Natural selection and the adaptive radiation of Haida Gwaii stickleback

Evolutionary Ecology Research

Volumn 15, Issue 3, 2013, Pages 241-269

  Reimchen, Thomas E ^a   Bergstrom, Carolyn ^a,b   Nosil, Patrik ^a,c  

^a UNIVERSITY OF VICTORIA   (Canada)

^b UNIVERSITY OF ALASKA SOUTHEAST   (United States)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Body size; Canadian Galapagos; Dystrophic lakes; Morphological variability; Predator prey defences; Queen Charlotte Islands; Stickleback

Indexed keywords

EID: 84879618489     PISSN: 15220613     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (127)

1. Baker, J.A. 1994. Life history variation in female threespine stickleback. In The Evolutionary Biology of the Threespine Stickleback (M.A. Bell and SA. Foster, eds.), pp. 144-187. New York: Oxford University Press.
2. Baldwin, B.G. and Sanderson, M.J. 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl. Acad. Sci. USA, 95: 9402-9406.
3. 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.
4. 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.
5. Barrett, R.D.H., Rogers, S.M. and Schluter, D. 2009a. Environment specific pleiotropy facilitates divergence at the ectodysplasin locus in threespine stickleback. Evolution, 63: 2831-2837.
6. Barrett, R.D.H., Vines, T.H., Bystriansky, J.S. and Schulte, P.M. 2009b. Should I stay or should I go? The ectodysplasin locus is associated with behavioural differences in threespine stickleback. Biol. Lett., 5: 788-791.
7. Bell, MA. 1977. Late Miocene marine threespine stickleback, Gasterosteus aculeatus aculeatus, and its zoogeographic and evolutionary significance. Copeia, 1977: 277-282.
8. Bell, MA. and Aguirre, WE. 2013. Contemporary evolution, allelic recycling, and adaptive radiation of the threespine stickleback. Evol. Ecol. Res., 15: 377-411.
9. Bell, MA. and Foster, SA. 1994. Introduction to the evolutionary biology of the threespine stickle-back. In The Evolutionary Biology of the Threespine Stickleback (MA. Bell and SA. Foster, eds.), pp 1-27. New York: Oxford University Press.
10. Bell, MA., Orti, G., Walker, J.A. and Koenings, J.P. 1993. Evolution of pelvic reduction in three-spine stickleback fish-a test of competing hypotheses. Evolution, 47: 906-914.
11. Bell, M.A., Aguirre, WE. and Buck, N.J. 2004. Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution, 58: 814-824.
12. Bergstrom, C.A. 2002. Fast-start swimming performance and reduction in lateral plate number in threespine stickleback. Can. J. Zool., 80: 207-213.
13. Bergstrom, C.A. and Reimchen, T.E. 2000. Functional implications of fluctuating asymmetry among endemic populations of Gasterosteus aculeatus. Behaviour, 137: 1097-1112.
14. Bergstrom, C.A. and Reimchen, T.E. 2002. Geographical variation in asymmetry in Gasterosteus aculeatus. Biol. J. Linn. Soc., 77: 9-22.
15. Bergstrom, C.A. and Reimchen, T.E. 2005. Habitat-dependent associations between parasitism and fluctuating asymmetry among endemic stickleback populations. J. Evol. Biol., 18: 939-948.
16. Blanckenhorn, W.U. 2000. The evolution of body size: what keeps organisms small? Q. Rev. Biol., 75: 385-407.
17. Bourgeois, J.F., Blouw, D.M., Koenings, J.P and Bell, M.A. 1994. Multivariate analysis of geographic covariance between phenotypes and environments in the threespine stickleback, Gasterosteus aculeatus, from the Cook Inlet area, Alaska. Can. J. Zool., 72: 1497-1509.
18. Brett, J.R. and Groves, T.D.D. 1979. Physiological energetics. In Fish Physiology, Vol. 8 (W.S. Hoar, D.J. Randall and J.R. Brett, eds.), pp. 279-352. New York: Academic Press.
19. Burnham, K.P. and Anderson, D.R. 2002. Model Selection and Multi-model Inference: A Practical Information-theoretic Approach, 2nd edn. New York: Springer-Verlag.
20. Byun, S.A., Koop, B.F. and Reimchen, T.E. 1997. North American black bear mtDNA phylo-geography: implications for morphology and the Haida Gwaii glacial refugium controversy Evolution, 51: 1647-1653.
21. Carpenter, S.R. and Pace, M.L. 1997. Dystrophy and eutrophy in lake ecosystems: implications of fluctuating inputs. Oikos, 78: 3-14.
