You are not currently logged in.

Access your personal account or get JSTOR access through your library or other institution:


Log in to your personal account or through your institution.

Functional Complexity Can Mitigate Performance Trade-Offs

Roi Holzman, David C. Collar, Rita S. Mehta and Peter C. Wainwright
The American Naturalist
Vol. 177, No. 3 (March 2011), pp. E69-E83
DOI: 10.1086/658366
Stable URL:
Page Count: 15
Subjects: Biological Sciences Ecology & Evolutionary Biology
Find more content in these subjects: Biological Sciences Ecology & Evolutionary Biology
  • Download PDF
  • Add to My Lists
  • Cite this Item
Functional Complexity Can Mitigate Performance Trade-Offs
We're having trouble loading this content. Download PDF instead.


AbstractTrade-offs are believed to impose major constraints on adaptive evolution, and they arise when modification of a trait improves one aspect of performance but incurs a cost in another. Here we show that performance costs that result from competing demands on one trait can be mitigated by compensatory changes in other traits, so long as performance has a complex basis. Numerical simulations indicate that increases in the number of traits that determine performance decrease the strength of performance trade-offs. In centrarchid fishes, multiple traits underlie suction feeding performance, and experimental data and hydrodynamic modeling show that combinations of traits evolve to increase the ability to feed on attached prey while mitigating costs to performance on evasive prey. Diet data for centrarchid species reveal a weak trade-off between these prey types, corroborating the results based on hydrodynamic modeling and suggesting that complexity in the functional basis of suction feeding performance enhances trophic diversification. Complexity may thus permit the evolution of combinations of high-performance behaviors that appear to violate underlying trade-offs, such as the ability to exert high suction forces with large gape. This phenomenon may promote morphological, functional, and ecological diversification in the face of the myriad selective demands organisms encounter.

Notes and References

This item contains 79 references.

