Radical alterations in the roles of homeobox genes during echinoderm evolution

Echinoderms possess one of the most highly derived body architectures of all metazoan phyla, with radial symmetry, a calcitic endoskeleton, and a water vascular system,. How these dramatic morphological changes evolved has been the subject of extensive speculation and debate, but remains unresolved. Because echinoderms are closely related to chordates and postdate the protostome/deuterostome divergence, they must have evolved from bilaterally symmetrical ancestors. Here we report the expression domains in echinoderms of three important developmental regulatory genes ( distal-less, engrailed and orthodenticle ), all of which encode transcription factors that contain a homeodomain. Our findings show that the reorganization of body architecture involved extensive changes in the deployment and roles of homeobox genes. These changes include modifications in the symmetry of expression domains and the evolution of several new developmental roles, as well as the loss of roles conserved between arthropods and chordates. Some of these modifications seem to have evolved very early in the history of echinoderms, whereas others probably evolved during the subsequent diversification of adult and larval morphology. These results demonstrate the evolutionary lability of regulatory genes that are widely viewed as conservative.

[1]  R. Angerer,et al.  An orthodenticle-related protein from Strongylocentrotus purpuratus. , 1995, Developmental biology.

[2]  L. Hyman,et al.  The Invertebrates Vol Ii , 1951 .

[3]  D. Weisblat,et al.  Segmental expression of an engrailed-class gene during early development and neurogenesis in an annelid. , 1991, Development.

[4]  R. Raff,et al.  Developmental genetics and traditional homology. , 1996, BioEssays : news and reviews in molecular, cellular and developmental biology.

[5]  T. Humphreys,et al.  An engrailed class homeo box gene in sea urchins. , 1988, Gene.

[6]  W. J. Dickinson,et al.  Molecules and morphology: where's the homology? , 1995, Trends in genetics : TIG.

[7]  A. Smith,et al.  Echinoderm phylogeny and evolutionary biology , 1988 .

[8]  N. Patel,et al.  Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. , 1994, Methods in cell biology.

[9]  P. Holland,et al.  Conservation, Duplication, and Divergence of Developmental Genes During Chordate Evolution , 1995 .

[10]  D. Duboule.  Guidebook to the homeobox genes , 1994 .

[11]  N. Brown,et al.  The Early Phylogeny of Chordates and Echinoderms and the Origin of Chordate Left–Right Asymmetry and Bilateral Symmetry , 1996 .

[12]  Y. Sasai,et al.  A common plan for dorsoventral patterning in Bilateria , 1996, Nature.

[13]  K. G. Coleman,et al.  Expression of engrailed proteins in arthropods, annelids, and chordates , 1989, Cell.

[14]  Primary mesenchyme cell migration in the sea urchin embryo: Distribution of directional cues , 1994 .

[15]  N. Patel,et al.  Developmental evolution: insights from studies of insect segmentation. , 1994, Science.

[16]  R. Raff,et al.  Deuterostome phylogeny and the sister group of the chordates: evidence from molecules and morphology. , 1994, Molecular biology and evolution.

[17]  S. Carroll,et al.  The origin and evolution of animal appendages. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[18]  S. Gould.  The Shape of Life , 1996 .

[19]  T. Lacalli.  Mesodermal pattern and pattern repeats in the starfish bipinnaria larva, and related patterns in other deuterostome larvae and chordates , 1996 .

[20]  J. M. W. Slack,et al.  The zootype and the phylotypic stage , 1993, Nature.

[21]  M. Averof,et al.  Diversification of arthropod Hox genes as a paradigm for the evolution of gene functions , 1996 .

[22]  M. F. Strathmann.  Reproduction and development of marine invertebrates of the northern Pacific coast , 1987 .