Sexual dimorphism and speciation on two ecological coins: Patterns from nature and theoretical predictions

Evolution

Volumn 65, Issue 9, 2011, Pages 2553-2571

  Cooper, Idelle A ^a   Gilman, R Tucker ^b   Boughman, Janette Wenrick ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Adaptive radiation; Adaptive splitting; Disruptive selection; Ecological dimorphism; Stickleback species pair

Indexed keywords

ADAPTIVE RADIATION; BODY SIZE; LAKE ECOSYSTEM; SEXUAL DIMORPHISM; SPECIATION (BIOLOGY); TELEOST; THEORETICAL STUDY;

ADAPTATION; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BODY SIZE; CANADA; EVOLUTION; FEMALE; GENETIC SELECTION; GENETICS; HEAD; HISTOLOGY; LAKE; MALE; MULTIVARIATE ANALYSIS; SEXUAL DEVELOPMENT; SMEGMAMORPHA; SPECIES DIFFERENTIATION;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; BODY SIZE; BRITISH COLUMBIA; FEMALE; GENETIC SPECIATION; HEAD; LAKES; MALE; MODELS, BIOLOGICAL; MULTIVARIATE ANALYSIS; SELECTION, GENETIC; SEX CHARACTERISTICS; SMEGMAMORPHA;

BRITISH COLUMBIA; CANADA;

GASTEROSTEUS; GASTEROSTEUS ACULEATUS;

EID: 80052272222     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01332.x     Document Type: Article

References (114)

