Intraguild predation drives evolutionary niche shift in threespine stickleback

Evolution

Volumn 66, Issue 6, 2012, Pages 1819-1832

  Ingram, Travis ^a   Svanbäck, Richard ^a,b   Kraft, Nathan J B ^c   Kratina, Pavel ^a   Southcott, Laura ^a   Schluter, Dolph ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b HARVARD UNIVERSITY   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

Character displacement; Cottus asper; Gasterosteus aculeatus; Geometric morphometrics; Mesocosm experiment; Omnivory

Indexed keywords

ALLOPATRY; ANTAGONISM; ANTIPREDATOR DEFENSE; BENTHOS; CHARACTER DISPLACEMENT; COMPETITIVE ABILITY; DIET; DIETARY SHIFT; EVOLUTIONARY BIOLOGY; FOOD WEB; INTRAGUILD PREDATION; MESOCOSM; MORPHOLOGY; MORPHOMETRY; MORTALITY; OMNIVORY; SYMPATRY; TELEOST; ZOOPLANKTON;

ANIMAL; ARTICLE; COMPARATIVE STUDY; EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; PHYSIOLOGY; PREDATION; SMEGMAMORPHA;

ANIMALS; BIOLOGICAL EVOLUTION; PREDATORY BEHAVIOR; SMEGMAMORPHA;

COTTUS ASPER; GASTEROSTEUS; GASTEROSTEUS ACULEATUS;

EID: 84861671686     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01545.x     Document Type: Article

References (62)

