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Heterochrony and heterotopy: stability and innovation in the evolution of form

Published online by Cambridge University Press:  14 July 2015

Miriam L. Zelditch
Affiliation:
Museum of Paleontology, University of Michigan, Ann Arbor, Michigan 48109
William L. Fink
Affiliation:
Museum of Zoology and Biology Department, University of Michigan, Ann Arbor, Michigan 48109

Abstract

Heterochrony, change in developmental rate and timing, is widely recognized as an agent of evolutionary change. Heterotopy, evolutionary change in spatial patterning of development, is less widely known or understood. Although Haeckel coined the term as a complement to heterochrony in 1866, few studies have detected heterotopy or even considered the possibility that it might play a role in morphological evolution. We here review the roles of heterochrony and heterotopy in evolution and discuss how they can be detected. Heterochrony is of interest in part because it can produce novelties constrained along ancestral ontogenies, and hence result in parallelism between ontogeny and phylogeny. Heterotopy can produce new morphologies along trajectories different from those that generated the forms of ancestors. We argue that the study of heterochrony has been bound to an analytical formalism that virtually precludes the recognition of heterotopy, so we provide a new framework for the construction of ontogenetic trajectories and illustrate their analysis in a phylogenetic context. The study of development of form needs tools that capture not only rates of development but the space in which the changes are manifest. The framework outlined here provides tools applicable to both. When appropriate tools are used and the necessary steps are taken, a more comprehensive interpretation of evolutionary change in development becomes possible. We suspect that there will be very few cases of change solely in developmental rate and timing or change solely in spatial patterning; most ontogenies evolve by changes of spatiotemporal pattern.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Alberch, P. 1985. Problems with the interpretation of developmental sequences. Systematic Zoology 34:4658.CrossRefGoogle Scholar
Alberch, P. and Alberch, J. 1981. Heterochronic mechanisms of morphological diversification and evolutionary change in the neotropical salamander Bolitoglossa occidentalis (Amphibia: Plethodontidae). Journal of Morphology 167:249264.CrossRefGoogle ScholarPubMed
Alberch, P., Gould, S. J., Oster, G. F., and Wake, D. B. 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5:296317.CrossRefGoogle Scholar
Blackstone, N. W., and Yund, P. O. 1989. Morphological variation in a colonial marine hydroid: a comparison of size-based and age-based heterochrony. Paleobiology 15:110.CrossRefGoogle Scholar
Bonner, J. T., ed. 1982. Evolution and development. Springer, New York.CrossRefGoogle Scholar
Bookstein, F. L. 1989. Principal warps: thin-plate splines and the decomposition of deformations. I. E. E. E. Transactions on Pattern Analysis and Machine Intelligence 11:567585.CrossRefGoogle Scholar
Bookstein, F. L. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, New York.Google Scholar
Budd, A. F., Johnson, K. G., and Potts, D. C. 1994. Recognizing morphospecies in colonial reef corals: I. Landmark-based methods. Paleobiology 20:484505.CrossRefGoogle Scholar
Brylski, P., and Hall, B. K. 1988. Ontogeny of a macroevolutionary phenotype: the external cheek pouches of geomyoid rodents. Evolution 42:391395.CrossRefGoogle ScholarPubMed
Clyde, W. C., and Gingerich, P. D. 1994. Rates of evolution in the dentition of Early Eocene Cantius: comparison of size and shape. Paleobiology 20:506522.CrossRefGoogle Scholar