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. Aguirre, W. E., and O. Akinpelu. 2010. Sexual dimorphism of head morphology in three-spined stickleback Gasterosteus aculeatus. J. Fish Biol. 77:802-821.
3. Albert, A. Y. K., N. P. Millar, and D. Schluter. 2007. Character displacement of male nuptial colour in threespine sticklebacks (Gasterosteus aculeatus). Biol. J. Linn. Soc. 91:37-48.
4. 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.
5. Attrill, M. J., and M. Power. 2004. Partitioning of temperature resources amongst an estuarine fish assemblage. Estuarine Coastal and Shelf Science 61:725-738.
6. Bakker, T. C. M. 1994. Genetic correlations and the control of behavior, exemplified by aggressiveness in sticklebacks. Adv. Study Behav. 23:135-171.
7. Bakker, T. C. M., and M. Milinski. 1993. The advantages of being red-sexual selection in the stickleback. Marine Behav. Physiol. 23:287-300.
8. Baylac, M., C. Villemant, and G. Simbolotti. 2003. Combining geometric morphometrics with pattern recognition for the investigation of species complexes. Biol. J. Linn. Soc. 80:89-98.
9. Behm, J. E., A. R. Ives, and J. W. Boughman. 2010. Breakdown in postmating isolation and the collapse of a species pair through hybridization. Am. Nat. 175:11-26.
10. Bentzen, P., and J. D. McPhail. 1984. Ecology and evolution of sympatric sticklebacks (Gasterosteus)-specialization for alternative trophic niches in the Enos Lake species pair. Can. J. Zool. 62:2280-2286.
11. Blake, R. W. 2004. Fish functional design and swimming performance. J. Fish Biol. 65:1193-1222.
12. Bolnick, D. I. 2004. Can intraspecific competition drive disruptive selection? An experimental test in natural populations of sticklebalks. Evolution 58:608-618.
13. Bolnick, D. I., and M. Doebeli. 2003. Sexual dimorphism and adaptive speciation: two sizes of the same ecological coin. Evolution 57:2433-2449.
14. Bolnick, D. I., and O. L. Lau. 2008. Predicable patterns of disruptive selection in stickleback in postglacial lakes. Am. Nat. 172:1-11.
15. Bolnick, D. I., and J. S. Paull. 2009. Morphological and dietary differences between individuals are weakly but positively correlated within a population of threespine stickleback. Evol. Ecol. Res. 11:1217-1233.
16. Bookstein, F. L. 1991. Morphometric tools for landmark data. Cambridge Univ. Press, Cambridge, UK.
17. Boughman, J. W. 2007. Divergence and speciation in sticklebacks. Pp. 83-126 in S. Östlund-Nilsson, I. Mayber and F. A. Huntingford, eds. The biology of threespine sticklebacks. CRC Press, Boca Raton, FL.
18. Brede, E. G., and T. J. C. Beebee. 2006. Large variations in the ratio of effective breeding and census population sizes between two species of pond-breeding anurans. Biol. J. Linn. Soc. 89:365-372.
19. Bürger, R., and K. A. Schneider. 2006. Intraspecific competitive divergence and convergence under assortative mating. Am. Nat. 167:190-205.
20. Bürger, R., K. A. Schneider, and M. Willensdorfer. 2006. The conditions for speciation through intraspecific competition. Evolution 60:2185-2206.
21. Butler, M. A., and J. B. Losos. 2002. Multivariate sexual dimorphism, sexual selection, and adaptation in Greater Antillean Anolis lizards. Ecol. Monogr. 72:541-559.
22. Butler, M. A., S. A. Sawyer, and J. B. Losos. 2007. Sexual dimorphism and adaptive radiation in Anolis lizards. Nature 447:202-205.
23. Caldecutt, W. J., and D. C. Adams. 1998. Morphometrics of trophic osteology in the threespine stickleback, Gasterosteus aculeatus. Copeia 1998:827-838.
24. Caldecutt, W. J., M. A. Bell, and J. A. Buckland-Nicks. 2001. Sexual dimorphism and geographic variation in dentition of threespine stickleback, Gasterosteus aculeatus. Copeia 4:936-944.
25. Caldera, E. J., and D. I. Bolnick. 2008. Effects of colonization history and landscape structure on genetic variation within and among threespine stickleback (Gasterosteus aculeatus) populations in a single watershed. Evol. Ecol. Res. 10:575-598.
26. Crispo, E. 2008. Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. J. Evol. Biol. 21:1460-1469.
27. Davis, A. B., and P. A. Verrell. 2005. Demography and reproductive ecology of the Columbia spotted frog (Rana luteiventris) across the Palouse. Can. J. Zool. 83:702-711.
28. Day, T., and J. D. McPhail. 1996. The effect of behavioural and morphological plasticity on foraging efficiency in the threespine stickleback (Gasterosteus sp). Oecologia 108:380-388.