1. Abrams, P. A. 1987. Alternative models of character displacement and niche shift. I. Adaptive shifts in resource use when there is competition for nutritionally nonsubstitutable resources. Evolution 41:651-661.
2. Albert, A. Y., 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. Amarasekare, P. 2007. Trade-offs, temporal variation, and species coexistence in communities with intraguild predation. Ecology 88:2720-2728.
4. Arim, M., and P. A. Marquet 2004. Intraguild predation: a widespread interaction related to species biology. Ecol. Lett. 7:557-564.
5. Bassar, R. D., M. C. Marshall, A. López-Sepulcre, E. Zandonà, S. K. Auer, J. Travis, C. M. Pringle, A. S. Flecker, S. A. Thomas, D. F. Fraser, et al. 2010. Local adaptation in Trinidadian guppies alters ecosystem processes. Proc. Natl. Acad. Sci. USA 107:3616-3621.
6. Bell, A. M., and A. Sih 2007. Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol. Lett. 10:828-834.
7. Berner, D., R. Kaeuffer, A. C. Grandchamp, J. A. M. Raeymaekers, K. Räsänen, and A. P. Hendry 2011. Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotype pair: implications for reproductive isolation. J. Evol. Biol. 24:1975-1983.
8. Bolnick, D. I., T. Ingram, W. E. Stutz, L. K. Snowberg, O. L. Lau, and J. S. Paull 2010. Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proc. R. Soc. Lond. B 277:1789-1797.
9. Crawley, M. J. 2007. The R book. John Wiley and Sons, Chichester, U.K
10. Daugherty, M. P., J. P. Harmon, and C. J. Briggs 2007. Trophic supplements to intraguild predation. Oikos 116:662-677.
11. Day, T., J. Pritchard, and D. Schluter 1994. Ecology and genetics of phenotypic plasticity: a comparison of two sticklebacks. Evolution 48:1723-1734.
12. Diehl, S. 1995. Direct and indirect effects of omnivory in a littoral lake community. Ecology 76:1727-1740.
13. Dingemanse, N. J., F. Van der Plas, J. Wright, D. Réale, M. Schrama, D. A. Roff, E. Van der Zee, and I. Barber 2009. Individual experience and evolutionary history of predation affect expression of heritable variation in fish personality and morphology. Proc. R. Soc. Lond. B 276:1285-1293.
14. Finke, D. L., and R. F. Denno 2006. Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades. Oecologia 149:265-275.
15. Grant, P. R., and B. R. Grant 2006. Evolution of character displacement in Darwin's finches. Science 313:224-226.
16. Harmon, L. J., B. Matthews, S. Des Roches, J. M. Chase, J. B. Shurin, and D. Schluter 2009. Evolutionary diversification in stickleback affects ecosystem functioning. Nature 458:1167-1170.
17. Hendry, A. P., K. Hudson, J. A. Walker, K. Räsänen, and L. J. Chapman 2011. Genetic divergence in morphology-performance mapping between Misty Lake and inlet stickleback. J. Evol. Biol. 24:23-35.
18. Holt, R. D., and G. R. Huxel 2007. Alternative prey and the dynamics of intraguild predation: theoretical perspectives. Ecology 88:2706-2712.
19. Holt, R. D., and G. A. Polis 1997. A theoretical framework for intraguild predation. Am. Nat. 149:745-764.
20. Kondoh, M. 2008. Building trophic modules into a persistent food web. Proc. Natl. Acad. Sci. USA 105:16631-16635.
21. Kratina, P., E. Hammill, and B. R. Anholt 2010. Stronger inducible defenses enhance persistence of intraguild prey. J. Anim. Ecol. 79:993-999.
22. Langerhans, R. B., C. A. Layman, A. M. Shokrollahi, and T. J. DeWitt 2004. Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58:2305-2318.
23. Lavin, P.A., and J. D. McPhail 1986. Adaptive divergence of trophic phenotype among freshwater populations of the threespine stickleback (Gasterosteus aculeatus). Can. J. Fish. Aquat. Sci. 43:2455-2463.
24. Matthews, B., K. B. Marchinko, D. I. Bolnick, and A. Mazumder 2010. Specialization of trophic position and habitat use by sticklebacks in an adaptive radiation. Ecology 91:1025-1034.
25. McCauley, E. 1984. The estimation of the abundance and biomass of zooplankton in samples. Pp. 228-265 in J. A. Downing and F. H. Rigler, eds. A manual on methods for the assessment of secondary productivity in fresh waters. Blackwell Scientific, Oxford, U.K
26. McPhail, J. D. 1994. Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of southwestern British Columbia. Pp. 399-437 in M. A. Bell and S. A. Foster, eds. Evolution of the threespine stickleback. Oxford Univ. Press, Oxford, U.K
27. Milinski, M., and R. Heller 1978. Influence of a predator on the optimal foraging behaviour of sticklebacks (Gasterosteus aculeatus L.). Nature 275:642-644.
28. Morin, P. 1999. Productivity, intraguild predation, and population dynamics in experimental food webs. Ecology 80:752-760.
29. Moodie, G. E. E. 1972. Predation, natural selection and adaptation in an unusual threespine stickleback. Heredity 28:155-167.
30. Nosil, P., and B. J. Crespi 2006. Experimental evidence that predation promotes divergence in adaptive radiation. Proc. Natl. Acad. Sci. USA 103:9090-9095.