22. Chan, Y.F., Marks, M.E., Jones, F.C., Villarreal, G., 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.
23. 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.
24. Deagle, B.E., Reimchen, T.E. and Levin, D.B. 1996. Origins of endemic stickleback from the Queen Charlotte Islands: mitochondrial and morphological evidence. Can. J. Zool., 74: 1045-1056.
25. Deagle, B.E., Jones, F.C., Chan, Y.F., Absher, D.B., 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.
26. Deagle, B.E., Jones, F.C., Absher, D.B., Kingsley, D.M. and Reimchen, T.E. 2013. Phylogeography and adaptation genetics of stickleback from the Haida Gwaii archipelago revealed using genome-wide single nucleotide polymorphism genotyping. Mol. Ecol., 22: 1917-1932.
27. Douglas, S.D. and Reimchen, T.E. 1988. Habitat characteristics and population estimates of breeding Red-throated Loons, Gavia stellata, on the Queen Charlotte Islands, British Columbia. Can. Field Nat., 102: 679-684.
28. Fladmark, K.R. 1979. Alternate migration corridors for early man in North America. Am. Antiquity, 44: 55-69.
29. Frommen, J.G., Herder, F., Engqvist, L., Mehlis, M., Bakker, T.C.M., Schwarzer, J. et al. 2011. Costly plastic morphological responses to predator specific odour cues in three-spined stickle-backs (Gasterosteus aculeatus). Evol. Ecol., 25: 641-656.
30. Gambling, S.J. and Reimchen, T.E. 2012. Prolonged life span among endemic Gasterosteus populations. Can. J. Zool., 90: 284-290.
31. Gavrilets, S. and Losos, J.B. 2009. Adaptive radiation: contrasting theory with data. Science, 323: 732-737.
32. Giles, N. 1983. The possible role of environmental calcium levels during the evolution of phenotypic diversity in the Outer Hebridean population of the threespine stickleback. J. Zool., Lond., 199: 535-544.
33. Giles, N. and Huntingford, FA. 1984. Predation risk and inter-population variation in antipredator behavior in the three-spined stickleback, Gasterosteus aculeatus L. Anim. Behav., 32: 264-275.
34. Godin, J.G.J. and Clark, K.A.V. 1997. Risk-taking in stickleback fishes faced with different predatory threats. Ecoscience, 4: 246-251.
35. Gould, S.J. 1984. Covariance sets and ordered geographic variation in Cerion from Aruba, Bonaire and Curacao: A way of studying nonadaptation. Syst. Zool., 33: 217-237.
36. Grant, B.R. and Grant, P.R. 2008. Fission and fusion of Darwin's finches populations. Phil. Trans. R. Soc. Lond. B, 363: 2821-2829.
37. Grant, PR and Grant, B.R. 2002. Adaptive radiation of Darwin's finches. Am. Sci., 90: 130-139.
38. Gross, H.P. 1977. Adaptive trends of environmentally sensitive traits in three-spined stickleback, Gasterosteus aculeatus L. J. Zool. Syst. Evol. Res., 15: 252-278.
39. Gross, H.P. 1978. Natural selection by predators on the defensive apparatus of the three-spined stickleback Gasterosteus aculeatus L. Can. J. Zool., 56: 398-413.
40. Hagen, D.W and Gilbertson, L.G. 1972. Geographic variation and environmental selection in Gasterosteus aculeatus L in Pacific Northwest, America. Evolution, 26: 32-51.
41. 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.
42. Heins, D.C. and Baker, J.A. 2008. The stickleback-Schistocephalus host-parasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour, 145: 625-645.
43. Hendry, A.P., Hudson, K., Walker, J.A., Räsänen, K. and Chapman, L. 2011. Genetic divergence in morphology-performance mapping between Misty Lake and inlet stickleback. J. Evol. Biol., 24: 23-35.
44. Heuts, M.J. 1947. Experimental studies on adaptive evolution in Gasterosteus aculeatus L. Evolution, 1: 89-102.
45. 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 Genet., 6: e11000862.
46. Hoogland, R.D.D., Morris, D. and Tinbergen, N. 1957. The spines of sticklebacks (Gasterosteus and Pygosteus) as a means of defence against predators (Perca and Esox). Behavior, 10: 205-237.
47. Jones, F.C., Chan, YF., Schmutz, J., Grimwood, J., Brady, S.D., Southwick, A.M. et al. 2012a. A genome-wide SNP genotyping array reveals patterns of global and species pair divergence in sticklebacks. Curr. Biol., 22: 83-90.
