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Heterochrony, disparity, and macroevolution

Published online by Cambridge University Press:  08 April 2016

Kenneth J. McNamara
Affiliation:
Department of Earth and Planetary Sciences, Western Australian Museum, Francis Street, Perth, Western Australia 6000, Australia. E-mail: [email protected]
Michael L. McKinney
Affiliation:
Department of Earth and Planetary Sciences, University of Tennessee, Knoxville, Tennessee 37996. E-mail: [email protected]

Abstract

The concept of heterochrony has long had a central place in evolutionary theory. During their long history, heterochrony and several associated concepts such as paedomorphosis and neoteny have often been contentious and they continue to be criticized. Despite these criticisms, we review many examples showing that heterochrony and its associated concepts are increasingly cited and used in many areas of evolutionary study. Furthermore, major strides are being made in our understanding of the underlying genetic and developmental mechanisms of heterochrony, and in the methods used to describe heterochronic changes. A general theme of this accumulating research is that some of the simplistic notions of heterochrony, such as terminal addition, simple rate genes, and “pure” heterochronic categories are invalid. However, this research also shows that a more sophisticated view of the hierarchical nature of heterochrony provides many useful insights and improves our understanding of how ontogenetic changes are translated into phylogenetic changes.

Type
Generating Disparity
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Alberch, P., and Blanco, M. J. 1996. Evolutionary patterns in ontogenetic transformation: from laws to regularities. International Journal of Developmental Biology 40:845858.Google Scholar
Alberch, P., Gould, S. J., Oster, G. F., and Wake, D. B. 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5:296317.Google Scholar
Bininda-Emonds, O. R. P., Jeffery, J. E., Coates, M. I., and Richardson, M. K. 2002. From Haeckel to event-pairing: the evolution of developmental sequences. Theory in Biosciences 121:297320.Google Scholar
Bininda-Emonds, O. R. P., Jeffery, J. E., and Richardson, M. K. 2003. Inverting the hourglass: quantitative evidence against the phylotypic stage in vertebrate development. Proceedings of the Royal Society of London B 270:341346.Google Scholar
Ciampaglio, C. N., Kemp, M., and McShea, D. W. 2001. Detecting changes in morphospace occupation patterns in the fossil record: characterizations and analysis of measures of disparity. Paleobiology 27:695715.2.0.CO;2>CrossRefGoogle Scholar
Cubo, J., Azagra, D., Casinos, A., and Castanet, J. 2002. Heterochronic detection through a function for the ontogenetic variation of bone shape. Journal of Theoretical Biology 215:5766.Google Scholar
De Beer, G. R. 1930. Embryology and evolution. Clarendon, Oxford.Google Scholar
Denoel, M. 2002. Paedomorphosis in the Alpine newt (Triturus alpestris): decoupling behavioural and morphological change. Behavioral Ecology and Sociobiology 52:394399.Google Scholar
Denoel, M., and Joly, P. 2000. Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata). Proceedings of the Royal Society of London B 267:14811485.Google Scholar
Eble, G. J. 1998. The role of development in evolutionary radiations. Pp. 132161in McKinney, M. L. and Drake, J. A., eds. Biodiversity dynamics: turnover of populations, taxa, and communities. Columbia University Press, New York.Google Scholar
Eble, G. J. 2000. Contrasting evolutionary flexibility in sister groups: disparity and diversity in Mesozoic atelostomate echinoids. Paleobiology 26:5679.Google Scholar
Eble, G. J. 2002. Multivariate approaches to development and evolution. Pp. 5178in Minugh-Purvis, N. and McNamara, K. J., eds. Human evolution through developmental change. Johns Hopkins University Press, Baltimore.Google Scholar
Erikson, G. M., de Ricqlès, A., de Buffrénil, V., Molnar, R. E., and Bayless, M. K. 2003. Vermiform bones and the evolution of gigantism in Megalania—how a reptilian fox became a lion. Journal of Vertebrate Paleontology 23:966970.CrossRefGoogle Scholar
Feduccia, A. 2003. Bird origins: problem solved, but the debate continues. Trends in Ecology and Evolution 18:910.Google Scholar
Foote, M. 1997. The evolution of morphological diversity. Annual Review of Ecology and Systematics 28:129152.Google Scholar
Foote, M. 1999. Morphological diversity in the evolutionary radiation of Paleozoic and Post-Paleozoic crinoids. Paleobiology Memoirs No. 1. Paleobiology 25(Suppl. to No. 2).Google Scholar