29. Day, T., J. Pritchard, and D. Schluter. 1994. A comparison of 2 sticklebacks. Evolution 48:1723-1734.
30. de Cara, M. A. R., N. H. Barton, and M. Kirkpatrick. 2008. A model for the evolution of assortative mating. Am. Nat. 171:580-596.
31. Dieckmann, U., and M. Doebeli. 1999. On the origin of species by sympatric speciation. Nature 400:354-357.
32. Dieckmann, U., M. Doebeli, J. A. J. Metz, and D. Tautz. 2004. Adaptive speciation. Univ. Press, Cambridge.
33. Doebeli, M., and U. Dieckmann. 2000. Evolutionary branching and sympatric speciation caused by different types of ecological interactions. Am. Nat. 156:S77-S101.
34. Doebeli, M., and U. Dieckmann. 2003. Speciation along environmental gradients. Nature 421:259-264.
35. Doebeli, M., and I. Ispolatov. 2010. Complexity and diversity. Science 328:494.
36. Foster, S. A. 1994. Interference of evolutionary patterns-diversionary displays of 3-spined sticklebacks. Behav. Ecol. 5:114-121.
37. Fraley, C., and A. E. Raftery. 1998. How many clusters? Which clustering method? Answers via model-based cluster analysis. Computer J. 41:578-588.
38. Friggens, M. M., and Brown, J. H. 2005. Niche partitioning in the cestode communities of two elasmobranchs. Oikos 108:76-84.
39. Gilbert, B., D. S. Srivastava, and K. R. Kirby. 2008. Niche partitioning at multiple scales facilitates coexistence among mosquito larvae. Oikos 117:944-950.
40. Gavrilets, S. 2004, Fitness landscapes and the origin of species. Princeton Univ. Press, Princeton, NJ.
41. Geritz, S. A. H., E. Kisdi, G. Meszena, and J. A. J. Metz. 1998. Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evol. Ecol. 12:35-57.
42. Gilman, R. T., and J. E Behm. Hybridization, species collapse, and species reemergence after disturbance to premating mechanisms of reproductive isolation. Evolution. In press.
43. Grant, P. R. 1986, Ecology and evolution of Darwin's finches. Princeton Univ. Press, Princeton, NJ.
44. Greenberg, R., and B. Olsen. 2010. Bill size and dimorphism in tidal-marsh sparrows: island-like processes in a continental habitat. Ecology 91:2428-2436.
45. Hammer, O., Harper, D. A. T., and P. D. Ryan. 2001. PAST: paleontological statistics software packages for education and data analysis. Paleontol. Electronica 4:9.
46. Hart, P. J. B., and A. B. Gill. 1994. Evolution of foraging behavior in the threespine stickleback. Pp. 207-236. in M. A. Bell and S. A. Foster, eds. The evolutionary biology of the three-spine stickleback. Oxford Univ. Press, Oxford.
47. Hatfield, T., and D. Schluter. 1999. Ecological speciation in sticklebacks: environment-dependent hybrid fitness. Evolution 53:866-873.
48. Hawthorne, D. J., and S. Via. 2001. Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412:904-907.
49. Jiggins, C. D., R. E. Naisbit, R. L. Coe, and J. Mallet. 2001. Reproductive isolation caused by colour pattern mimicry. Nature 411:302-305.
50. Kisdi, E., and S. A. H. Geritz. 1999. Adaptive dynamics in allele space: evolution of genetic polymorphism by small mutations in a heterogeneous environment. Evolution 53:992-1008.
51. Kitano, J., S. Mori, and C. L. Peichel. 2007. Sexual dimorphism in the external morphology of the threespine stickleback (Gasterosteus aculeatus). Copeia 2:336-349.
52. Kraack, S. B. M., T. C. M. Batkker, and B. Mundwiler. 1999. Sexual selection in sticklebacks in the field: correlates of reproductive, mating, and paternal success. Behav. Ecol. 10:696-706.
53. Kume, M., J. Kitano, S. Mori, and T. Shibuya. 2010. Ecological divergence and habitat isolation between two migratory forms of Japanese threespine stickleback (Gasterosteus aculeatus). J. Evol. Biol. 23:1436-1446.
54. Larson, G. L. 1976. Social behaviour and feeding ability of two phenotypes of Gasterosteus aculeatus in relation to their spatial and trophic segregation in a temperate lake. Can. J. Zool 54:107-121.
55. Lavin, P. A., and J. D. McPhail. 1986. Adaptive divergence of trophic phenotype among freshwater populations of the threespine stickleback (Gasterosteus aculeatus). Can. J. Fisheries Aquatic Sci. 43:2455-2463.
56. Law, T. C., and R. W. Blake. 1996. Comparison of the fast-start performances of closely related, morphologically distinct threespine sticklebacks (Gasterosteus spp). J. Exp. Biol. 199:2595-2604.
57. Liem, K. F. 1993. Ecomorphology of the teleostean skull. Pp. 422-452. in J. Hanken and B. K. Hall eds. The skull. Univ. of Chicago Press, Chicago.
