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5 - A focus on both form and function in examining selection versus constraint

Published online by Cambridge University Press:  28 June 2009

Manfred D. Laubichler
Arizona State University
Jane Maienschein
Arizona State University
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One of the challenges for a modern integrative biology is to more fully understand why assemblages of related species occupy morphospace in the way they do. An integration of analyses of both form and function is required to achieve this goal. The burgeoning understanding of development in emerging model species is providing evolutionary biologists with the potential to explore contributions to the evolution of patterns in morphospace by the processes involved in making variation in forms as well as those resulting from their performance in natural environments. Such an approach is illustrated here by drawing on work on butterfly eyespot patterns and scaling relationships. Relevant studies are being performed in some other groups of animals (see Brakefield 2006), and progress is also being made in plants (see Langlade et al. 2005; Niklas, ch. 3 in this volume).

Patterns in morphospace have always fascinated biologists, especially when they are known to reflect adaptive radiation among new ecological niches. In such examples, while there can be no doubt that natural selection plays a major role in shaping the evolution of morphological diversity and disparity, it is by no means clear how much the processes involved in generating variation in the phenotype to be screened by the natural selection also contribute. Thus, the extent to which evolution by natural selection of adaptations to local environments is compromised or biased by the genetical and developmental origins of phenotypic variation remains an open issue.