31. Pace, M. L., J. J. Cole, S. R. Carpenter, and J. F. Kitchell 1999. Trophic cascades revealed in diverse ecosystems. Trends Ecol. Evol. 14:483-488.
32. Palkovacs, E. P., and D. M. Post 2009. Experimental evidence that phenotypic divergence in predators drives community divergence in prey. Ecology 90:300-305.
33. Palkovacs, E. P., M. C. Marshall, B. A. Lamphere, B. R. Lynch, D. J. Weese, D. F. Fraser, D. N. Reznick, C. M. Pringle, and M. T. Kinnison 2009. Experimental evaluation of evolution and coevolution as agents of ecosystem change in Trinidadian streams. Phil. Trans. R. Soc. Lond. B 364:1617-1628.
34. Palkovacs, E. P., B. A. Wasserman, and M. T. Kinnison 2011. Eco-evolutionary trophic dynamics: loss of top predators drives trophic evolution and ecology of prey. PLoS One 6:e18879.
35. Polis, G. A., and R. D. Holt 1992. Intraguild predation: the dynamics of complex trophic interactions. Trends Ecol. Evol. 7:151-155.
36. Polis, G. A., C. A. Myers, and R. D. Holt 1989. The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu. Rev. Ecol. Syst. 20:297-330.
37. Post, D. M., and E. P. Palkovacs 2009. Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Phil. Trans. R. Soc. Lond. B 364:1629-1640.
38. Post, D. M., and G. Takimoto 2007. Proximate mechanisms for variation in food-chain length. Oikos 116:775-782.
39. Pressley, P. H. 1981. Parental effort and the evolution of nest-guarding tactics in the threespine stickleback, Gasterosteus aculeatus L. Evolution 35:282-295.
40. Pritchard, J. R., and D. Schluter 2001. Declining interspecific competition during character displacement: summoning the ghost of competition past. Evol. Ecol. Res. 3:209-220.
41. R Development Core Team. 2009. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
42. Reimchen, T. E. 1994. Predators and morphological evolution in threespine stickleback. Pp. 240-273 in M. A. Bell and S. A. Foster, eds. The evolutionary biology of the threespine stickleback. Oxford Univ. Press, Oxford, U.K
43. Reznick, D. N., F. H. Shaw, F. H. Rodd, and R. G. Shaw 1997. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275:1934-1937.
44. Rohlf, F. J. 2005a. tpsDig, version 1.40. Distributed by the author, Department of Ecology and Evolution, State University of New York, Stony Brook, NY
45. --- 2005b. tpsRelw, version 1.44. Distributed by the author. Department of Ecology and Evolution, State University of New York, Stony Brook, NY.
46. Rooney, N., K. S. McCann, and J. C. Moore 2008. A landscape theory for food web architecture. Ecol. Lett. 11:867-881.
47. Rundle, H. D., S. M. Vamosi, and D. Schluter 2003. Experimental test of predation's effect on divergent selection during character displacement in sticklebacks. Proc. Natl. Acad. Sci. USA 100:14943-14948.
48. Sample, B. E., R. J. Cooper, R. D. Greer, and R. C. Whitmore 1993. Estimation of insect biomass by length and width. Am. Midl. Nat. 129:234-240.
49. Schluter, D. 1994. Experimental evidence that competition promotes divergence in adaptive radiation. Science 266:798-801.
50. Schluter, D., E. A. Clifford, M. Nemethy, and J. S. McKinnon 2004. Parallel evolution and inheritance of quantitative traits. Am. Nat. 163:809-822.
51. Schoener, T. W. 2011. The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 331:426-429.
52. Spoljaric, M. A., and T. E. Reimchen 2007. 10 000 years later: evolution of body shape in Haida Gwaii three-spined stickleback. J. Fish Biol. 70:1484-1503.
53. Tabachnick, B., and L. Fidell 1996. Using multivariate statistics, 3rd ed. Harper and Row, New York
54. Vamosi, S. M. 2003. The presence of other fish species affects speciation in threespine sticklebacks. Evol. Ecol. Res. 5:717-730.
55. Vamosi, S. M., and D. Schluter 2002. Impacts of trout predation on fitness of sympatric sticklebacks and their hybrids. Proc. R. Soc. Lond. B 269:923-930.
56. Vance-Chalcraft, H. D., J. A. Rosenheim, J. R. Vonesh, C. W. Osenberg, and A. Sih 2007. The influence of intraguild predation on prey suppression and prey release: a meta-analysis. Ecology 88:2689-2696.
57. Vandermeer, J. 2006 Omnivory and the stability of food webs. J. Theor. Biol. 238:497-504.
58. Venables, W. N., and B. D. Ripley 2002. Modern applied statistics with S, 4th ed. Springer, New York
59. Walker, J. A. 1997. Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L (Gasterosteidae) body shape. Biol. J. Linn. Soc. 61:3-50.
60. 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.
61. Werner, E. E., and D. J. Hall 1988. Ontogenetic habitat shifts in bluegill: the foraging rate-predation risk trade-off. Ecology 69:1352-1366.
62. Zelditch, M. L., D. L. Swiderski, H. D. Sheets, and W. L. Fink 2004. Geometric morphometrics for biologists. Elsevier Academic Press, Amsterdam, The Netherlands