Fink, W. L. 1982. The conceptual relationship between ontogeny and phylogeny. Paleobiology 8:254264.CrossRefGoogle Scholar
Fink, W. L. 1988. Phylogenetic analysis and the detection of ontogenetic patterns. pp. 7191in McKinney 1988Google Scholar
Fink, W. L., and Zelditch, M. L. 1995. Phylogenetic analysis of ontogenetic shape transformations: a reassessment of the piranha genus Pygocentrus (Teleostei). Systematic Biology 44:343360.CrossRefGoogle Scholar
Fink, W. L., and Zelditch, M. L. 1996. Historical patterns of developmental integration in piranhas. American Zoologist 36:6179.CrossRefGoogle Scholar
Gould, S. J. 1977. Ontogeny and phylogeny. Harvard University Press, Cambridge.Google Scholar
Gould, S. J. 1982. Change in developmental timing as a mechanism of macroevolution. pp. 333346in Bonner 1982.Google Scholar
Gould, S. J. 1995. A task for Paleobiology at the threshold of majority. Paleobiology 21:114.CrossRefGoogle Scholar
Haeckel, E. 1866. Generelle Morphologie der Organismen: Allgemeine Grundzüge der organischen Formen-Wissenschaft, mechanisch bergründet durch die von Charles Darwin reformirte Descendenz-Theorie. Reimer, Berlin.CrossRefGoogle Scholar
Hafner, J. C., and Hafner, M. S. 1988. Heterochrony in primates. pp. 217235in McKinney 1988.Google Scholar
Hall, B. K. 1992. Evolutionary developmental biology. Chapman and Hall, New York.CrossRefGoogle Scholar
Levinton, J. S. 1988. Genetics, paleontology and evolution. Cambridge University Press, New York.Google Scholar
Maderson, P. F. A., Alberch, P., Goodwin, B., Gould, S. J., Hoffman, A., Murray, J. D., Raup, D. M., de Ricqles, A., Seilacher, A., Wagner, G. P., and Wake, D. B. 1982. The role of development in macroevolutionary change. pp. 79312in Bonner 1982.Google Scholar
McKinney, M. L. 1988. Heterochrony in evolution: a multidisciplinary approach. Plenum, New York.CrossRefGoogle Scholar
McKinney, M. L., and McNamara, K. J. 1991. Heterochrony: the evolution of ontogeny. Plenum, New York.CrossRefGoogle Scholar
McNamara, K. J. 1987. Plate translocation in spatangoid echinoids: its morphological, functional and phylogenetic significance. Paleobiology 13:312325.CrossRefGoogle Scholar
Schweitzer, P. N., Kaesler, R. L., and Lohmann, G. P. 1986. Ontogeny and heterochrony in the ostracode Cavellina Coryell from the Lower Permian rocks in Kansas. Paleobiology 12:290301.CrossRefGoogle Scholar
Shea, B. T. 1988. Heterochrony in primates. pp. 237266in McKinney 1988.Google Scholar
Swiderski, D. L. 1994. Morphological evolution of the scapula in tree squirrels, chipmunks and ground squirrels (Sciuridae): an analysis using thin-plate splines. Evolution 47:18541873.CrossRefGoogle Scholar
Tabachnick, R. E., and Bookstein, F. L. 1990. The structure of individual variation in Miocene Globorotalia. Evolution 44:416434.CrossRefGoogle ScholarPubMed
Thacker, C. 1996. Gametogenesis in the progenetic teleost Schindleria: effects of extreme paedomorphosis. Copeia (in press).Google Scholar
Wolpert, L. 1982. Pattern formation and change. pp. 169188in Bonner 1982.Google Scholar
Wray, G. A. and McClay, D. R. 1989. Molecular heterochronies and heterotopies in early echinoid development. Evolution 43:803813.CrossRefGoogle ScholarPubMed
Zelditch, M.L., and Fink, W.L. 1995. Developmental integration and complexity of body growth in a piranha, Pygocentrus nattereri (Teleostei: Ostariophysi). Journal of Morphology 223:341355.CrossRefGoogle Scholar
Zelditch, M. L., Bookstein, F. L., and Lundrigan, B. L. 1992. Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer. Evolution 46:11641180.CrossRefGoogle ScholarPubMed
Zelditch, M. L., Fink, W. L., and Swiderski, D. L. 1995. Morphometrics, homology, and phylogenetics: Quantified characters as synapomorphies. Systematic Biology 44:179189.CrossRefGoogle Scholar