48. Jones, F.C., Grabherr, M.G., Chan, YF., Russell, P., Mauceli, E., Johnson, J. et al. 2012b. The genomic basis of adaptive evolution in threespine sticklebacks. Nature, 484: 55-61.
49. Josenhans, H.W., Fedje, D.W., Conway, K.W. and Barrie, J.V. 1995. Post glacial sea levels on the Western Canadian continental shelf: evidence for rapid change, extensive subaerial exposure, and early human habitation. Mar. Geol., 125: 73-94.
50. 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.
51. 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.
52. Kolbe, J.J., Leal, M., Schoener, T.W., Spiller, D.A. and Losos, J.B. 2012. Founder effects persist despite adaptive differentiation: a field experiment with lizards. Science, 335: 1086-1089.
53. Langerhans, R.B., Layman, C.A., Shokrollahi, A.M. and DeWitt, T.J. 2004. Predator-driven pheno-typic diversification in Gambusia affinis Evolution, 58: 2305-2318.
54. Langerhans, R.B., Gifford, M.E. and Joseph, E.O. 2007. Ecological speciation in Gambusia fishes. Evolution, 61: 2056-2074.
55. Law, T.C. and Blake, R.W. 1996. Comparison of the fast-start performances of closely related, morphologically distinct threespine sticklebacks (Gasterosteus spp.). J. Exp. Biol., 199: 2595-2604.
56. 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: 495-509.
57. Leinonen, T., Herczeg, G., Cano, J.M. and Merila, J. 2012. Predation-imposed selection on threespine stickleback (Gasterosteus aculeatus) morphology: a test of the refuge use hypothesis. Evolution, 65: 2916-2926.
58. Le Rouzic, A., Ostbye, K., Klepaker, T.O., Hansen, T.F., Bernatchez, L., Schluter, D. et al. 2011. Strong and consistent natural selection associated with armour reduction in sticklebacks. Mol. Ecol., 20: 2483-2493.
59. Losos, J.B. 2009. Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles. Berkeley, CA: University of California Press.
60. Losos, J.B., Jackman, T.R., Larson, A., de Queiroz, K. and Rodriguez-Schettino, L. 1998. Contingency and determinism in replicated adaptive radiations of island lizards. Science, 279: 2115-2118.
61. Lucek, K., Haesler, M.P. and Sivasundar, A. 2012. When phenotypes do not match genotypes-unexpected phenotypic diversity and potential environmental constraints in Icelandic stickle-back. J. Hered., 103: 579-584.
62. 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.
63. Maccoll, A.D., Nagar, A.E. and de Roij, J. 2013. The evolutionary ecology of dwarfism in three-spined sticklebacks. J. Anim. Ecol., 82: 642-652.
64. Magurran, A.E., Seghers, B.H., Shaw, P.W. and Carvalho, G.R. 1995. The behavioral diversity and evolution of guppy, Poecilia reticulata populations in Trinidad. Adv. Study Behav., 24: 155-202.
65. Manly, B.F.J. 1997. Randomization, Bootstrap and Monte Carlo Methods in Biology, 2nd edn. New York: Chapman & Hall.
66. Marchinko, K.B. 2008. Predation's role in repeated phenotypic and genetic divergence of armor in threespine stickleback. Evolution, 63: 127-138.
67. Marchinko, K.B. and Schluter, D. 2007. Parallel evolution by correlated response: lateral plate reduction in threespine stickleback. Evolution, 61: 1084-1090.
68. Meyer, A. 1993. Phylogenetic relationships and evolutionary processes in East African cichlid fishes. Trends Ecol. Evol., 8: 279-284.
69. 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, 1: 52-69.
70. Moodie, G.E.E. 1972a. Predation, natural selection and adaptation in an unusual threespine stickle-back. Heredity, 28: 155-167.
71. Moodie, G.E.E. 1972b. Morphology, life history, and ecology of an unusual stickleback (Gasterosteus aculeatus) in the Queen Charlotte Islands, Canada. Can. J. Zool., 50: 721-732.
72. Moodie, G.E.E. and Reimchen, T.E. 1976. Phenetic variation and habitat differences in Gasterosteus populations of Queen Charlotte Islands. Syst. Zool., 25: 49-61.
73. Mori, S. and Takamura, N. 2004. Changes in morphological characteristics of an introduced population of the threespine stickleback Gasterosteus aculeatus in Lake Towada, northern Japan. Ichthyol. Res., 51: 295-300.
74. Myhre, F. and Klepaker, T. 2009. Body armour and lateral-plate reduction in freshwater three-spined stickleback Gasterosteus aculeatus: adaptations to a different buoyancy regime? J. Fish Biol., 75: 2062-2074.
