Natural selection drives patterns of lake-stream divergence in stickleback foraging morphology

Journal of Evolutionary Biology

Volumn 21, Issue 6, 2008, Pages 1653-1665

  Berner, D ^a   Adams, D C ^b,c   Grandchamp, A C ^a   Hendry, A P ^a  

^a MCGILL UNIVERSITY   (Canada)

^b IOWA STATE UNIVERSITY   (United States)

^c Department of Statistics Center for Statistics and Applications in Forensic Evidence Iowa State University 2438 Osborn Dr Ames   (United States)

Author keywords

Determinism; Divergent selection; Evolutionary constraint; Gasterosteus aculeatus; Limnetic benthic differentiation; Line of least resistance; Parallel evolution; Phenotypic covariance

Indexed keywords

FRESH WATER;

DIET; DIVERGENCE; EVOLUTION; FORAGING BEHAVIOR; MORPHOLOGY; NATURAL SELECTION; TELEOST;

ANIMAL; ARTICLE; BIODIVERSITY; ECOSYSTEM; FEEDING BEHAVIOR; GENETIC SELECTION; GILL; HISTOLOGY; PHENOTYPE; PHYSIOLOGY; SMEGMAMORPHA; SPECIES DIFFERENCE; STOMACH JUICE;

ANIMALS; BIODIVERSITY; ECOSYSTEM; FEEDING BEHAVIOR; FRESH WATER; GASTROINTESTINAL CONTENTS; GILLS; PHENOTYPE; SELECTION (GENETICS); SMEGMAMORPHA; SPECIES SPECIFICITY;

GASTEROSTEUS; GASTEROSTEUS ACULEATUS;

EID: 54049094097     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2008.01583.x     Document Type: Article

References (72)