Literature Cited
  • ['Adamowicz, S. J., A. Purvis, and M. A. Wills. 2008. Increasing morphological complexity in multiple parallel lineages of the Crustacea. Proceedings of the National Academy of Sciences of the USA 105:4786–4791.']
  • ['Alfaro, M. E., D. I. Bolnick, P. C. Wainwright, and J. Wiens. 2004. Evolutionary dynamics of complex biomechanical systems: an example using the four-bar mechanism. Evolution 58:495–503.']
  • ['Alfaro, M. E., D. I. Bolnick, and P. C. Wainwright. 2005. Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. American Naturalist 165:E140–E154.']
  • ['Arnold, S. J. 1983. Morphology, performance, and fitness. American Zoologist 23:347–361.']
  • ['Arnott, S. A., D. M. Neil, and A. D. Ansell. 1999. Escape trajectories of the brown shrimp Crangon crangon, and a theoretical consideration of initial escape angles from predators. Journal of Experimental Biology 202:193–209.']
  • ['Avise, J. C., and F. J. Ayala. 2007. In the light of evolution I: adaptation and complex design. Proceedings of the National Academy of Sciences of the USA 104:8563–8566.']
  • ['Bauwens, D., T. Garland Jr., A. M. Castilla, and R. Van Damme. 1995. Evolution of sprint speed in lacertid lizards: morphological, physiological, and behavioral covariation. Evolution 49:848–863.']
  • ['Bellwood, D. R., P. C. Wainwright, C. J. Fulton, and A. S. Hoey. 2006. Functional versatility supports coral reef biodiversity. Proceedings of the Royal Society B: Biological Sciences 273:101–107.']
  • ['Bennett, A. F., and R. E. Lenski. 2007. An experimental test of evolutionary trade-offs during temperature adaptation. Proceedings of the National Academy of Sciences of the USA 104:8649–8654.']
  • ['Buskey, E. J., P. H. Lenz, and D. K. Hartline. 2002. Escape behavior of planktonic copepods in response to hydrodynamic disturbances: high speed video analysis. Marine Ecology Progress Series 235:135–146.']
  • ['Carroll, A. M., and P. C. Wainwright. 2009. Energetic limitations on suction feeding performance in centrarchid fishes. Journal of Experimental Biology 212:3241–3251.']
  • ['Carroll, A. M., P. C. Wainwright, S. H. Huskey, D. C. Collar, and R. G. Turingan. 2004. Morphology predicts suction feeding performance in centrarchid fishes. Journal of Experimental Biology 207:3873–3881.']
  • ['Carroll, S. B. 2001. Chance and necessity: the evolution of morphological complexity and diversity. Nature 409:1102–1109.']
  • ['Chung, W.-Y., R. Albert, I. Albert, A. Nekrutenko, and K. Makova. 2006. Rapid and asymmetric divergence of duplicate genes in the human gene coexpression network. BMC Bioinformatics 7:46.']
  • ['Cohen, J. 1988. Statistical power analysis for the behavioral sciences. Erlbaum, Hillsdale, NJ.']
  • ['Collar, D. C., and P. C. Wainwright. 2006. Discordance between morphological and mechanical diversity in the feeding mechanism of centrarchid fishes. Evolution 60:2575–2584.']
  • ['Collar, D. C., B. C. O’Meara, P. C. Wainwright, and T. J. Near. 2009. Piscivory limits diversification of feeding morphology in centrarchid fishes. Evolution 63:1557–1573.']
  • ['Day, S. W., T. E. Higham, A. Y. Cheer, and P. C. Wainwright. 2005. Spatial and temporal patterns of water flow generated by suction-feeding bluegill sunfish Lepomis macrochirus resolved by particle image velocimetry. Journal of Experimental Biology 208:2661–2671.']
  • ['Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1–15.']
  • ['Ferry-Graham, L., P. Wainwright, M. Westneat, and D. Bellwood. 2002. Mechanisms of benthic prey capture in wrasses (Labridae). Marine Biology 141:819–830.']
  • ['Friel, J. P., and P. C. Wainwright. 1997. A model system of structural duplication: homologies of adductor mandibulae muscles in tetraodontiform fishes. Systematic Biology 46:441–463.']
  • ['Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19:207–233.']
  • ['Garland, T., Jr., P. H. Harvey, and A. R. Ives. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology 41:18–32.']
  • ['Gatesy, S. M., and K. M. Middleton. 1997. Bipedalism, flight, and the evolution of theropod locomotor diversity. Journal of Vertebrate Paleontology 17:308–329.']
  • ['Ghalambor, C. K., J. A. Walker, and D. N. Reznick. 2003. Multi-trait selection, adaptation, and constraints on the evolution of burst swimming performance. Integrative and Comparative Biology 43:431–438.']
  • ['Ghalambor, C. K., D. N. Reznick, and J. A. Walker. 2004. Constraints on adaptive evolution: the functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata). American Naturalist 164:38–50.']
