Skip to main content
Log in

Functional evolution in the ancestral lineage of vertebrates or when genomic complexity was wagging its morphological tail

  • Published:
Journal of Structural and Functional Genomics

Abstract

Early vertebrate evolution is characterized by a significant increase of organismal complexity over a relatively short time span. We present quantitative evidence for a high rate of increase in morphological complexity during early vertebrate evolution. Possible molecular evolutionary mechanisms that underlie this increase in complexity fall into a small number of categories, one of which is gene duplication and subsequent structural or regulatory neofunctionalization. We discuss analyses of two gene families whose regulatory and structural evolution shed light on the connection between gene duplication and increases in organismal complexity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ahn, S. and Tanksley, S.D. (1993) Linkage maps of the rice and maize genomes. Proc. Natl. Acad. Sci. USA, 90, 7980-7984.

    Google Scholar 

  • Adachi, J. and Hasegawa, M. (1992) MOLPHY, Programs for Molecular Phylogenetics, I. PROTML, Maximum Likelihood Inference of Protein Phylogeny (Computer Science Monographs, Vol. 27). Institute of Statistical Mathematics, Tokyo, Japan

    Google Scholar 

  • Allendorf, F.W. and Utter, F.M., (1976) Gene duplication in the family Salmonidae. III. Linkage between two duplicated loci coding for aspartate aminotransferase in the cutthroat trout (Salmo clarki). Hereditas, 82, 19-24.

    Google Scholar 

  • Amores, A., Force, A., Yan, Y.-L., Joly, L., Amemiya, C., Fritz, A., Ho, R.K., Langeland, J., Prince, V., Wang, Y.-L. et al. (1998) Zebrafish hox clusters and vertebrate genome evolution. Science, 282, 1711-1714.

    Google Scholar 

  • Asano, M. and Gruss, P. (1992) Pax?5 is expressed at the midbrain-hindbrain boundary during mouse development. Mech. Dev., 39, 29-39.

    Google Scholar 

  • Baker C.V.H. and Bronner-Fraser M. (1997a) The origins of the neural crest. Part I: Embryonic induction. Mech. Dev., 69, 13-29.

    Google Scholar 

  • Baker, C.V.H. and Bronner-Fraser, M. (1997b) The origins of the neural crest. Part II: An evolutionary perspective. Mech. Dev., 69, 3-11.

    Google Scholar 

  • Bouchard, M., Pfeffer, P. and Busslinger, M. (2000) Functional equivalence of the transcription factors Pax2 and Pax5 in mouse development. Development, 127, 3703-3713.

    Google Scholar 

  • Doyle, J.J., Doyle, J.L., Brown, A.H. and Grace, J.P. (1990) Multiple origins of polyploids in the Glycine tabacina complex inferred from chloroplast DNA polymorphism. Proc. Natl. Acad. Sci. USA, 87, 714-717.

    Google Scholar 

  • Gale, M.D. and Devos, K.M. (1997) Comparative genetics in the grasses Proc. Natl. Acad. Sci. USA, 95, 1971-1974.

    Google Scholar 

  • Ganter, B. and Lipsick, J.S. (1999) Myb and oncogenesis. Adv. Cancer Res., 76, 21-60.

    Google Scholar 

  • Gibson, T.J. and Spring, J. (2000) Evidence in favour of ancient octaploidy in the vertebrate genome. Biochem. Soc. Trans., 28, 259-264.

    Google Scholar 

  • Gilbert, S.F. and Raunio, A.M. (1997) Embryology, Sinauer, Sunderland, MA.

    Google Scholar 

  • Heller, N. and Brändli, A.W. (1999) Xenopus Pax?2/5/8 orthologues: novel insights into Pax gene evolution and identification of Pax?8 as the earliest marker for otic and pronephric cell lineages. Dev. Genet., 24, 208-219.

    Google Scholar 

  • Holland P.W.H. (1996) Molecular biology of lancelets: insights into development and evolution. Israel J. Zool., 42, 247-272.

