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Two genomic paths to the evolution of complexity in bodyplans

  • James W. Valentine (a1)


Morphologically complex metazoans appear abruptly during the Cambrian explosion. Suggested measures of metazoan complexity include number of cell morphotypes and aspects of the genome such as the amount of DNA, the number of genes, and the information content of the genome or egg. Estimates of gene numbers are now available for metazoan species belonging to five different phyla or subphyla. There is little correlation between gene number and morphological complexity in the invertebrates: relatively complex forms can have fewer genes than relatively simple forms. Presumably, the more complex forms use more gene-expression events during development, implying that, on average, cis-regulatory elements of more complex invertebrates are richer in binding sites than are those of simpler forms. Vertebrates have many more genes than invertebrates and therefore have more total gene-expression events during development, although they may have, on average, fewer expression events per gene than the invertebrates. There are thus two genomic pathways in the evolution of metazoan complexity: one involves increasing the number of genes, the other involves increasing the number of cis-regulatory binding sites. Both modes were associated with the origin of bodyplans that first appear as fossils during the Cambrian explosion.



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Adams, M. D., et al. 2000. The genome sequence of Drosophila melanogaster. Science 287:21852195.
Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., and Watson, J. D. 1989. Molecular Biology of the Cell, 2d ed. Garland, New York.
Amores, A., Force, A., Yan, Y., Joly, L., Amemiya, C., Fritz, A., Ho, R. K., Langeland, J., Price, V., Wang, Y., Westerfield, M., Ekker, M., and Postlethwait, J. H. 1998. Zebrafish Hox clusters and vertebrate genome evolution. Science 282:17111714.
Antequera, F., and Bird, A. 1993. Number of CpG islands and genes in human and mouse. Proceedings of the National Academy of Sciences USA 90:1199511999.
Bird, A. 1995. Gene number, noise reduction and biological complexity. Trends in Genetics 11:94100.
Bird, A., and Tweedie, S. 1995. Transcriptional noise and the evolution of gene number. Philosophical Transactions of the Royal Society of London B 349:249253.
Bonner, J. T. 1965. Size and cycle. Princeton University Press, Princeton, N.J.
Bonner, J. T. 1988. The evolution of complexity. Princeton University Press, Princeton, N.J.
Burighel, P., and Cloney, R. A. 1997. Urochordata: Ascidiacea. Pp. 221347in Harrison, F. W. and Ruppert, E. E., eds. Microscopic anatomy of invertebrates, Vol. 5. Hemichordata, Chaetognatha, and the invertebrate chordates. Wiley-Liss, New York.
C. elegans Sequencing Consortium. 1998. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:20122018.
Chen, J.-Y., Huang, D.-Y., and Li, C.-W. 1999. An Early Cambrian craniate-like chordate. Nature 402:518522.
Chervitz, S. A., Aravind, L., Sherlock, G., Bell, C. A., Koomin, E. V., Dwight, S. S., Harris, M. A., Dolinski, K., Mohr, S., Smith, T., Weng, S., Cherry, J. M., and Bostein, C. 1998. Comparison of the complete protein sets of worm and yeast: orthology and divergence. Science 282:20222028.
Cooke, J., Nowak, M. A., Boerlijst, M., and Maynard-Smith, J. 1997. Evolutionary origins and maintenance of redundant gene-expression during metazoan development. Trends in Genetics 13:360364.
Duboule, D., and Wilkins, A. S. 1998. The evolution of “bricolage.” Trends in Genetics 14:5459.
Fields, C., Adams, M. D., White, O., and Venter, J. C. 1994. How many genes in the human genome? Nature Genetics 7:345346.
Galau, G. A., Klein, W. H., Davis, M. M., Wold, B. J., Britten, R. J., and Davidson, E. H. 1976. Structural gene sets active in embryos and adult tissues of the sea urchin. Cell 7:487505.
Garcia-Fernàndez, J., and Holland, P. W. H. 1994. Archetypal organization of the amphioxus gene cluster. Nature 370:563566.
Gilbert, S. F. 1997. Developmental biology, 5th ed.Sinauer, Sunderland, Mass.
Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W., Dujon, B., Feldmann, H., Galibert, F., Hoheisel, J. D., Jacq, C., Johnston, M., Louis, E. J., Mewes, H. W., Murakami, Y., Philippsen, P., Tettelin, H., and Oliver, S. G. 1996. Life with 6000 genes. Science 274:546567.
Hardisty, M. W., and Potter, I. C., eds. 1971. The biology of lampreys. Academic Press, London.