Publisher: Cambridge University Press
Print publication year: 2009

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Allen, C., Beldade, P., Zwaan, B. J., and Brakefield, P. M. (2008). Differences in the selection response of serially repeated color pattern characters: standing variation, development, and evolution. BMC Evolutionary Biology 8, 94.CrossRefGoogle ScholarPubMed
Arthur, W. (2001). Developmental drive: an important determinant of the direction of phenotypic evolution. Evolution & Development 3, 271–8.CrossRefGoogle ScholarPubMed
Beldade, P. and Brakefield, P. M. (2002). The genetics and evo-devo of butterfly wing patterns. Nature Reviews Genetics 3, 442–52.CrossRefGoogle ScholarPubMed
Beldade, P., Brakefield, P. M., and Long, A. D. (2005). Generating phenotypic variation: prospects from ‘evo-devo’ research on Bicyclus anynana wing patterns. Evolution & Development 7, 101–7.CrossRefGoogle ScholarPubMed
Beldade, P., Koops, K., and Brakefield, P. M. (2002). Developmental constraints versus flexibility in morphological evolution. Nature 416, 844–7.CrossRefGoogle ScholarPubMed
Beldade, P., Koops, K., and Brakefield, P. M. (2003). Modularity, individuality, and evo-devo in butterfly wings. Proceedings of the National Academy of Sciences USA 99, 14262–7.CrossRefGoogle Scholar
Blows, M. W. and Hoffmann, A. A. (2005). A reassessment of genetic limits to evolutionary change. Ecology 86, 1371–84.CrossRefGoogle Scholar
Boulding, E. G. and Hay, T. K. (1993). Quantitative genetics of shell form of an intertidal snail: constraints on short-term response to selection. Evolution 47, 576–92.CrossRefGoogle ScholarPubMed
Brakefield, P. M. (1998). The evolution–development interface and advances with the eyespot patterns of Bicyclus butterflies. Heredity 80, 265–72.CrossRefGoogle Scholar
Brakefield, P. M. (2006). Evo-devo and constraints on selection. Trends in Ecology & Evolution 21, 362–8.CrossRefGoogle ScholarPubMed
Brakefield, P. M. and Frankino, W. A. (2008). Polyphenisms in Lepidoptera: multidisciplinary approaches to studies of evolution. In Whitman, D. W. and Ananthakrishnan, T. N. (eds.), Phenotypic Plasticity of Insects: Mechanisms and Consequences. Plymouth: Science Publishers, Inc., pp. 121–51.Google Scholar
Brakefield, P. M. and French, V. (2006). Evo-devo focus issue. Heredity 97, 137–8.CrossRefGoogle Scholar
Brakefield, P. M. and Roskam, J. C. (2006). Exploring evolutionary constraints is a task for an integrative evolutionary biology. The American Naturalist 168, S4–S13.CrossRefGoogle ScholarPubMed
Breuker, C. J. and Brakefield, P. M. (2002). Female choice depends on size but not symmetry of dorsal eyespots in the butterfly Bicyclus anynana. Proceedings of the Royal Society London B: Biological Sciences 269, 1233–9.CrossRefGoogle Scholar
Brunetti, C. R., Selegue, J. E., Monteiro, A., French, V., Brakefield, P. M., and Carroll, S. B. (2001). The generation and diversification of butterfly eyespot color patterns. Current Biology 11, 1578–85.CrossRefGoogle ScholarPubMed
Cain, A. J. (1977). Variation in the spire index of some coiled gastropod shells, and its evolutionary significance. Philos Trans R Soc Lond B Biol Sci 277, 333–424.CrossRefGoogle ScholarPubMed
Cain, A. J. (1981). Variation in shell shape and size of helicid snails in relation to other Pulmonates in faunas of the Palaeacrtic region. Malacologia 21, 149–76.Google Scholar
Cain, A. J. and Sheppard, P. M. (1954). Natural selection in Cepaea. Genetics 39, 89–116.Google ScholarPubMed
Carroll, S. B., Gates, J., Keys, D., Paddock, S. W., Panganiban, G. F., Selegue, J., and Williams, J. A. (1994). Pattern formation and eyespot determination in butterfly wings. Science 265, 109–14.CrossRefGoogle ScholarPubMed
Carroll, S. B., Grenier, J. K., and Weatherbee, S. D. (2005). From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design. Oxford: Blackwell Scientific.Google Scholar
Ciampaglio, C. N., Kemp, M., and McShea, D. W. (2001). Paleobiology 27, 695–715.2.0.CO;2>CrossRef
Cook, L. M. (1990). Differences in shell properties between morphs of Littoraria pallescens. Hydrobiologia 193, 217–21.CrossRefGoogle Scholar
Cowie, R. H. (1995). Variation in species diversity and shell shape in Hawaiian land snails: in situ speciation and ecological relationships. Evolution 49, 1191–202.CrossRefGoogle ScholarPubMed
Dawkins, R. (1989). The evolution of evolvability. In Langton, C. (ed.), Artificial Life. Redwood City, CA: Addison-Wesley, pp. 201–20.Google Scholar
Frankino, W. A., Zwaan, B. J., Stern, D. L., and Brakefield, P. M. (2005). Natural selection and developmental constraints in the evolution of allometries. Science 307, 718–20.CrossRefGoogle ScholarPubMed
Frankino, W. A., Zwaan, B. J., Stern, D. L. and Brakefield, P. M. (2007). Internal and external constraints in the evolution of allometries among morphological traits in a butterfly. Evolution 61(12), 2958–7.CrossRefGoogle Scholar
French, V. and Brakefield, P. M. (1995). Eyespot development on butterfly wings: the focal signal. Developmental Biology 168, 112–23.CrossRefGoogle ScholarPubMed
Galant, R., Skeath, J. B., Paddock, S., Lewis, D. L., and Carroll, S. B. (1998). Expression of an achaete-scute homolog during butterfly scale development reveals the homology of insect scales and sensory bristles. Current Biology 8, 807–13.CrossRefGoogle ScholarPubMed
Gittenberger, A. (2006). The evolutionary history of parasitic gastropods and their coral hosts in the Indo-Pacific. Ph.D. thesis, Leiden University, The Netherlands.