  • ['Hazen, R. M., P. L. Griffin, J. M. Carothers, and J. W. Szostak. 2007. Functional information and the emergence of biocomplexity. Proceedings of the National Academy of Sciences of the USA 104:8574–8581.']
  • ['Herrel, A., J. C. O. Reilly, and A. M. Richmond. 2002. Evolution of bite performance in turtles. Journal of Evolutionary Biology 15:1083–1094.']
  • ['Herrel, A., J. Podos, B. Vanhooydonck, and A. P. Hendry. 2009. Force-velocity trade-off in Darwin’s finch jaw function: a biomechanical basis for ecological speciation? Functional Ecology 23:119–125.']
  • ['Higham, T. E., S. W. Day, and P. C. Wainwright. 2006a. Multidimensional analysis of suction feeding performance in fishes: fluid speed, acceleration, strike accuracy and the ingested volume of water. Journal of Experimental Biology 209:2713–2725.']
  • ['———. 2006b. The pressures of suction feeding: the relation between buccal pressure and induced fluid speed in centrarchid fishes. Journal of Experimental Biology 209:3281–3287.']
  • ['Holzman, R., and P. C. Wainwright. 2009. How to surprise a copepod: strike kinematics reduce hydrodynamic disturbance and increase stealth of suction-feeding fish. Limnology and Oceanography 54:2201–2212.']
  • ['Holzman, R., S. W. Day, and P. C. Wainwright. 2007. Timing is everything: coordination of strike kinematics affects the force exerted by suction feeding fish on attached prey. Journal of Experimental Biology 210:3328–3336.']
  • ['Holzman, R., S. W. Day, R. S. Mehta, and P. C. Wainwright. 2008a. Integrating the determinants of suction feeding performance in centrarchid fishes. Journal of Experimental Biology 211:3296–3305']
  • ['———. 2008b. Jaw protrusion enhances forces exerted on prey by suction feeding fishes. Journal of the Royal Society, Interface 5:1445–1457.']
  • ['Holzman, R., D. C. Collar, S. W. Day, K. L. Bishop, and P. C. Wainwright. 2008c. Scaling of suction-induced flows in bluegill: morphological and kinematic predictors for the ontogeny of feeding performance. Journal of Experimental Biology 211:2658–2668.']
  • ['Huckins, C. J. F. 1997. Functional linkages among morphology, feeding performance, diet, and competitive ability in molluscivorous sunfish. Ecology 78:2401–2414.']
  • ['Hughes, A., and R. Friedman. 2005. Gene duplication and the properties of biological networks. Journal of Molecular Evolution 61:758–764.']
  • ['Hulsey, C. D., and P. C. Wainwright. 2002. Projecting mechanics into morphospace: disparity in the feeding system of labrid fishes. Proceedings of the Royal Society B: Biological Sciences 269:317–326.']
  • ['Jayne, B. C., and A. F. Bennett. 1990. Selection on locomotor performance capacity in a natural population of garter snakes. Evolution 44:1204–1229.']
  • ['Keast, A. 1985. The piscivore feeding guild of fishes in small fresh-water ecosystems. Environmental Biology of Fishes 12:119–129.']
  • ['Koehl, M. A. R. 1996. When does morphology matter? Annual Review of Ecology and Systematics 27:501–542.']
  • ['Lauder, G. V. 1980. Hydrodynamics of prey capture in teleost fishes. Pages 161–181 in D. Schenck, ed. Biofluid mechanics. Plenum, New York.']
  • ['———. 1985. Aquatic feeding in lower vertebrates. Pages 210–229 in M. Hildebrand, D. M. Bramble, K. F. Liem, and D. B. Wake, eds. Functional vertebrate morphology. Harvard University Press, Cambridge, MA.']
  • ['———. 1990. Functional morphology and systematics: studying functional patterns in an historical context. Annual Review of Ecology and Systematics 21:317.']
  • ['Lenz, P. H., and D. K. Hartline. 1999. Reaction times and force production during escape behavior of a calanoid copepod, Undinula vulgaris. Marine Biology 133:249–258.']
  • ['Liem, K. F. 1973. Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Systematic Zoology 22:425–441.']
  • ['———. 1984. Functional versatility, speciation and niche overlap: are fishes different? Pages 269–305 in D. G. Meyers and J. R. Strickler, eds. Trophic interactions within aquatic ecosystems. AAAS Selected Symposium 85. Westview, Boulder, CO.']
  • ['———. 1990. Aquatic versus terrestrial feeding modes: possible impacts on the trophic ecology of vertebrates. American Zoologist 30:209–221.']
  • ['Lynch, M., and J. S. Conery. 2003. The origins of genome complexity. Science 302:1401–1404.']
  • ['McShea, D. W. 1996. Metazoan complexity and evolution: is there a trend? Evolution 50:477–492.']
  • ['Muller, M., J. W. M. Osse, and J. H. G. Verhagen. 1982. A quantitative hydrodynamical model of suction feeding in fish. Journal of Theoretical Biology 95:49–79.']