75. Nelson, J.S. 1969. Geographic variation in the brook stickleback, Culaea inconstans, and notes on nomenclature and distribution. J. Fish. Res. Board Can., 26: 2431-2447.
76. Nilsson, S.G. and Nilsson, I.N. 1976. Numbers, food consumption and fish predation by birds in Lake Mockeln, southern Sweden. Ornis Scand., 7: 61-70.
77. Noor, M.A.F. and Feder, J.L. 2006. Speciation genetics: evolving approaches. Nature Rev. Genet., 7: 851-861.
78. Nosil, P. and Feder, J.L. 2012. Genomic divergence during speciation: causes and consequences. Phil. Trans. R. Soc. Lond. B, 367: 332-342.
79. O'Reilly, P., Reimchen, T.E., Beech, R. and Strobeck, C. 1993. Mitochondrial DNA in Gasterosteus and Pleistocene glacial refugium on the Queen Charlotte Islands, British Columbia. Evolution, 47: 678-684.
80. Orti, G., Bell, M.A., Reimchen, T.E. and Meyer, A. 1994. Global survey of mitochondrial DNA sequences in the threespine stickleback-evidence for recent migrations. Evolution, 48: 608-622.
81. Peichel, C.L., Nereng, K.S., Ohgi, K.A., Cole, B.L.E., Colosimo, P.F., Buerkle, C.A. et al. 2001. The genetic architecture of divergence between threespine stickleback species. Nature, 414: 901-905.
82. Poulin, R., Blanar, C.A., Thieltges, D.W. and Marcogliese, D.J. 2011. The biogeography of parasitism in sticklebacks: distance, habitat differences and the similarity in parasite occurrence and abundance. Ecography, 34: 540-551.
83. Quinn, G.P. and Keough, M.J. 2002. Experimental Design and Data Analysis for Biologists. Cambridge: Cambridge University Press.
84. R Development Core Team. 2008. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
85. Ravinet, M., Prodöhl, PA. and Harrod, C. 2013. On Irish sticklebacks: morphological diversification in a secondary contact zone. Evol. Ecol. Res., 15: 271-294.
86. Reimchen, T.E. 1980. Spine deficiency and polymorphism in a population of Gasterosteus aculeatus: an adaptation to predators? Can. J. Zool., 58: 1232-1244.
87. Reimchen, T.E. 1982. Incidence and intensity of Cyathocephalus truncatus and Schistocephalus solidus infection in Gasterosteus aculeatus. Can. J. Zool., 60: 1091-1095.
88. Reimchen, T.E. 1983. Structural relationships between spines and lateral plates in threespine stickle-back (Gasterosteus aculeatus). Evolution, 37: 931-946.
89. Reimchen, T.E. 1988. Inefficient predators and prey injuries in a population of giant stickleback. Can. J. Zool., 66: 2036-2044.
90. Reimchen, T.E. 1989. Loss of nuptial color in threespine sticklebacks (Gasterosteus aculeatus). Evolution, 43: 450-460.
91. Reimchen, T.E. 1991a. Trout foraging failures and the evolution of body size in stickleback. Copeia, 1991: 1098-1104.
92. Reimchen, T.E. 1991b. Evolutionary attributes of headfirst prey manipulation and swallowing in piscivores. Can. J. Zool., 69: 2912-2916.
93. Reimchen, T.E. 1992. Injuries on stickleback from attacks by a toothed predator (Oncorhynchus) and implications for the evolution of lateral plates. Evolution, 46: 1224-1230.
94. Reimchen, T.E. 1994. Predators and morphological evolution in threespine stickleback. In The Evolutionary Biology of the Threespine Stickleback (M.A. Bell and S.A. Foster, eds.), pp. 240-276. New York: Oxford University Press.
95. Reimchen, T.E. 1995. Predator-induced cyclical changes in lateral plate frequencies of Gasterosteus. Behaviour, 132: 1079-1094.
96. Reimchen, T.E. 2000. Predator handling failures of lateral plate morphs in Gasterosteus aculeatus: implications for stasis and distribution of the ancestral plate condition. Behavior, 137: 1081-1096.
97. Reimchen, T.E. and Byun, A. 2005. The evolution of endemic species on Haida Gwaii in Haida Gwaii: human history and environment from the time of Loon to the time of the Iron people (D. Fedje and R. Mathewes, eds.), pp 77-95. Vancouver, BC: UBC Press.
98. Reimchen, T.E. and Douglas, S.D. 1980. Observations of loons (Gavia immer and G stellata) at a bog lake on the Queen Charlotte Islands. Can. Field Nat., 94: 398-404.