Fortey, R. A., Briggs, D. E. G., and Wills, M. A. 1996. The Cambrian evolutionary “explosion”: decoupling cladogenesis from morphological disparity. Biological Journal of the Linnean Society 57:1333.Google Scholar
Friedman, W. E., and Carmichael, J. S. 1998. Heterochrony and developmental innovation: evolution of female gametophyte ontogeny in Gnetum, a highly apomorphic seed plant. Evolution 52:10161030.Google Scholar
Galis, F., Kundrát, M., and Sinervo, B. 2003. An old controversy solved: bird embryos have five fingers. Trends in Ecology and Evolution 18:79.Google Scholar
Gariepy, J. L., Bauer, D. J., and Cairns, R. B. 2001. Selective breeding for differential aggression in mice provides evidence for heterochrony in social behaviours. Animal Behaviour 61:933947.Google Scholar
Gould, S. J. 1977. Ontogeny and phylogeny. Belknap Press of 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 2:241248.Google Scholar
Gould, S. J. 2002. The structure of evolutionary theory. Belknap Press of Harvard University Press, Cambridge.Google Scholar
Haeckel, E. 1905. The evolution of man, 5th ed.Watts, London.Google Scholar
Hall, B. K. 1998. Evolutionary developmental biology, 2d ed.Kluwer Academic, Dordrecht, The Netherlands.Google Scholar
Hall, B. K. 2001. Foreword. Pp. viiixin Zelditch, 2001.Google Scholar
Hanken, J., and Wake, D. B. 1993. Miniaturization of body size: organismal consequences and evolutionary significance. Annual Review of Ecology and Systematics 24:501519.Google Scholar
Harvell, C. D. 1994. The evolution of polymorphism in colonial invertebrates and social insects. Quarterly Review of Biology 69:155185.Google Scholar
Holder, N. 1983. The vertebrate limb: patterns and constraints in development and evolution. Pp. 399425in Goodwin, B. C., Holder, N., and Wylie, C. C., eds. Development and evolution. Cambridge University Press, Cambridge.Google Scholar
Ivany, L. C., Wilkinson, B. H., and Jones, D. S. 2003. Using stable isotopic data to resolve rate and duration of growth throughout ontogeny: an example from the surf clam, Spisula solidissima. Palaios 18:126137.Google Scholar
Jablonski, D. 2000. Micro- and macroevolution: scale and hierarchy in evolutionary biology and paleobiology. Paleobiology 26:1552.Google Scholar
Jaecks, G. S., and Carlson, S. J. 2001. How phylogenetic inference can shape our view of heterochrony: examples from thecideide brachiopods. Paleobiology 27:205225.Google Scholar
Jeffery, J. E., Richardson, M. K., Coates, M. I., and Bininda-Emonds, O. R. P. 2002. Analyzing developmental sequences within a phylogenetic framework. Systematic Biology 51:478491.CrossRefGoogle ScholarPubMed
Jones, D. S., and Gould, S. J. 1999. Direct measurement of age in fossil Gryphaea: the solution to a classic problem in heterochrony. Paleobiology 25:158187.Google Scholar
Kellogg, E. A. 2000. The grasses: a case study in macroevolution. Annual Review of Ecology and Systematics 31:217238.Google Scholar
Kim, J., Kerr, J. Q., and Min, G. S. 2000. Molecular heterochrony in the early development of Drosophila. Proceedings of the National Academy of Sciences USA 97:212216.CrossRefGoogle ScholarPubMed
Kordikova, E. G. 2002. Heterochrony in the evolution of the shell of Chelonia. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen. 226:343417.CrossRefGoogle Scholar
Langer, M. C., Ferigolo, J., and Schultz, J. 2000. Heterochrony and tooth evolution in hyperodapedontine rhynchosaurs (Reptilia, Diapsida). Lethaia 33:119128.Google Scholar
Long, J. A. 1995. The rise of fishes. Johns Hopkins University Press, Baltimore.Google Scholar
McDonald, M. A., and Smith, M. H. 1994. Behavioral and morphological correlates of heterochrony in Hispaniolan palm tanagers. Condor 96:433446.Google Scholar
McKinney, M. L., ed. 1988. Heterochrony in evolution: a multidisciplinary approach. Plenum, New York.CrossRefGoogle Scholar
McKinney, M. L., ed. 1999. Heterochrony: beyond words. Paleobiology 25:149153.Google Scholar
McKinney, M. L., and McNamara, K. J. 1991. Heterochrony: the evolution of ontogeny. Plenum, New York.CrossRefGoogle Scholar
McNamara, K. J., ed. 1995. Evolutionary change and heterochrony. Wiley, Chichester, U.K.Google Scholar
McNamara, K. J., ed. 1997. Shapes of time: the evolution of growth and development. Johns Hopkins University Press, Baltimore.Google Scholar
McNamara, K. J., ed. 2002a. Changing times, changing places: heterochrony and heterotopy. Paleobiology 28:551558.Google Scholar
