How Weird is The Worm? Evolution of the Developmental Gene Toolkit in Caenorhabditis elegans

Abstract

Comparative developmental biology and comparative genomics are the cornerstones of evolutionary developmental biology. Decades of fruitful research using nematodes have produced detailed accounts of the developmental and genomic variation in the nematode phylum. Evolutionary developmental biologists are now utilising these data as a tool with which to interrogate the evolutionary basis for the similarities and differences observed in Nematoda. Nematodes have often seemed atypical compared to the rest of the animal kingdom-from their totally lineage-dependent mode of embryogenesis to their abandonment of key toolkit genes usually deployed by bilaterians for proper development-worms are notorious rule breakers of the bilaterian handbook. However, exploring the nature of these deviations is providing answers to some of the biggest questions about the evolution of animal development. For example, why is the evolvability of each embryonic stage not the same? Why can evolution sometimes tolerate the loss of genes involved in key developmental events? Lastly, why does natural selection act to radically diverge toolkit genes in number and sequence in certain taxa? In answering these questions, insight is not only being provided about the evolution of nematodes, but of all metazoans.

Keywords: evo-devo; gene duplication; gene toolkit.

Figure 1

Phylogenetic Summary of Nematoda. Panel (A) shows a dendrogram summarising the results of Blaxter et al.'s maximum parsimony analysis as well as the maximum likelihood analysis performed by Smythe et al. on nematode orders [18,19]. Clades I–V are colour-coded: I (burgundy), II (olive), III (orange), IV (light blue), and V (purple). Panel (B) shows a summary dendrogram of the Caenorhabditis genus adapted from Bayesian analysis by Stevens et al. [22]. All species are in the Caenorhabditis genus and rooted with a Pristionchus pacificus outgroup. The Elegans (El.) and Drosophilae (Dr.) supergroups are depicted (black) as well as the Elegans (El.) and Japonica (Ja.) groups (grey) therein.

Figure 2

Metazoan Toolkit Evolution. Panel (A) depicts the phylogenetic relationships between four metazoan species, from the top: Homo sapiens, Drosophila melanogaster, Caenorhabditis elegans, and Nematostella vectensis. Silhouettes of animals were obtained from http://phylopic.org (open source). Their gene toolkits, from the left. Hedgehog (red): Hedgehog (Hh), Patched (Ptc), Smoothened (Smo), Cubitus Interruptus (Ci); Wnt (orange)-sensu stricto: ‘Wingless-related Integration site’ (Wnt), Frizzled, Dishevelled (Dsh), β-cat (β-catenin); Transforming Growth Factor-β (TGF-β) (blue)-sensu lato: Ligand, Type I receptor, Type II receptor, Smad (Small Mothers Against Decapentaplegic); Notch (purple)-sensu stricto: Notch, Delta, Serrate/Jagged (Ser/Jag), Fringe; Homeobox (green): Hox, ParaHox, TALE (Three Amino Acid Loop Extension), PRD (Paired), Other (all other additional homeobox genes mined from the proteomes); are depicted. All copy numbers were obtained by the authors of this review from mining the predicted proteomes of H. sapiens, D. melanogaster, C. elegans and N. vectensis using reciprocal (NCBI) BLASTp searches. Panel (B) depicts the Hox clusters of C. elegans and D. melanogaster. Their genomic location with an approximate scale (Mb = Megabase) and syntenic relationships are schematised, where gene colours denote Hox orthogroups. These colours are also used to depict the gene expression in the adults of these two species.