99. Reimchen, T.E. and Douglas, S.D. 1984. Seasonal and diurnal abundance of aquatic birds on the Drizzle Lake Reserve, Queen Charlotte Islands, British Columbia. Can. Field Nat., 98: 22-28.
100. Reimchen, T.E. and Nosil, P. 2002. Temporal cycles in divergent selection on spine number in three-spine stickleback. Evolution, 56: 2472-2483.
101. Reimchen, T.E. and Nosil, P. 2004. Variable predation regimes predict the evolution of sexual dimorphism in a population of threespine stickleback. Evolution, 58: 1274-1281.
102. Reimchen, T.E. and Nosil, P. 2006. Replicated ecological landscapes and the evolution of mor-phological diversity among Gasterosteus populations from an archipelago on the west coast of Canada Can. J. Zool., 84: 643-654.
103. 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.
104. Reist, J.D. 1980. Predation upon pelvic phenotypes of brook stickleback, Culaea inconstans, by selected invertebrates. Can. J. Zool., 58: 1253-1258.
105. Reznick, D. and Endler, J.A. 1982. The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution, 36: 160-177.
106. Salzburger, W. 2009. The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol. Ecol., 18: 169-185.
107. Schluter, D. 2000a. The Ecology of Adaptive Radiation. Oxford: Oxford University Press.
108. Schluter, D. 2000b. Ecological character displacement in adaptive radiation. Am. Nat., 156: S4-S16.
109. Schluter, D., Marchinko, K.B., Barrett, R.D.H. and Rogers, S.M. 2010. Natural selection and the genetics of adaptation in threespine stickleback. Phil. Trans. R. Soc. Lond. B, 365: 2479-2486.
110. Seehausen, O. 2006. African cichlid fish: a model system in adaptive radiation research. Proc. R. Soc. Lond. B, 273: 1987-1998.
111. Shoup, D.E., Callahan, S.P., Wahl, D.H. and Pierce, C.L. 2007. Size-specific growth of bluegill, largemouth bass and channel catfish in relation to prey availability and limnological variables. J. Fish Biol., 70: 21-34.
112. Spoljaric, M. and Reimchen, T.E. 2007. 10,000 years later: evolution of body shape in Haida Gwaii threespine stickleback. J. Fish Biol., 70: 1484-1503.
113. Spoljaric, M.A. and Reimchen, T.E. 2008. Habitat-dependent reduction of sexual dimorphism in geometric body shape of Haida Gwaii threespine stickleback. Biol. J. Linn. Soc., 95: 505-516.
114. Spoljaric, M.A. and Reimchen, T.E. 2011. Habitat-specific trends in ontogeny of body shape in stickleback from coastal archipelago: potential for rapid shifts in colonizing populations. J. Morphol., 272: 590-597.
115. Stinchcombe, J.R. and Hoekstra, H.P. 2008. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity, 100: 158-170.
116. Sutherland-Brown, A. 1968. Geology of the Queen Charlotte Islands, British Columbia. Victoria, BC: British Columbia Department of Energy, Mines and Petroleum Resources Bulletin 54.
117. Taylor, E.B. and McPhail, J.D. 1985. Prolonged and burst swimming in anadromous and freshwater threespine stickleback, Gasterosteus aculeatus. Can. J. Zool., 64: 416-420.
118. Taylor, E.B. and McPhail, J.D. 2000. Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc. R. Soc. Lond. B, 267: 2375-2384.
119. Vamosi, S.M. 2005. On the roles of enemies in divergence and diversification of prey: a review and synthesis. Can. J. Zool., 83: 894-910.
120. Vermeij, G.J. 1982. Unsuccessful predation and evolution. Am. Nat., 120: 701-720.
121. Wade, M.J. and Kalisz, S. 1990. The causes of natural selection. Evolution, 44: 1947-1955.
122. Wagner, C.E., Harmon, L.J. and Seehausen, O. 2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature, 487: 366-369.
123. Walker, J.A. 1997. Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L (Gasterosteidae) body shape. Biol. J. Linn. Soc., 61: 3-50.
124. Webb, P.W. 1982. Locomotor patterns in the evolution of actinopteryigian fishes. Am. Zool., 24: 329-342.
125. Witter, M.S. and Carr, G.D. 1988. Adaptive radiation and genetic differentiation in the Hawaiian silversword alliance (Compositae, Madiinae). Evolution, 42: 1278-1287.
126. Wootton, R.J. 1976. The Biology of the Sticklebacks. New York: Academic Press.
127. Wootton, R.J. 1984. A Functional Biology of Sticklebacks. Berkeley, CA: University of California Press. Canada