Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-24T01:43:40.890Z Has data issue: false hasContentIssue false
  • English
  • Français

Evolutionary modifications of ontogeny: heterochrony and beyond

Published online by Cambridge University Press:  08 April 2016

Mark Webster  and
Miriam Leah Zelditch
Mark Webster
Affiliation:
Department of the Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue, Chicago, Illinois 60637. E-mail: [email protected]
Miriam Leah Zelditch
Affiliation:
Museum of Paleontology, University of Michigan, Ann Arbor, Michigan 48109-1079
Get access Rights & Permissions [Opens in a new window]

Abstract

Consideration of the ways in which ontogenetic development may be modified to give morphological novelty provides a conceptual framework that can greatly assist in formulating and testing hypotheses of patterns and constraints in evolution. Previous attempts to identify distinct modes of ontogenetic modification have been inconsistent or ambiguous in definition, and incomprehensive in description of interspecific morphological differences. This has resulted in a situation whereby almost all morphological evolution is attributed to heterochrony, and the remainder is commonly either assigned to vague or potentially overly inclusive alternative classes, or overlooked altogether.

The present paper recognizes six distinct modes of ontogenetic change, each a unique modification to morphological development: (1) rate modification, (2) timing modification, (3) heterotopy, (4) heterotypy, (5) heterometry, and (6) allometric repatterning. Heterochrony, modeled in terms of shape /time /size ontogenetic parameters, relates to parallelism between ontogenetic and phylogenetic shape change and results from a rate or timing modification to the ancestral trajectory of ontogenetic shape change. Loss of a particular morphological feature may be described in terms of timing modification (extreme postdisplacement) or heterometry, depending on the temporal development of the feature in the ancestor. Testing hypotheses of the operation of each mode entails examining the morphological development of the ancestor and descendant by using trajectory-based studies of ontogenetically dynamic features and non-trajectory-based studies of ontogenetically static features.

The modes identified here unite cases based on commonalities of observed modification to the process of morphological development at the structural scale. They may be heterogeneous or partially overlapping with regard to changes to genetic and cellular processes guiding development, which therefore require separate treatment and terminology. Consideration of the modes outlined here will provide a balanced framework within which questions of evolutionary change and constraint within phylogenetic lineages can be addressed more meaningfully.

