Skip to main content Accessibility help
×
Home
Hostname: page-component-7f7b94f6bd-l8tfn Total loading time: 0.237 Render date: 2022-06-29T19:27:55.399Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "useNewApi": true } hasContentIssue true

Article contents

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: ken.mcnamara@museum.wa.gov.au
Michael L. McKinney
Affiliation:
Department of Earth and Planetary Sciences, University of Tennessee, Knoxville, Tennessee 37996. E-mail: mmckinney@utk.edu

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 

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

Alberch, P., and Blanco, M. J. 1996. Evolutionary patterns in ontogenetic transformation: from laws to regularities. International Journal of Developmental Biology 40:845858.Google 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
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.CrossRefGoogle 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 ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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 26:5679.2.0.CO;2>CrossRefGoogle 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.CrossRefGoogle Scholar
Foote, M. 1997. The evolution of morphological diversity. Annual Review of Ecology and Systematics 28:129152.CrossRefGoogle 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).CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
Harvell, C. D. 1994. The evolution of polymorphism in colonial invertebrates and social insects. Quarterly Review of Biology 69:155185.CrossRefGoogle 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 18:126137.2.0.CO;2>CrossRefGoogle Scholar
Jablonski, D. 2000. Micro- and macroevolution: scale and hierarchy in evolutionary biology and paleobiology. Paleobiology 26:1552.CrossRefGoogle Scholar
Jaecks, G. S., and Carlson, S. J. 2001. How phylogenetic inference can shape our view of heterochrony: examples from thecideide brachiopods. Paleobiology 27:205225.2.0.CO;2>CrossRefGoogle 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.CrossRefGoogle Scholar
Kellogg, E. A. 2000. The grasses: a case study in macroevolution. Annual Review of Ecology and Systematics 31:217238.CrossRefGoogle 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.Google 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.CrossRefGoogle 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.CrossRefGoogle 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 ScholarPubMed
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 28:551558.2.0.CO;2>CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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 21:604613.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Schlosser, G. 2001. Using heterochrony plots to detect the dissociated coevolution of characters. Journal of Experimental Zoology 291:282304.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Smith, K. K. 2002. Sequence heterochrony and the evolution of development. Journal of Morphology 252:8297.CrossRefGoogle ScholarPubMed
Sneath, P. H. A., and Sokal, R. R. 1973. Numerical taxonomy. W. H. Freeman, San Francisco.Google ScholarPubMed
Snir, S., and Sachs, T. 2002. The evolution of epidermal development: examples from the Fabaceae. Israel Journal of Plant Sciences 50(Suppl.):S129S139.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Zelditch, M. L., Sheets, H. D., and Fink, W. L. 2003. The ontogenetic dynamics of shape disparity. Paleobiology 29:139156.2.0.CO;2>CrossRefGoogle 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
47
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Heterochrony, disparity, and macroevolution
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

Heterochrony, disparity, and macroevolution
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

Heterochrony, disparity, and macroevolution
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *