Major changes in the core developmental pathways of nematodes: Romanomermis culicivorax reveals the derived status of the Caenorhabditis elegans model

TL;DR

This study compares the genome and developmental pathways of Romanomermis culicivorax with Caenorhabditis elegans, revealing significant evolutionary differences in genetic circuitry despite similar morphology, and highlights R. culicivorax as a valuable alternative model organism.

Contribution

The paper provides the first draft genome of R. culicivorax and demonstrates its retention of ancestral developmental genes lost in C. elegans, offering new insights into nematode evolution.

Findings

R. culicivorax retains conserved developmental toolkit genes.

C. elegans has a highly derived developmental gene set.

Major differences exist in genetic programs for early development.

Abstract

Background Despite its status as a model organism, the development of Caenorhabditis elegans is not necessarily archetypical for nematodes. The phylum Nematoda is divided into the Chromadorea (indcludes C. elegans) and the Enoplea. Compared to C. elegans, enoplean nematodes have very different patterns of cell division and determination. Embryogenesis of the enoplean Romanomermis culicivorax has been studied in great detail, but the genetic circuitry underpinning development in this species is unknown. Results We created a draft genome of R. culicivorax and compared its developmental gene content with that of two nematodes, C. elegans and Trichinella spiralis (another enoplean), and a representative arthropod Tribolium castaneum. This genome evidence shows that R. culicivorax retains components of the conserved metazoan developmental toolkit lost in C. elegans. T. spiralis has independently lost even more of the toolkit than has C. elegans. However, the C. elegans toolkit is not simply depauperate, as many genes essential for embryogenesis in C. elegans are unique to this lineage, or have only extremely divergent homologues in R. culicivorax and T. spiralis. These data imply fundamental differences in the genetic programmes for early cell specification, inductive interactions, vulva formation and sex determination. Conclusions Thus nematodes, despite their apparent phylum-wide morphological conservatism, have evolved major differences in the molecular logic of their development. R. culicivorax serves as a tractable, contrasting model to C. elegans for understanding how divergent genomic and thus regulatory backgrounds can generate a conserved phenotype. The availability of the draft genome will promote use of R. culicivorax as a research model.