Type
Articles
Information
Paleobiology , Volume 31 , Issue 3 , Summer 2005 , pp. 354 - 372
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Abzhanov, A., and Kaufman, T. C. 1999. Novel regulation of the homeotic gene Scr associated with a crustacean leg-to-max-illiped appendage transformation. Development 126:1121–1128.Google Scholar
Akam, M., Averof, M., Castelli-Gair, J., Dawes, R., Falciani, F., and Ferrier, D. 1994. The evolving role of Hox genes in arthropods. Development 1994(Suppl.):209–215.Google Scholar
Alberch, P. 1985. Problems with the interpretation of developmental sequences. Systematic Zoology 34:46–58.Google Scholar
Alberch, P., and Blanco, M. J. 1996. Evolutionary patterns in ontogenetic transformation: from laws to regularities. International Journal of Developmental Biology 40:845–858.Google Scholar
Alberch, P., Gould, S. J., Oster, G. F., and Wake, D. B. 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5:296–317.Google Scholar
Arthur, W. 2000. The concept of developmental reprogramming and the quest for an inclusive theory of evolutionary mechanisms. Evolution and Development 2:49–57.Google Scholar
Atchley, W. R. 1987. Developmental quantitative genetics and the evolution of ontogenies. Evolution 41:316–330.CrossRefGoogle ScholarPubMed
Bookstein, F. L. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, New York.Google Scholar
Brochu, C. A. 1995. Heterochrony in the crocodylian scapulocoracoid. Journal of Herpetology 29:464–468.Google Scholar
Carroll, S. B. 1994. Developmental regulatory mechanisms in the evolution of insect diversity. Development 1994(Suppl.):217–223.Google Scholar
Edgecombe, G. D., and Chatterton, B. D. E. 1987. Heterochrony in the Silurian radiation of encrinurine trilobites. Lethaia 20:337–351.Google Scholar
Fink, W. L. 1982. The conceptual relationship between ontogeny and phylogeny. Paleobiology 8:254–264.Google Scholar
Fink, W. L. 1988. Phylogenetic analysis and the detection of ontogenetic patterns. Pp. 71–91in McKinney, M. L., ed. Heterochrony in evolution: a multidisciplinary approach. Plenum, New York.Google Scholar
Gellon, G., and McGinnis, W. 1998. Shaping animal body plans in development and evolution by modulation of Hox expression patterns. BioEssays 20:116–125.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Godfrey, L. R., and Sutherland, M. R. 1995. What's growth got to do with it? Process and product in the evolution of ontogeny. Journal of Human Evolution 29:405–431.Google Scholar
Godfrey, L. R., and Sutherland, M. R. 1996. Paradox of peramorphic paedomorphosis: heterochrony and human evolution. American Journal of Physical Anthropology 99:17–42.Google Scholar
Gould, S. J. 1977. Ontogeny and phylogeny. Harvard University Press, Cambridge.Google Scholar
Gould, S. J. 2000. Of coiled oysters and big brains: how to rescue the terminology of heterochrony, now gone astray. Evolution and Development 2:241–248.Google Scholar
Haeckel, E. 1875. Die Gastrula und die Eifurchung der Thiere. Jenaische Zeitschrift für Naturwissenschaft 9:402–508.Google Scholar
Halder, G., Callaerts, P., and Gehring, W. J. 1995. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267:1788–1792.Google Scholar
Hughes, N. C., and Chapman, R. E. 1995. Growth and variation in the Silurian proetide trilobite Aulacopleura konincki and its implications for trilobite paleobiology. Lethaia 28:333–353.Google Scholar
Hughes, N. C., Chapman, R. E., and Adrain, J. M. 1999. The stability of thoracic segmentation in trilobites: a case study in developmental and ecological constraints. Evolution and Development 1:24–35.Google Scholar
Jaecks, G. S., and Carlson, S. J. 2001. How phylogenetic inference can shape our view of heterochrony: examples from thecideide brachiopods. Paleobiology 27:205–225.Google Scholar
Kettle, C., Arthur, W., Jowett, T., and Minelli, A. 1999. Homeotic transformation in a centipede. Trends in Genetics 15:393.Google Scholar
Kjaer, C. R., and Thomsen, E. 1999. Heterochrony in bourgue-ticrinid sea-lilies at the Cretaceous/Tertiary boundary. Paleobiology 25:29–40.Google Scholar
Klingenberg, C. P. 1998. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biological Reviews 73:79–123.CrossRefGoogle ScholarPubMed
Lewis, E. B. 1978. A gene complex controlling segmentation in Drosophila. Nature 276:565–570.Google Scholar
Li, P., and Johnston, M. O. 2000. Heterochrony in plant evolutionary studies through the twentieth century. Botanical Review 66:57–88.Google Scholar
Lovejoy, C. O., Cohn, M. J., and White, T. D. 1999. Morphological analysis of the mammalian postcranium: a developmental perspective. Proceedings of the National Academy of Sciences USA 96:13247–13252.CrossRefGoogle ScholarPubMed
McKinney, M. L. 1999. Heterochrony: beyond words. Paleobiology 25:149–153.Google Scholar
McKinney, M. L., and McNamara, K. J. 1991. Heterochrony: the evolution of ontogeny. Plenum, New York.Google Scholar
McNamara, K. J. 1978. Paedomorphosis in Scottish olenellid trilobites. Palaeontology 21:635–655.Google Scholar
McNamara, K. J. 1981. The role of paedomorphosis in the evolution of Cambrian trilobites. U.S. Geological Survey Open-File Report 81;c- 743:126–129.Google Scholar
McNamara, K. J. 1983. Progenesis in trilobites. Special Papers in Palaeontology 30:59–68.Google Scholar
