Harnessing Caenorhabditis Genomics for Evolutionary Developmental Biology

Abstract

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.

Endomesoderm specification in Caenorhabditis elegans and other nematodes

“…Although identification of an interspecific ortholog does not guarantee that the gene performs the same function, (86) it can provide a starting point for further study. Two close relatives of C. elegans that are used for comparative molecular genetics are the hermaphroditic species C. briggsae and the closely related male-female species C. remanei.…”

Knockdown of SKN-1 and the Wnt effector TCF/POP-1 reveals differences in endomesoderm specification in C. briggsae as compared with C. elegans

“…During speciation, genetic drift and natural selection may lead to changes in cell fate specification mechanisms, even if the phenotype does not change overall (Felix and Barriere, 2005). The related nematodes C. elegans and C. briggsae are emerging as good comparative systems for probing molecular differences in similar developmental pathways (Haag and Pilgrim, 2005). Recent estimates for the divergence time of the two species range from as low as 4–30 MYA to as high as 80–110 MYA (Cutter, 2008; Stein et al, 2003).…”

Comparative Genetics of Sex Determination: Masculinizing Mutations in Caenorhabditis briggsae

“…Like Drosophila, sex determination in nematodes proceeds through assessment of the X:A ratio (Nigon 1951;Madl and Herman 1979). However, unlike Drosophila, the nematode responds to X dosage through a cell-nonautonomous negative regulatory cascade that probably represents a highly modified version of the hedgehog-signaling pathway (Cline and Meyer 1996;Haag and Pilgrim 2005).…”

“…In contrast, comparisons between closely related species are ideal for addressing this. C. elegans is one of the beststudied sex determination models, and its congeners offer such comparisons on both the molecular and the developmental genetic level (reviewed by Haag 2005;Haag and Pilgrim 2005). Further, because these relatives include both ancestrally gonochoristic (male/ female) and derived androdioecious (male/hermaphrodite) mating systems, Caenorhabditis presents an excellent system in which to study the adaptive evolution of an organismally important reproductive trait.…”