58. Lucentini, L., A. Palomba, L. Gigliarelli, G. Sgaravizzi, H. Lancioni, L. Lanfaloni, M. Natali, F. Panara. 2009. Temporal changes and effective population size of an Italian isolated and supportive-breeding managed northern pike (Esox lucius) population. Fisheries Res. 96:139-147.
59. Nosil, P., and T. E. Reimchen. Ecological opportunity and levels of morphological variance within freshwater stickleback populations. Biol. J. Linn. Soc. 85:297-308.
60. Malmquist, H. J. 1992. Phenotype-specific feeding-behavior of two Arctic Charr Salvelinus alpinius morphs. Oecologia 92:354-361.
61. Martin, R. A., and D. W. Pfennig. 2010. Field and experimental evidence that competition and ecological opportunity promote resource polymorphism. Biol. J. Linn. Soc. 100:73-88.
62. McKinnon, J. S., and J. D. McPhail. 1996. Male aggression and colour in divergent populations of threespine stickleback: experiment with animations. Can. J. Zool. 74:1727-1733.
63. McKinnon, J. S., and H. D. Rundle. 2002. Speciation in nature: the threespine stickleback model systems. Trends Ecol. Evol. 17:480-488.
64. McLennan, D. A., and J. D. McPhail. 1989. Experimental investigation of the evolutionary significance of sexually dimorphic nuptial coloration in Gasterosteus aculeatus (L)-temporal changes in the structure of the male mosaic signal. Can. J. Zool. 67:1767-1777.
65. McPhail, J. D. 1984. Ecology and evolution of sympatric sticklebacks (Gasterosteus): morphological and genetic evidence for a species pair in Enos Lake, British Columbia. Can. J. Zool. 62:1402-1408.
66. McPhail, J. D. 1992. Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species pair in Paxton Lake, Texada Island, British Columbia. Can. J. Zool. 70:361-369.
67. McPhail, J. D. 1993. Ecology and evolution of sympatric sticklebacks (Gasterosteus)-origin of the species pairs. Can. J. Zool. 71:515-523.
68. McPhail, J. D. 1994. Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of south-western British Columbia. Pp. 399-437 in M. A. Bell and S. A. Foster eds. The evolutionary biology of the threespine stickleback. Oxford Univ. Press, Oxford.
69. Metz, J. A. J., S. A. H. Ge ritz, G. Mesze'na, F. J. A. Jacobs, and J.S. van Heerwaarden. 1996. Pp. 183-231 in S. J. van Strien and S. M. Verduyn Lunel, eds. Stochastic and spatial structures of dynamical systems. North Holland, Amsterdam.
70. Meer, H. J., and G. C. Anker. 1984. Retinal resolving power and sensitivity of the photopic system in seven haplochromine species (Teleostei, Cichlidae). Neth. J. Zool. 34:197-209.
71. Niemiller, M. L., B. M. Fitzpatrick, and B. T. Miller. 2008. Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies. Mol. Ecol. 17:2258-2275.
72. Nosil, P., L. J. Harmon, and O. Seehausen. 2009. Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. 24:145-156.
73. Otto, S. P., M. R. Servedio, and S. L. Nuismer. 2008. Frequency-dependent selection and the evolution of assortative mating. Genetics 179:2091-2112.
74. Parent, C. E., and B. Crespi. 2009. Ecological opportunity in adaptive radiation of Galapagos endemic land snails. Am. Nat. 174:898-905.
75. Pennings, P. S., M. Kopp, G. Meszena, U. Dieckmann, and J. Hermisson. 2008. An analytically tractable model for competitive speciation. Am. Nat. 171:E44-E71.
76. 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.
77. Podos, J. 2001. Correlated evolution of morphology and vocal signal structure in Darwin's finches. Nature 409:185-188.
78. Poe, S., J. R. Goheen, and E. P. Hulbak. 2007. Convergent exaptation and adaptation in solitary island lizards. Proc. R. Soc. Lond. B 274:2231-2237.
79. Rice, W. R., and Hostert, E. E. 1993. Laboratory experiments in speciation: what have we learned in 40 years? Evol. Int. J. Org. Evol. 47:1637-1653.
80. Reimchen, T. E. 1980. Spine deficiency and polymorphism in a population of Gasterosteus aculeatus-an adaptation to predators. Can. J. Zool. 58:1232-1244.
81. Reimchen, T. E. 1991. Trout foraging failures and the evolution of body size in stickleback. Copeia 4:1098-1104.
82. Reimchen, T. E., and P. Nosil. 2001. Lateral plate asymmetry, diet and parasitism in threespine stickleback. J. Evol. Biol. 14:632-645.
83. Reimchen, T. E., and P. Nosil. 2002. Temporal variation in divergent selection on spine number in threespine stickleback. Evolution 56:2472-2483.