Heinzeller, T., and Welsch, U. 1994. Crinoidea. Pp. 9148in Harrison, F. W. and Chia, F.-S., eds. Microscopic anatomy of invertebrates, Vol. 14. Echinodermata. Wiley-Liss, New York.
Hinegardner, R., and Engleberg, J. 1983. Biological complexity. Journal of Theoretical Biology 104:720.
Holland, P. W. H., and Garcia-Fernàndez, J. 1996. Hox genes and chordate evolution. Developmental Biology 173:382395.
Jahn, B., and Miklos, G. 1988. The eukaryotic genome in development and evolution. Allen and Unwin, London.
Lundin, L.-G. 1999. Gene duplications in early metazoan evolution. Cell and Developmental Biology 10:523530.
Marshall, C. R., Raff, E. C., and Raff, R. A. 1994. Dollo's law and the death and resurrection of genes. Proceedings of the National Academy of Sciences USA 91:1228312287.
Martin, J. W. 1992. Branchiopoda. Pp. 25224in Harrison, F. W. and Humes, A. G., eds. Microscopic anatomy of invertebrates, Vol. 9. Crustacea. Wiley-Liss, New York.
McShea, D. W. 1991. Complexity and evolution: what everybody knows. Biology and Philosophy 6:303324.
Ohno, S. 1970. Evolution by gene duplication. Springer, New York.
Patton, S. J., Luke, G. N., and Holland, P. W. H. 1998. Complex history of a chromosomal paralogy region: insights from amphioxus aromatic amino acid hydroxylase genes and insulin-related genes. Molecular Biology and Evolution 15:13731380.
Pébusque, M.-J., Coulier, F., Birnbaum, D., and Pontarotti, P. 1998. Ancient large-scale genome duplications: phylogenetic and linkage analyses shed light on chordate genome evolution. Molecular Biology and Evolution 15:11451159.
Raff, R. A., and Kaufman, T. C. 1983. Embryos, genes, and evolution. Macmillan, New York.
Riedl, R. 1977. A systems-analytic approach to macro-evolutionary phenomena. Quarterly Review of Biology 52:351370.
Rubin, G. M., et al. 2000. Comparative genomics of the eukaryotes. Science 287:22042215.
Ruppert, E. E. 1997. Cephalochordata (Acrania). Pp. 349504in Harrison, F. W. and Ruppert, E. E., eds. Microscopic anatomy of Invertebrates, Vol. 15. Hemichordata, Chaetognatha, and the invertebrate chordates. Wiley-Liss, New York.
Saunders, P. T., and Ho, M.-W. 1976. On the increase in complexity in evolution. Journal of Theoretical Biology 90:515530.
Sharman, A. C., and Holland, P. W. H. 1996. Conservation, duplication and divergence of developmental genes during chordate evolution. Netherlands Journal of Zoology 46:4767.
Sharman, A. C., and Holland, P. W. H. 1998. Estimation of Hox cluster number in lampreys. International Journal of Developmental Biology 42:617620.
Shu, D.-G., Luo, H.-L., Morris, S. Conway, Zhang, X.-L., Hu, S.-X., Chen, L., Han, J., Zhu, M., Li, Y., and Chen, L.-Z. 1999. Lower Cambrian vertebrates from south China. Nature 402:4246.
Simmen, M. W., Leitgeb, S., Clark, V. H., Jones, S. J. M., and Bird, A. 1998. Gene number in an invertebrate chordate, Ciona intestinalis. Proceedings of the National Academy of Sciences USA 95:44374440.
Sneath, P. H. A. 1964. Comparative biochemical genetics in bacterial taxonomy. Pp. 565583in Leone, C. A., ed. Taxonomic biochemistry and serology. Ronald, New York.
Valentine, J. W. 1991. Major factors in the rapidity and extent of the metazoan radiation during the Proterozoic-Phanerozoic transition. Pp. 1113in Simonetta, A. M. and Morris, S. Conway, eds. The early evolution of the Metazoa and the significance of problematic taxa. Cambridge University Press, Cambridge.
Valentine, J. W. 1994. Late Precambrian bilaterians: grades and clades. Proceedings of the National Academy of Sciences USA 91:67516757.
Valentine, J. W., Collins, A. G., and Meyer, C. P. 1994. Morphological complexity increase in metazoans. Paleobiology 20:131142.
Valentine, J. W., Jablonski, D., and Erwin, D. H. 1999. Fossils, molecules and embryos: new perspectives on the Cambrian explosion. Development 126:851859.
Wainright, P. O., Hinkle, T., Sogin, M. L., and Stickel, S. K. 1993. Monophyletic origins of the Metazoa: an evolutionary link with fungi. Science 260:340342.
Wicken, J. W. 1979. The generation of complexity in evolution: a thermodynamic and information-theoretical discussion. Journal of Theoretical Biology 77:349365.
Wright, K. A. 1991. Nematoda. Pp. 111195in Harrison, F. W. and Ruppert, E. E., eds. Microscopic anatomy of invertebrates, Vol. 4. Aschelminthes. Wiley-Liss, New York.

Two genomic paths to the evolution of complexity in bodyplans

  • James W. Valentine (a1)


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