1. Adams, D.C. Collyer, M.L. 2007. Analysis of character divergence along environmental gradients and other covariates. Evolution 61 : 510 515.
2. Aguirre, W.E., Doherty, P.K. Bell, M.A. 2004. Genetics of lateral plate and gillraker phenotypes in a rapidly evolving population of threespine stickleback. Behaviour 141 : 1465 1483.
3. 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.
4. Arnold, S.J. 1992. Constraints on phenotypic evolution. Am. Nat. 140 : S85 S107.
5. Arnold, S.J., Pfrender, M.E. Jones, A.G. 2001. The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica 112-113 : 9 32.
6. Badyaev, A.V. Hill, G.E. 2000. The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure. Evolution 54 : 1784 1794.
7. Bégin, M. Roff, D.A. 2004. From micro- to macroevolution through quantitative genetic variation: positive evidence from field crickets. Evolution 58 : 2287 2304.
8. Bégin, M., Roff, D.A. Debat, V. 2004. The effect of temperature and wing morphology on quantitative genetic variation in the cricket Gryllus firmus, with an appendix examining the statistical properties of the Jackknife-manova method of matrix comparison. J. Evol. Biol. 17 : 1255 1267.
9. Bentzen, P. McPhail, J.D. 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.
10. Berner, D. Blanckenhorn, W.U. 2006. Grasshopper ontogeny in relation to time constraints: adaptive divergence and stasis. J. Anim. Ecol. 75 : 130 139.
11. Björklund, M. 1996. The importance of evolutionary constraints in ecological time scales. Evol. Ecol. 10 : 423 431.
12. Blake, R.W. 2004. Fish functional design and swimming performance. J. Fish Biol. 65 : 1193 1222.
13. Bolnick, D.I. 2004. Can intraspecific competition drive disruptive selection? An experimental test in natural populations of sticklebacks Evolution 58 : 608 618.
14. Bolnick, D.I., Caldera, E.J. Matthews, B. 2008. Evidence for asymmetric migration load in a pair of ecologically divergent lacustrine stickleback populations. Biol. J. Linn. Soc. 94 : 273 287.
15. Bookstein, F.L., Chernoff, B., Elder, R.L., Humphries, J.M., Smith, G.R. Strauss, R.E. 1985. Morphometrics in evolutionary biology. Acad. Nat. Sci. Phila. Spec. Publ. 15 : 1 277.
16. Brakefield, P.M. Roskam, J.C. 2006. Exploring evolutionary constraints is a task for an integrative evolutionary biology. Am. Nat. 168 : S4 S13.
17. Caldecutt, W.J. Adams, D.C. 1998. Morphometrics of trophic osteology in the threespine stickleback, Gasterosteus aculeatus. Copeia 1998 : 827 838.
18. Cheverud, J.M. 1988. A comparison of genetic and phenotypic correlations. Evolution 42 : 958 968.
19. Clague, J.J. James, T.S. 2002. History and isostatic effects of the last ice sheet in southern British Columbia. Quatern. Sci. Rev. 21 : 71 87.
20. Collyer, M.L. Adams, D.C. 2007. Analysis of two-state multivariate phenotypic change in ecological studies. Ecology 88 : 683 692.
21. Day, T. McPhail, J.D. 1996. The effect of behavioural and morphological plasticity on foraging efficiency in the threespine stickleback (Gasterosteus sp.). Oecologia 108 : 380 388.
22. Day, T., Pritchard, J. Schluter, D. 1994. Ecology and genetics of phenotypic plasticity: a comparison of two sticklebacks. Evolution 48 : 1723 1734.
23. Endler, J.A. 1986. Natural Selection in the Wild. Princeton University, Princeton, NJ.
24. Gerking, S.D. 1994. Feeding Ecology of Fish. Academic, San Diego, CA.
25. Gross, H.P. Anderson, J.M. 1984. Geographic variation in the gillrakers and diet of European sticklebacks, Gasterosteus aculeatus. Copeia 1984 : 87 97.
26. Hagen, D.W. 1973. Inheritance of numbers of lateral plates and gill rakers in Gasterosteus aculeatus. Heredity 30 : 303 312.
27. Hatfield, T. 1997. Genetic divergence in adaptive characters between sympatric species of stickleback. Am. Nat. 149 : 1009 1029.
28. Hendry, A.P. Taylor, E.B. 2004. How much of the variation in adaptive divergence can be explained by gene flow? An evaluation using lake-stream stickleback pairs. Evolution 58 : 2319 2331.
29. Hendry, A.P., Taylor, E.B. McPhail, J.D. 2002. Adaptive divergence and the balance between selection and gene flow: lake and stream stickleback in the Misty system. Evolution 56 : 1199 1216.
30. Hermida, M., Fernandez, C., Amaro, R. San Miguel, E. 2002. Heritability and "evolvability" of meristic characters in a natural population of Gasterosteus aculeatus. Can. J. Zool. 80 : 532 541.
31. Jastrebski, C.J. Robinson, B.W. 2004. Natural selection and the evolution of replicated trophic polymorphisms in pumpkinseed sunfish (Lepomis gibbosus). Evol. Ecol. Res. 6 : 285 305.
32. Jolicoeur, P. 1963. Multivariate generalization of allometry equation. Biometrics 19 : 497 499.
33. Lande, R. 1979. Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33 : 402 416.
34. Langerhans, R.B. DeWitt, T.J. 2004. Shared and unique features of evolutionary diversification. Am. Nat. 164 : 335 349.
35. Langerhans, R.B., Layman, C.A., Shokrollahi, A.M. DeWitt, T.J. 2004. Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58 : 2305 2318.