McNamara, K. J. 1986a. A guide to the nomenclature of heterochrony. Journal of Paleontology 60:4–13.Google Scholar
McNamara, K. J. 1986b. The role of heterochrony in the evolution of Cambrian trilobites. Biological Reviews 6:121–156.Google Scholar
McNamara, K. J. 1988. The abundance of heterochrony in the fossil record. Pp. 287–325in Heterochrony in evolution: a multidisciplinary approach. McKinney, M. L., ed. Plenum, New York.Google Scholar
McNamara, K. J. 1995. Evolutionary change and heterochrony. Wiley, Chichester, U.K.Google Scholar
McNamara, K. J. 1997. Shapes of time: the evolution of growth and development. Johns Hopkins University Press, Baltimore.Google Scholar
Nedin, C., and Jenkins, R. J. F. 1999. Heterochrony in the Cambrian trilobite Hsuaspis. Alcheringa 23:1–7.Google Scholar
Nehm, R. H. 2001. The developmental basis of morphological disarmament in Prunum (Neogastropoda: Marginellidae). Pp. 1–26in Zelditch, 2001.Google Scholar
O'Keefe, F. R., Rieppel, O., and Sander, P. M. 1999. Shape dissociation and inferred heterochrony in a clade of pachypleurosaurs (Reptilia, Sauropterygia). Paleobiology 25:504–517.Google Scholar
Raff, R. A. 1996. The shape of life: genes, development, and the evolution of animal form. University of Chicago Press, Chicago.Google Scholar
Raff, R. A., and Wray, G. A. 1989. Heterochrony: developmental mechanisms and evolutionary results. Journal of Evolutionary Biology 2:409–434.Google Scholar
Regier, J. C., and Vlahos, N. S. 1988. Heterochrony and the introduction of novel modes of morphogenesis during the evolution of moth choriogenesis. Journal of Molecular Evolution 28:19–31.Google Scholar
Reilly, S. M., Wiley, E. O., and Meinhardt, D. J. 1997. An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomena. Biological Journal of the Linnean Society 60:119–143.Google Scholar
Rice, S. H. 1997. The analysis of ontogenetic trajectories: when a change in size or shape is not heterochrony. Proceedings of the National Academy of Sciences USA 94:907–912.Google Scholar
Roopnarine, P. D. 2001. Testing the hypothesis of heterochrony in morphometric data: lessons from a bivalved mollusk. Pp. 271–303in Zelditch, 2001.Google Scholar
Sattler, R. 1992. Process morphology: structural dynamics in development and evolution. Canadian Journal of Botany 70:708–714.Google Scholar
Shea, B. T. 1985. Bivariate and multivariate growth allometry: statistical and biological considerations. Journal of Zoology 206:367–390.Google Scholar
Smith, K. K. 1997. Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 51:1663–1678.Google Scholar
Smith, K. K. 2001. Heterochrony revisited: the evolution of developmental sequences. Biological Journal of the Linnean Society 73:169–186.Google Scholar
Stephen, D. A., Manger, W. L., and Baker, C. 2002. Ontogeny and heterochrony in the Middle Carboniferous ammonoid Arkanites relictus (Quinn, McCaleb, and Webb) from northern Arkansas. Journal of Paleontology 76:810–821.Google Scholar
Sundberg, F. A. 2000. Homeotic evolution in Cambrian trilobites. Paleobiology 26:258–270.Google Scholar
Takhtajan, A. 1972. Patterns of ontogenetic alterations in the evolution of higher plants. Phytomorphology 22:164–171.Google Scholar
Wagner, G. P., Chiu, C.-H., and Laubichler, M. 2000. Developmental evolution as a mechanistic science: the inference from developmental mechanisms to evolutionary processes. American Zoologist 40:819–831.Google Scholar
Wake, D. B. 1996. Evolutionary developmental biology—prospects for an evolutionary synthesis at the developmental level. Pp. 97–107in Ghiselin, M. T. and Pinna, G., eds. New perspectives on the history of life. California Academy of Sciences, San Francisco.Google Scholar
Wake, D. B., and Roth, G. 1989. The linkage between ontogeny and phylogeny in the evolution of complex systems. Pp. 361–377in Wake, D. B. and Roth, G., eds. Complex organismal functions: integration and evolution in vertebrates. Wiley, Chichester, U.K.Google Scholar
Wayne, R. W. 1986. Cranial morphology of domestic and wild canids: the influence of development on morphological change. Evolution 40:243–261.Google Scholar
Webster, M., Sheets, H. D., and Hughes, N. C. 2001. Allometric patterning in trilobite ontogeny: testing for heterochrony in Nephrolenellus. Pp. 105–144in Zelditch, 2001.Google Scholar
Wray, G. A., and McClay, D. R. 1989. Molecular heterochronies and heterotopies in early echinoid development. Evolution 43:803–813.CrossRefGoogle ScholarPubMed
Zelditch, M. L., ed. 2001. Beyond heterochrony: the evolution of development. Wiley, New York.Google Scholar
Zelditch, M. L., and Fink, W. L. 1996. Heterochrony and heterotopy: stability and innovation in the evolution of form. Paleobiology 22:241–254.Google Scholar
Zelditch, M. L., Sheets, H. D., and Fink, W. L. 2000. Spatiotemporal reorganization of growth rates in the evolution of ontogeny. Evolution 54:1363–1371.Google Scholar
Zelditch, M. L., Sheets, H. D., and Fink, W. L. 2003a. The ontogenetic dynamics of shape disparity. Paleobiology 29:139–156.Google Scholar
Zelditch, M. L., Lundigran, B. L., Sheets, H. D., and Garland, T. Jr. 2003b. Do precocial mammals develop at a faster rate? A comparison of rates of skull development in Sigmodon fulviventer and Mus musculus domesticus. Journal of Evolutionary Biology 16:708–720.Google Scholar
Zimmermann, W. 1959. Die Phylogenie der Pflanzen, 2d ed.Gustav Fischer, Jena.Google Scholar