84. Reimchen, T. E., and P. Nosil. 2004. Variable predation regimes predict the evolution of sexual dimorphism in a population of threespine stickleback. Evolution 58:1274-1281.
85. Robinson, B. W., and D. Schluter. 2000. Natural selection and the evolution of adaptive genetic variation in northern freshwater fishes. Pp. 65-94 in T. Mousseau, B. Sinervo and J. A. Endler, eds. Adaptive genetic variation in the wild. Oxford Univ. Press, New York, New York, USA.
86. Robinson, B. W., and D. S. Wilson. 1994. Character release and displacement in fishes-a neglected literature. Am. Nat. 144:596-627.
87. Rohlf, F. J. 1997. TPSDIG program. Department of Ecology and Evolution, SUNY, Stony Brook, New York. Available from.
88. Rohlf, F. J. 1999. Shape statistics: Procrustes superimpositions and tangent spaces. J. Classif. 16:197-223.
89. Rueffler, C., T. J. M. Van Dooren, O. Leimar, and P. A. Abrams. 2006. Disruptive selection and then what?Trends Ecol. Evol. 21:238-245.
90. Rundle, H. D., L. Nagel, J.W. Boughman, and D. Schluter. 2000. Natural selection and parallel speciation in sympatric sticklebacks. Science 287:306-308.
91. Rundle, H. D., and P. Nosil. 2005. Ecological speciation. Ecol. Letts. 8:336-352.
92. Rundle, H. D., and D. Schluter. 2004. Natural selection and ecological speciation in sticklebacks. Pp. 192-209 in U. Dieckmann, M. Doebeli, J. A. J. Metz and D. Tautz, eds. Adaptive speciation. Cambridge Univ. Press, Cambridge, UK.
93. Schluter, D. 1993. Adaptive radiation in sticklebacks-size, shape, and habitat use efficiency. Ecology 74:699-709.
94. Schluter, D. 1994. Experimental evidence that competition promotes divergence in adaptive radiation. Science 266:798-801.
95. Schluter, D. 1995. Adaptive radiation in sticklebacks-trade-offs in feeding performance and growth. Ecology 76:82-90.
96. Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50:1766-1774.
97. Schluter, D. 2003. Frequency dependent natural selection during character displacement in sticklebacks. Evolution 57:1142-1150.
98. Schluter, D., and J. D. McPhail. 1992. Ecological character displacement and speciation in sticklebacks. Am. Nat. 140:85-108.
99. Schmeller, D. S., and J. Merila. 2007. Demographic and genetic estimates of effective population and breeding size in the amphibian Rana temporaria. Conserv. Biol. 21:142-151.
100. Schoener, T. W. 1967. The ecological significance of sexual dimorphism in size in the lizard Anolis conspersus. Science 155:474-477.
101. Selander, R. K. 1966. Sexual dimorphism and differential niche utilization in birds. Condor 68:113-151.
102. Shine, R. 1989. Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q. Rev. Biol. 64:419-461.
103. Skulason, S., and T. B. Smith. 1995. Resource polymorphism in vertebrates. Trends Ecol. Evol. 10:366-370.
104. Slatkin, M. 1984. Ecological causes of sexual dimorphism. Evolution 38:622-630.
105. Spoljaric, M. A., and T. E. Reimchen. 2008. Habitat-dependent reduction of sexual dimorphism in geometric body shape of Haida Gwaii threespine stickleback. Biol. J. Linn. Soc. 95:505-516.
106. Stephens, P. R., and J. J. Wiens. 2009. Evolution of sexual size dimorphism in emydid turtles: ecological dimorphism, Rensch's rule, and sympatric divergence. Evolution 63:910-925.
107. Taylor, E. B., J. W. Boughman, M. Groenenboom, M. Sniatynski, D. Schluter, and J. L. Gow. 2006. Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol. Ecol. 15:343-355.
108. Temeles, E. J., I. L. Pan, and J. L. Brennan. 2000. Evidence for ecological causation of sexual dimorphism in a hummingbird. Science 289:441-443.
109. Vamosi, S. M. 2002. Predation sharpens the adaptive peaks: survival trade-offs in sympatric sticklebacks. Ann. Zool. Fennici. 39:237-248.
110. van Doorn, G. S., U. Dieckman, and F. J. Weissing. 2004. Sympatric speciation by sexual selection: a critical reevaluation. Am. Nat. 163:709-725.
111. Walker, J. A. 1997. Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L (Gasterosteidae) body shape. Biol. J. Linn. Soc. 61:3-50.
112. Walton, W. E., S. S. Easter, Jr., C. Malinoski, and N. G. Hairston, Jr. 1994. Size-related change in the visual resolution of sunfish (Lepomis spp.). Can. J. Fish. Aquat. Sci. 51:2017-2026.
113. Webb, P. W. 1984. Body form, locomotion and foraging in aquatic vertebrates. Am. Zool. 24: 107-120.
114. Wund, M. A., J. A. Baker, B. Clancy, J. L. Golub, and S. A. Foster. 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.