 15: 271-294.
132. Reimchen, T.E. 1995. Predator-induced cyclical changes in lateral plate frequencies of Gasterosteus. Behaviour, 132: 1079-1094.
133. Reimchen, T.E. and Nosil, P. 2002. Temporal variation in divergent selection on spine number in threespine stickleback. Evolution, 56: 2472-2483. (Pubitemid 36108562)
134. Reimchen, T.E., Stinson, E.M. and Nelson, J.S. 1985. Multivariate differentiation of parapatric and allopatric populations of threespine stickleback in the Sangan River watershed, Queen Charlotte Islands. Can. J. Zool., 63: 2944-2951.
135. Reimchen, T.E., Bergstrom, C. and Nosil, P. 2013. Natural selection and the adaptive radiation of Haida Gwaii stickleback. Evol. Ecol. Res., 15: 241-269.
136. Ricklefs, R.E. and Bermingham, E. 2002. The concept of the taxon cycle in biogeography. Global. Ecol. Biogeogr., 11: 353-361. (Pubitemid 44769604)
137. Roesti, R., Hendry, A.P., Salzburger, W. and Berner, D. 2012. Genome divergence during evolutionary diversification as revealed in replicate lake-stream stickleback population pairs. Mol. Ecol., 21: 2852-2862.
138. Roesti, R., Moser, D. and Berner, D. 2013. Recombination in the threespine stickleback genome: patterns and consequences. Mol. Ecol., 22: 3014-3027.
139. Roughgarden, J. 1996. The Theory of Population Genetics and Evolutionary Ecology: An Introduction. Upper Saddle River, NJ: Prentice-Hall.
140. Schindel, D.E. 1980. Microstratigraphic sampling and the limits of paleontologic resolution. Paleobiology. 6: 408-426. (Pubitemid 11273321)
141. Schluter, D. and Conte, G.L. 2009. Genetics and ecological speciation. Proc. Natl. Acad. Sci. USA, 106: 9955-9962.
142. Schluter, D., Clifford, E.A., Nemethy, M. and McKinnon, J.S. 2004. Parallel evolution and inheritance of quantitative traits. Am. Nat., 163: 809-822. (Pubitemid 38852136)
143. Seehausen, O. 2004. Hybridization and adaptive radiation. Trends Ecol. Evol., 19: 198-207. (Pubitemid 38355799)
144. Shapiro, M.D., Marks, M.E., Peichel, C.L., Blackman, B.K., Nereng, K.S., Johnsson, B. et al. 2004. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature, 428: 717-723. (Pubitemid 38508276)
145. Sharpe, D.M.T., Räsänen, K., Berner, D. and Hendry, A.P. 2008. Genetic and environmental contributions to the morphology of lake and stream stickleback: implications for gene flow and reproductive isolation. Evol. Ecol. Res., 10: 849-866.
146. Shimada, Y., Shikano, T. and Merilä, J. 2011. A high incidence of selection on physiologically important genes in the three-spined stickleback, Gasterosteus aculeatus. Mol. Biol. Evol., 28: 181-193.
147. Slatkin, M. 2008. Linkage disequilibrium - understanding the evolutionary past and mapping the medical future. Nature Rev. Genet., 9: 477-485. (Pubitemid 351693977)
148. Sokal, R.R. and Rohlf, F.J. 2012. Biometry, 4th edn. New York: W.H. Freeman.
149. Spoljaric, M.A. and Reimchen, T.E. 2007. 10,000 years later: evolution of body shape in Haida Gwaii threespine stickleback. J. Fish Biol., 70: 1484-1503. (Pubitemid 46642890)
150. SPSS, Inc. 1998. SPSS for Windows, release 9.0. Cary, NC: SPSS, Inc.
151. Stockwell, C.A., Hendry, A.P. and Kinnison, M.T. 2003. Contemporary evolution meets conservation biology. Trends. Ecol. Evol., 18: 94-101. (Pubitemid 36072684)
152. Swain, D.P. 1992a. The functional basis of natural selection for vertebral traits of larvae in the stickleback Gasterosteus aculeatus. Evolution, 46: 987-997.
153. Swain, D.P. 1992b. Selective predation for vertebral phenotype in Gasterosteus aculeatus: reversal in the direction of selection at different larval sizes. Evolution, 46: 987-997.
154. Taylor, E.B. and McPhail, J.D. 1999. Evolutionary history of an adaptive radiation in species pairs of threespine sticklebacks (Gasterosteus): insights from mitochondrial DNA. Biol. J. Linn. Soc., 66: 271-291. (Pubitemid 29157981)
155. Taylor, E.B. and McPhail, J.D. 2000. Historical contingency and determinism interact to prime speciation in sticklebacks. Proc. R. Soc. Lond, B, 271: 2375-2384. (Pubitemid 32001478)
156. Teotónio, H., Chelo, I.M., Bradic, M., Rose, M.R. and Long, A.D. 2009. Experimental evolution reveals natural selection on standing genetic variation. Nature Genet., 41: 251-257.
157. Tuomainen, U., Sylvin, E. and Candolin, U. 2011. Adaptive phenotypic differentiation of courtship in response to recent anthropogenic disturbance. Evol. Ecol. Res., 13: 697-710.
158. Vamosi, S.M. 2006. Contemporary evolution of armor and body size in a recently introduced population of threespine stickleback Gasterosteus aculeatus. Acta Zool. Sinica, 52: 482-490.
159. Walker, J.A. 1997. Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L (Gasterosteidae) body shape. Biol. J. Linn. Soc., 61: 3-50. (Pubitemid 27274764)
160. Walker, J.A. and Bell, M.A. 2000. Net evolutionary trajectories of body shape evolution within a microgeographic radiation of threespine sticklebacks (Gasterosteus aculeatus). J. Zool., Lond., 252: 293-302.
161. Wallace, A.R. 1891. Darwinism: An Exposition of the Theory of Natural Selection, with Some of its Applications. London: Macmillan.
162. West-Eberhard, M.J. 2003. Developmental Plasticity and Evolution. New York: Oxford University Press.
163. Williams, G.C. 1992. Natural Selection: Domains, Levels, and Applications. Oxford: Oxford University Press.
164. Wilson, E.O. 1961. The nature of the taxon cycle in the Melanesian ant fauna. Am. Nat., 95: 169-193.
165. Withler, R.E. and McPhail, J.D. 1985. Genetic variability in freshwater and anadromous sticklebacks (Gasterosteus aculeatus) of southern British Columbia. Can. J. Zool., 63: 528-533.
166. Wund, M.A., Baker, J.A., Clancy, B., Golub, J.L. and Foster, S.A. 2008. A test of the 'flexible stem' model of evolution: ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. Am. Nat., 172: 449-462.
167. Ziuganov, V.V. 1995. Reproductive isolation among lateral plate phenotypes (low, partial, complete) of the threespine stickleback, Gasterosteus aculeatus, from the White Sea basin and the Kamchatka Peninsula, Russia. Behaviour, 132: 1173-1181. (Pubitemid 26454324)