McNamara, K. J., ed. 2002b. Sequential hypermorphosis: stretching ontogeny to the limit. Pp. 102121in Minugh-Purvis, N. and McNamara, K. J., eds. Human evolution through developmental change. Johns Hopkins University Press, Baltimore.Google Scholar
Minugh-Purvis, N., and McNamara, K. J., eds. 2002. Human evolution through developmental change. Johns Hopkins University Press, Baltimore.Google Scholar
Miya, M., and Nishida, M. 1996. Molecular phylogenetic perspective on the evolution of the deep-sea fish genus Cyclothone (Stomiiformes: Gonostomatidae). Ichthyological Research 43:375398.Google Scholar
Nehm, R. H. 2001. The developmental basis of morphological disarmament in Prunum (Neogastropoda: Marginellidae). Pp. 126in Zelditch, 2001Google Scholar
Parker, S. T., and McKinney, M. L. 1999. Origins of intelligence: the evolution of cognitive development in monkey, apes, and humans. Johns Hopkins University Press, Baltimore.Google Scholar
Pasquinelli, A. E., and Ruvkun, G. 2002. Control of developmental timing by microRNAs and their targets. Annual Review of Cell and Developmental Biology 18:495513.Google Scholar
Raff, R. A. 1996. The shape of life. University of Chicago, Chicago.Google Scholar
Richardson, M. K. 1999. Vertebrate evolution: the developmental origins of adult variation. Bioessays 21:604613.Google Scholar
Richardson, M. K., and Oelschläger, H. H. A. 2002. Time, pattern, and heterochrony: a study of hyperphalangy in the dolphin embryo flipper. Evolution and Development 4:435444.Google Scholar
Ryan, T. J., and Semlitsch, R. D. 1998. Intraspecific heterochrony and life history evolution: decoupling somatic and sexual development in a facultatively paedomorphic salamander. Proceedings of the National Academy of Sciences USA 95:56435648.Google Scholar
Schlosser, G. 2001. Using heterochrony plots to detect the dissociated coevolution of characters. Journal of Experimental Zoology 291:282304.Google Scholar
Schlosser, G. 2003. Mosaic evolution of neural development in anurans: acceleration of spinal cord development in the direct developing frog Eleutherodactylus coqui. Anatomy and Embryology 206:215227.Google Scholar
Skaer, N., Pistillo, D., and Simpson, P. 2002. Transcriptional heterochrony of scute and changes in bristle pattern between two closely related species of blowfly. Developmental Biology 252:3145.Google Scholar
Smith, K. K. 2002. Sequence heterochrony and the evolution of development. Journal of Morphology 252:8297.Google Scholar
Sneath, P. H. A., and Sokal, R. R. 1973. Numerical taxonomy. W. H. Freeman, San Francisco.Google Scholar
Snir, S., and Sachs, T. 2002. The evolution of epidermal development: examples from the Fabaceae. Israel Journal of Plant Sciences 50(Suppl.):S129S139.Google Scholar
Sordino, P., van der Hoeven, F., and Duboule, D. 1995. Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 375:678681.Google Scholar
Takeshi, K., and Yoshino, T. 2002. Diversity and evolution of life histories of gobioid fishes from the viewpoint of heterochrony. Marine and Freshwater Research 53:377402.Google Scholar
Van Valen, L. 1974. Multivariate structural statistics in natural history. Journal of Theoretical Biology 45:235247.Google Scholar
Wagner, G. P., and Gauthier, J. A. 1999. 1,2,3 = 2,3,4: a solution to the problem of the homology of the digits in the avian hand. Proceedings of the National Academy of Sciences USA 96:51115116.Google Scholar
Webster, M., Sheets, H. D., and Hughes, N. C. 2001. Allometric patterning in trilobite ontogeny: testing for heterochrony in Nephrolenellus. Pp. 105144in Zelditch, 2001.Google Scholar
Wray, G. A. 1995. Causes and consequences of heterochrony in early echinoderm development. Pp. 197223in McNamara, K. J., ed. Evolutionary change and heterochrony. Wiley, Chichester, U.K.Google Scholar
Wray, G. A., and Raff, R. A. 1991. The evolution of developmental strategy in marine invertebrates. Trends in Ecology and Evolution 6:4550.Google Scholar
Zelditch, M. L. 2001. Beyond heterochrony: the evolution of development. Wiley-Liss, New York.Google Scholar
Zelditch, M. L., and Fink, W. L. 1996. Heterochrony and heterotopy: stability and innovation in the evolution of form. Paleobiology 22:241254.Google Scholar
Zelditch, M. L., Sheets, H. D., and Fink, W. L. 2003. The ontogenetic dynamics of shape disparity. Paleobiology 29:139156.Google Scholar
Zopfi, H. J. 1998. Life-history variation among populations of Euphrasia rostkoviana Hayne (Scrophulariaceae) in relation to grassland management. Biological Journal of the Linnean Society 64:179205.Google Scholar