36. Lavin, P.A. McPhail, J.D. 1993. Parapatric lake and stream sticklebacks on northern Vancouver Island: disjunct distribution or parallel evolution? Can. J. Zool. 71 : 11 17.
37. Losos, J.B., Jackman, T.R., Larson, A., de Queiroz, K. Rodriguez-Schettino, L. 1998. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279 : 2115 2118.
38. Lynch, M. Walsh, B. 1998. Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, MA.
39. Manly, B.F.J. 2007. Randomization, Bootstrap and Monte Carlo Methods in Biology, 3rd edn. Chapman & Hall, Boca Raton, FL.
40. McGuigan, K. 2006. Studying phenotypic evolution using multivariate quantitative genetics. Mol. Ecol. 15 : 883 896.
41. McGuigan, K., Franklin, C.E., Moritz, C. Blows, M.W. 2003. Adaptation of rainbow fish to lake and stream habitats. Evolution 57 : 104 118.
42. McGuigan, K., Chenoweth, S.F. Blows, M.W. 2005. Phenotypic divergence along lines of genetic variance. Am. Nat. 165 : 32 43.
43. McKinnon, J.S., Mori, S., Blackman, B.K., David, L., Kingsley, D.M., Jamieson, L., Chou, J. Schluter, D. 2004. Evidence for ecology's role in speciation. Nature 429 : 294 298.
44. McPeek, M.A. 1995. Morphological evolution mediated by behavior in the damselflies of two communities. Evolution 49 : 749 769.
45. Merilä, J. Björklund, M. 1999. Population divergence and morphometric integration in the greenfinch (Carduelis chloris) - evolution against the trajectory of least resistance? J. Evol. Biol. 12 : 103 112.
46. Moore, J.S., Gow, J.L., Taylor, E.B. Hendry, A.P. 2007. Quantifying the constraining influence of gene flow on adaptive divergence in the lake-stream threespine stickleback system. Evolution 61 : 2015 2026.
47. Ostbye, K., Amundsen, P.A., Bernatchez, L., Klemetsen, A., Knudsen, R., Kristoffersen, R., Naesje, T.F. Hindar, K. 2006. Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times. Mol. Ecol. 15 : 3983 4001.
48. Peichel, C.L., Nereng, K.S., Oghi, K.A., Cole, B.L.E., Colosimo, P.F., Buerkle, C.A., Schluter, D. Kingsley, D.M. 2001. The genetic architecture of divergence between threespine stickleback species. Nature 414 : 901 905.
49. Pennak, R.W. 1989. Fresh-water Invertebrates of the United States, 3rd edn. Wiley, New York.
50. R Development Core Team 2006. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
51. Reimchen, T.E., Stinson, E.M. 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.
52. Robinson, B.W. 2000. Trade offs in habitat-specific foraging efficiency and the nascent adaptive divergence of sticklebacks in lakes. Behaviour 137 : 865 888.
53. Robinson, B.W. Wilson, D.S. 1994. Character release and displacement in fishes - a neglected literature. Am. Nat. 144 : 596 627.
54. Roff, D.A. 1995. The estimation of genetic correlations from phenotypic correlations - a test of Cheverud's conjecture. Heredity 74 : 481 490.
55. Roff, D.A. 1996. The evolution of genetic correlations: an analysis of patterns. Evolution 50 : 1392 1403.
56. Roff, D. 2000. The evolution of the G matrix: selection of drift? Heredity 84 : 135 142.
57. Roff, D. 2002. Comparing G matrices: a manova approach. Evolution 56 : 1286 1291.
58. Roff, D.A., Mousseau, T.A. Howard, D.J. 1999. Variation in genetic architecture of calling song among populations of Allonemobius socius, A. fasciatus, and a hybrid population: drift or selection? Evolution 53 : 216 224.
59. Rundle, H.D., Nagel, L., Boughman, J.W. Schluter, D. 2000. Natural selection and parallel speciation in sympatric sticklebacks. Science 287 : 306 308.
60. Schluter, D. 1993. Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology 74 : 699 709.
61. Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50 : 1766 1774.
62. Schluter, D. 2000. The Ecology of Adaptive Radiation. Oxford University, Oxford.
63. Schluter, D. McPhail, J.D. 1992. Ecological character displacement and speciation in sticklebacks. Am. Nat. 140 : 85 108.
64. Schluter, D., Clifford, E.A., Nemethy, M. McKinnon, J.S. 2004. Parallel evolution and inheritance of quantitative traits. Am. Nat. 163 : 809 822.
65. Shaw, F.H., Shaw, R.G., Wilkinson, G.S. Turelli, M. 1995. Changes in genetic variances and covariances: G whiz! Evolution 49 : 1260 1267.
66. Skulason, S. Smith, T.B. 1995. Resource polymorphism in vertebrates. Trends Ecol. Evol. 10 : 366 370.
67. Steppan, S.J., Phillipps, P.C. Houle, D. 2002. Comparative quantitative genetics: evolution of the G matrix. Trends Ecol. Evol. 17 : 320 327.
68. Svanbäck, R. Bolnick, D.I. 2007. Intraspecific competition drives increased resource use diversity within a natural population. Proc. R. Soc. B 274 : 839 844.
69. Thompson, C.E., Taylor, E.B. McPhail, J.D. 1997. Parallel evolution of lake-stream pairs of threespine sticklebacks (Gasterosteus) inferred from mitochondrial DNA variation. Evolution 51 : 1955 1965.
70. Thorp, J.H. Covich, A.P. (eds 2001) Ecology and Classification of North American Freshwater Invertebrates. Academic, San Diego, CA.
71. Walker, J.A. 1997. Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L. (Gasterosteidae) body shape. Biol. J. Linn. Soc. 61 : 3 50.
72. Webb, P.W. 1984. Body form, locomotion and foraging in aquatic vertebrates. Am. Zool. 24 : 107 120.