Goodfriend, G. A. (1986). Variation in land snail shell form and size and its causes: a review. Systematic Zoology 35, 204–23.CrossRefGoogle Scholar
Jablonski, D. (2005). Evolutionary innovations in the fossil record: the intersection of ecology, development and macroevolution. Journal of Experimental Zoology. Part B. Molecular and Developmental Evolution 304B, 504–19.CrossRefGoogle Scholar
Joron, M. and Brakefield, P. M. (2003). Captivity masks inbreeding effects on male mating success in butterflies. Nature 424, 191–4.CrossRefGoogle ScholarPubMed
Joron, M., Jiggins, C. D., Papanicolaou, A., and McMillan, W. O. (2006). Heliconius wing patterns: an evo-devo model for understanding phenotypic diversity. Heredity 97, 157–67.CrossRefGoogle ScholarPubMed
Kauffmann, S. A. (1985). Self-organisation, selective adaptation, and its limits. In Depew, D. J. and Weber, B. H. (eds.), Evolution at a Crossroads. Cambridge, MA: MIT Press, pp. 169–207.Google Scholar
Keys, D. N., Lewis, D. L., Selegue, J. E., Pearson, B. J., Goodrich, L. V., Johnson, R. L., Gates, J., Scott, M. P., and Carroll, S. B. (1999). Recruitment of a Hedgehog regulatory circuit in butterfly eyespot evolution. Science 283, 532–4.CrossRefGoogle ScholarPubMed
Kirschner, M. and Gerhart, J. (1998). Evolvability. Proceedings of the National Academy of Sciences USA 95, 8420–7.CrossRefGoogle ScholarPubMed
Langlade, N. B., Feng, X., Dransfield, T., Copsey, L., Hanna, A. I., Thebaud, C., Bangham, A., Hudson, A., and Coen, E. (2005). Evolution through genetically controlled allometry space. Proceedings of the National Academy of Sciences USA 102, 10221–6.CrossRefGoogle ScholarPubMed
Maynard Smith, J., Burian, R., Kaufman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Raup, D., and Wolpert, L. (1985). Developmental constraints and evolution. Quarterly Review of Biology 60, 265–87.CrossRefGoogle Scholar
McClain, C. R. (2005). Bathymetric patterns of morphological disparity in deep-sea gastropods from the western North Atlantic Basin. Evolution 59, 1492–9.CrossRefGoogle ScholarPubMed
McClain, C. R., Johnson, N. A., and Rex, M. A. (2004). Morphological disparity as a biodiversity metric in lower bathyal and abyssal gastropod assemblages. Evolution 58, 338–48.Google ScholarPubMed
McGhee, G. R. (1999). Theoretical Morphology. New York: Columbia University Press.Google Scholar
McGhee, G. R. (2007). The Geometry of Evolution: Adaptive Landscapes and Theoretical Morphospaces. Cambridge: Cambridge University Press.Google Scholar
Monteiro, A., Brakefield, P. M., and French, V. (1994). The evolutionary genetics and developmental basis of wing pattern variation in the butterfly Bicyclus anynana. Evolution 48, 1147–57.CrossRefGoogle ScholarPubMed
Monteiro, A., Brakefield, P. M., French, V. (1997). Butterfly eyespots: the genetics and development of the color rings. Evolution 51, 1207–16.CrossRefGoogle ScholarPubMed
Nijhout, H. F. (1991). The Development and Evolution of Butterfly Wing Patterns. Washington, DC: Smithsonian Institute Press.Google Scholar
Raup, D. M. (1966). Geometric analysis of shell coiling: general problems. Journal of Paleontology 40, 1178–90.Google Scholar
Raup, D. M. (1967). Geometric analysis of shell coiling: coiling in ammonoids. Journal of Paleontology 41, 43–65.Google Scholar
Reed, R. D., and Serfas, M. S. (2004). Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process. Current Biology 14, 1159–66.CrossRefGoogle Scholar
Ridley, M. (2003). Evolution (third edition). Oxford: Blackwell Publishing.
Robertson, K. A. and Monteiro, A. (2005). Female Bicyclus anynana butterflies choose males on the basis of their dorsal UV-reflective eyespot pupils. Proceedings of the Royal Society London B: Biological Sciences 272, 1541–6.CrossRefGoogle ScholarPubMed
Saenko, S. V., French, V., Brakefield, P. M., and Beldade, P. (2008). Conserved developmental processes and the formation of evolutionary novelties: examples from butterfly wings. Philos Trans R Soc Lond B Biol Sci 363, 1549–55.CrossRefGoogle ScholarPubMed
Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution 50, 1766–74.CrossRefGoogle ScholarPubMed
Stevens, M. (2005). The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera. Biological Reviews 80, 573–88.CrossRefGoogle ScholarPubMed
Stone, J. R. (1996). Computer-simulated shell size and shape variation in the Caribbean land snail genus Cerion: a test of geometrical constraints. Evolution 50, 341–7.Google ScholarPubMed
Thompson, J. N. (2005). The Geographic Mosaic of Coevolution. University of Chicago Press.Google Scholar
Via, S. and Lande, R. (1985). Genotype–environment interaction and the evolution of phenotypic plasticity. Evolution 39, 505–22.CrossRefGoogle ScholarPubMed
Wagner, A. (2005). Robustness and Evolvability in Living Systems. New Jersey: Princeton University Press.Google Scholar
Wagner, G. P. and Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution 50, 967–76.CrossRefGoogle ScholarPubMed
Wagner, P. J. (1995). Testing evolutionary constraint hypotheses with early Paleozoic gastropods. Paleobiology 21, 248–72.CrossRefGoogle Scholar
Wagner, P. J. and Erwin, D. H. (2006). Patterns of convergence in general shell form among Paleozoic gastropods. Paleobiology 32, 316–37.CrossRefGoogle Scholar
Weatherbee, S. D., Nijhout, H. F., Halder, G., Galant, R., Selegue, J., and Carroll, S. B. (1999). Ultrabithorax function in butterfly wings and the evolution of insect wing patterns. Current Biology 9, 109–15.CrossRefGoogle ScholarPubMed

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