    Google Scholar 

  • Hughes, A.L. (1999) Phylogenies of developmentally important proteins do not support the hypothesis of two rounds of genome duplication early in vertebrate history. J. Mol. Evol., 48, 565-576.

    Google Scholar 

  • Kardong, K.V. (1997) Vertebrates, 2nd ed., McGraw-Hill, New York, NY.

    Google Scholar 

  • Kobel, H.R. and Du Pasquier, L. (1986) Genetics of polyploid Xenopus. Trends Genet., 2, 310-315.

    Google Scholar 

  • Kozmik, Z., Holland, N.D., Kalousova, A., Paces, J., Schubert, M. and Holland, L.Z. (1999) Characterization of an amphioxus paired box gene, AmphiPax2/5/8: developmental expression patterns in optic support cells, nephridium, thyroid-like structures and pharyngeal gill slits, but not in the midbrain-hindbrain boundary region. Development, 126, 1295-1304.

    Google Scholar 

  • Maddison, D.R. and Maddison, W.P. (2001) Mac Clade Version 4.0, Sinauer, Sunderland, MA.

    Google Scholar 

  • Martin, A. (2001) Is tetralogy true? Lack of support for the 'oneto-four rule'. Mol. Biol. Evol., 18, 89-93.

    Google Scholar 

  • Meyer, A. and Schartl, M. (1999) Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr. Opin. Cell Biol., 11, 699-704.

    Google Scholar 

  • Millet, S., Bloch-Gallego, E., Simeone, A. and Alvarado-Mallart, R.M. (1996) The caudal limit of Otx2 gene expression as a marker of the midbrain/hindbrain boundary: a study using in situ hybridisation and chick/quail homotopic grafts. Development, 122, 3785-3797.

    Google Scholar 

  • Murphy, P. and Hill, R.E. (1991) Expression of the mouse labiallike homeobox-containing genes, Hox 2.9 and Hox 1.6, during segmentation of the hindbrain. Development, 111, 61-74.

    Google Scholar 

  • Pfeffer, P.L., Gerster, T., Lun, K., Brand, M. and Busslinger, M. (1998) Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2.1 (noi) function. Development, 125, 3063-3074.

    Google Scholar 

  • Pfeffer, P.L., Payer, B., Reim, G., di Magliano, M.P. and Busslinger, M. (2002) The activation and maintenance of Pax2 expression at the mid-hindbrain boundary is controlled by separate enhancers. Development, 129, 307-318.

    Google Scholar 

  • Pough, F.H., Janis, C.M. and Heiser J.B. (1999) Vertebrate Life, 5th ed., Prentice Hall, Upper Saddle River, NJ.

    Google Scholar 

  • Shimeld, S.M. and Holland, P.W.H. (2000) Vertebrate innovations. Proc. Natl. Acad. Sci. USA, 97, 4449-4452.

    Google Scholar 

  • Sidow, A. (1996) Gen(om)e duplications in the evolution of early vertebrates. Curr. Opin. Genet. Dev., 6, 715-22.

    Google Scholar 

  • Simon, A.L., Stone, E.A. and Sidow, A. (2002) Inference of functional regions in proteins by quantification of evolutionary constraints. Proc. Natl. Acad. Sci. USA, 99, 2912-2917.

    Google Scholar 

  • Spring, J. (1997) Vertebrate evolution by interspecific hybridisation— are we polyploid? FEBS Lett., 400, 2-8.

    Google Scholar 

  • Wada, H., Saiga, H., Satoh, N. and Holland, P.W. (1998) Tripartite organization of the ancestral chordate brain and the antiquity of placodes: insights from ascidian Pax?2/5/8, Hox and Otx genes. Development, 125, 1113-1122.

    Google Scholar 

  • Wolfe, K.H. and Shields, D.C. (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature, 387, 708-713.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aburomia, R., Khaner, O. & Sidow, A. Functional evolution in the ancestral lineage of vertebrates or when genomic complexity was wagging its morphological tail. J Struct Func Genom 3, 45–52 (2003). https://doi.org/10.1023/A:1022648729770

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022648729770

Navigation