Evo-devo: variations on ancestral themes

Abstract

Most animals evolved from a common ancestor, Urbilateria, which already had in place the developmental genetic networks for shaping body plans. Comparative genomics has revealed rather unexpectedly that many of the genes present in bilaterian animal ancestors were lost by individual phyla during evolution. Reconstruction of the archetypal developmental genomic tool-kit present in Urbilateria will help to elucidate the contribution of gene loss and developmental constraints to the evolution of animal body plans.

Figure 1. Evolutionary Relationships among Animals

(A) Urbilateria is the archetypal animal that was the last common ancestor shared by protostomes and deuterostomes. The Urbilateria in this image is depicted as a segmented bottom-dwelling (benthic) animal with eyes, central nervous system, a small appendage, and an open slit-like blastopore. Endoderm is shown in red, central nervous system in dark blue, and surface ectoderm in light blue. (B) The new animal phylogeny, showing that cnidarians are basal to bilateria and that protostomes are divided into two branches, the molting Ecdysozoans and the nonmolting Lophotrochozoans.

Figure 2. Hox Complexes of Drosophila and Mammals

The Hox complex has been duplicated twice in mammalian genomes and comprises 39 genes. Note that microRNA genes, which inhibit translation of more anterior Hox mRNAs, have been conserved between Drosophila and humans.

Figure 3. Posterior Repression of Hox-C6 mRNA Translation in the Mouse Embryo

Translation of Hox-C6 mRNA is seen in eight thoracic segments of the day 13 mouse embryo but blocked in the tail region, probably through the action of microRNAs. The inset shows that Hox-C6 mRNA is expressed all the way to the tip of the tail (using a Hox-C6-lacZ gene fusion). Note that the anterior border of expression of the Hox-C6 protein starts in the posterior half of the T1 segment, indicating that the sclerotome has already resegmented (G. Oliver and E.M.D.R., unpublished data; for methods see Oliver et al., 1988).

Figure 4. The Conserved Chordin-BMP Signaling Network

Although the Chordin-BMP signaling network is conserved, there has been a D-V axis inversion from Drosophila to Xenopus. (A) In Xenopus, Chordin is expressed on the dorsal side and BMP4 at the opposite ventral pole (image courtesy of Hojoon X. Lee). (B) In Drosophila, Dpp is dorsal (blue) and Sog is ventral (in brown) in the ectoderm (Image courtesy of Ethan Bier and reproduced from François et al., 1994, Genes Dev. 8, 2602−2616, with permission from Cold Spring Harbor Laboratory Press, copyright 1994). (C) A network of conserved secreted proteins mediates D-V body patterning in Xenopus and Drosophila.

Figure 5. A-P and D-V Integration in the Embryonic Morphogenetic Field

Shown is a model of the embryonic morphogenetic field in which a Cartesian System of A-P (Wnt) and D-V (BMP) gradients are integrated at the level of phosphorylation of the transcription factors Smads 1, 5, and 8. Note that in this self-regulating model the BMP gradient provides the intensity, but the Wnt gradient controls the duration of the Smad 1, 5, 8, signal. Direct protein-protein interactions are shown in black, and transcriptional activity of Smads 1, 5, and 8 are in blue.