Harnessing Caenorhabditis Genomics for Evolutionary Developmental Biology

The genome sequence of the nematode C. elegans transformed the study of this important research organism in countless ways. In this paper, we outline the equally great impact it has had on evolutionary developmental biology, with an emphasis on sex determination. Sex determination is a compelling area for comparative studies in Caenorhabditis for two reasons. First, striking differences in reproductive mode (gonochorism vs. androdioecy) are seen even between sister species, and these depend at some level on changes in the regulation of sex determination. Second, as an early and continually active area of C. elegans research, many molecular mechanisms are known that suggest hypotheses about how these reproductive modes differ from each other. Testing these hypotheses has required development of genomic resources for several non-elegans species of Caenorhabditis. Much progress has been made on this front, and several other major projects are currently underway. With these tools in hand, both reverse genetic approaches (RNA interference, cross-species transformation, gene knockouts) and forward genetic screens can be employed in multiple species in the genus. While much remains to be learned, some major surprises have already emerged. One is that the molecular evolution of interacting sex-determining proteins is characterized by rapid compensatory evolution. Another is that outwardly similar hermaphroditic species of Caenorhabditis may have gained this important reproductive adaptation in parallel via distinct germline modifications of the ancestral sex determination pathway. These results provide insights into how nematode mating systems evolve, and important context in which to refine our understanding of the C. elegans model whose characterization made it all possible.