  • ['Near, T. J., D. I. Bolnick, and P. C. Wainwright. 2005. Fossil calibrations and molecular divergence time estimates in centrarchid fishes (Teleostei: Centrarchidae). Evolution 59:1768–1782.']
  • ['Norton, S. F., and E. L. Brainerd. 1993. Convergence in the feeding mechanics of ecomorphologically similar species in the Centrarchidae and Cichlidae. Journal of Experimental Biology 176:11–29.']
  • ['Osse, J. W. M. 1969. Functional morphology of the head of the perch (Perca fluviatilis L.): an electromyographic study. Netherlands Journal of Zoology 19:289–392.']
  • ['R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.']
  • ['Rice, A. 2008. Coordinated mechanics of feeding, swimming, and eye movements in Tautoga onitis, and implications for the evolution of trophic strategies in fishes. Marine Biology 154:255–267.']
  • ['Rice, S. H. 2004. Developmental associations between traits: covariance and beyond. Genetics 166:513–526.']
  • ['Robinson, B. W., and D. S. Wilson. 1998. Optimal foraging, specialization, and a solution to Liem’s paradox. American Naturalist 151:223–235.']
  • ['Schluter, D. 1995. Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth. Ecology 76:82–90.']
  • ['Svanback, R., P. C. Wainwright, and L. A. Ferry-Graham. 2002. Linking cranial kinematics, buccal pressure, and suction feeding performance in largemouth bass. Physiological and Biochemical Zoology 75:532–543.']
  • ['Titelman, J. 2001. Swimming and escape behavior of Copepod nauplii: implications for predator-prey interactions among copepods. Marine Ecology Progress Series 213:203–213.']
  • ['Toro, E., A. Herrel, and D. Irschick. 2004. The evolution of jumping performance in Caribbean Anolis lizards: solutions to biomechanical trade-offs. American Naturalist 163:844–856.']
  • ['Van Damme, R., P. Aerts, and B. Vanhooydonck. 1997. No trade-off between sprinting and climbing in two populations of the lizard Podarcis hispanica (Reptilia: Lacertidae). Biological Journal of the Linnean Society 60:493–503.']
  • ['Van Wassenbergh, S., and P. Aerts. 2009. Aquatic suction feeding dynamics: insights from computational modelling. Journal of the Royal Society, Interface 6:149–158.']
  • ['Van Wassenbergh, S., P. Aerts, and A. Herrel. 2006b. Scaling of suction feeding performance in the catfish Clarias gariepinus. Physiological and Biochemical Zoology 79:43–56.']
  • ['Vogel, S. 1994. Life in moving fluids. Princeton University Press, Princeton, NJ.']
  • ['Wainwright, P. C. 2007. Functional versus morphological diversity in macroevolution. Annual Review of Ecology Evolution and Systematics 38:381–401.']
  • ['Wainwright, P. C., and D. R. Bellwood. 2002. Ecomorphology of feeding in coral reef fishes. Pages 33–55 in P. F. Sale, ed. Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, CA.']
  • ['Wainwright, P. C., and S. W. Day. 2007. The forces exerted by aquatic suction feeders on their prey. Journal of the Royal Society, Interface 4:553–560.']
  • ['Wainwright, P. C., and B. A. Richard. 1995. Scaling the feeding mechanism of the largemouth bass (Micropterus salmoides): motor pattern. Journal of Experimental Biology 198:1161–1171.']
  • ['Wainwright, P. C., L. A. Ferry-Graham, T. B. Waltzek, A. M. Carroll, C. D. Hulsey, and J. R. Grubich. 2001. Evaluating the use of ram and suction during prey capture by cichlid fishes. Journal of Experimental Biology 204:3039–3051.']
  • ['Wainwright, P. C., A. M. Carroll, D. C. Collar, S. W. Day, T. E. Higham, and R. Holzman. 2007. Suction feeding mechanics, performance, and diversity in fishes. Integrative and Comparative Biology 47:96–106.']
  • ['Walker, J. A. 2007. A general model of functional constraints on phenotypic evolution. American Naturalist 170:681–689.']
  • ['Weihs, D., and P. W. Webb. 1984. Optimal avoidance and evasion tactics in predator-prey interactions. Journal of Theoretical Biology 106:189–206.']
  • ['Werner, E. E. 1977. Species packing and niche complementarity in three sunfishes. American Naturalist 111:553–578.']
  • ['Westneat, M. W. 1995. Feeding, function, and phylogeny: analysis of historical biomechanics in labrid fishes using comparative methods. Systematic Biology 44:361–383.']
  • ['———. 2001. Functional morphology and physiology: comparative methods. Encyclopedia of Life Sciences. Wiley Interscience, doi:10.1038/npg.els.0001817.']
  • ['Westneat, M. W., M. E. Alfaro, P. C. Wainwright, D. R. Bellwood, J. R. Grubichl, J. L. Fessler, K. D. Clements, et al. 2005. Local phylogenetic divergence and global evolutionary convergence of skull function in reef fishes of the family Labridae. Proceedings of the Royal Society B: Biological Sciences 272:993–1000.']