Evolution and Developmental System Drift in the Endoderm Gene Regulatory Network of Caenorhabditis and Other Nematodes

Abstract

Developmental gene regulatory networks (GRNs) underpin metazoan embryogenesis and have undergone substantial modification to generate the tremendous variety of animal forms present on Earth today. The nematode Caenorhabditis elegans has been a central model for advancing many important discoveries in fundamental mechanistic biology and, more recently, has provided a strong base from which to explore the evolutionary diversification of GRN architecture and developmental processes in other species. In this short review, we will focus on evolutionary diversification of the GRN for the most ancient of the embryonic germ layers, the endoderm. Early embryogenesis diverges considerably across the phylum Nematoda. Notably, while some species deploy regulative development, more derived species, such as C. elegans, exhibit largely mosaic modes of embryogenesis. Despite the relatively similar morphology of the nematode gut across species, widespread variation has been observed in the signaling inputs that initiate the endoderm GRN, an exemplar of developmental system drift (DSD). We will explore how genetic variation in the endoderm GRN helps to drive DSD at both inter-and intraspecies levels, thereby resulting in a robust developmental system. Comparative studies using divergent nematodes promise to unveil the genetic mechanisms controlling developmental plasticity and provide a paradigm for the principles governing evolutionary modification of an embryonic GRN.

Natural cryptic variation in epigenetic modulation of an embryonic gene regulatory network

“…Interestingly, low SKN-1 requirement appears to be partially compensated by a higher MOM-2/Wnt requirement. Thus, the early stages in the endoderm GRN has undergone rapid change during relatively short evolutionary periods in C. elegans (21,22). In this study, we focus on variation in a single major input node, SKN-1.…”

Opinion: What do rescue experiments with heterologous proteins tell us and what not?

“…But, to conclude that they do the same in their species of origin, P. pacificus, would be wrong. A number of other examples for developmental systems drift exist in nematodes, for example, in the gene regulatory networks that control endoderm formation or sex determination, and some of them can be observed even between closely related species within single genera (reviewed in Ewe et al 2020;Haag et al 2018;Sommer and Bumbarger 2012). This illustrates that the phenomenon is by no means restricted to the comparison of rather distantly related parasitic and free-living species but occurs also between close relatives with very similar live styles.…”

“…Indeed, many mutations isolated in model organisms affect components of a group of phylogenetically widespread signaling pathways, which are used at multiple places and times during the ontogeny of animals (Pires-DaSilva and Sommer 2003). The proteins that make up the core of signaling pathways and their direct interactions tend to be rather highly conserved among different taxa; while what operates these biological switches (the users) and the processes (devices) they control and the regulatory logic according to which the different pathways interact are much more evolutionarily variable, a phenomenon known as "developmental systems drift" (Ewe et al 2020;Haag et al 2018;Pires-DaSilva and Sommer 2003;Sommer and Bumbarger 2012). One of the best studied examples among nematodes is the induction of the vulva, the egg-laying and copulatory organ, in the model nematodes C. elegans and P. pacificus.…”

Primordial Germ Cell Specification in Vertebrate Embryos: Phylogenetic Distribution and Conserved Molecular Features of Preformation and Induction

“…Thus, in this scenario, preformative mechanisms of PGC determination may have evolved to enhance the effectiveness of the germ line-soma distinction in early developmental stages. In this sense germ cell specification and its malleability through evolution may parallel morphological and gene expression divergence in somatic cells according to the “hourglass” model of morphological diversification, in which early developmental processes and zygotic gene expression show wide divergence but which nevertheless lead to a conserved “phylotypic” body plan ( Duboule, 1994 ; Hazkani-Covo et al, 2005 ; Raff, 2006 ; Cruickshank and Wade, 2008 ; Heyn et al, 2014 ; Cutter et al, 2019 ; Ewe et al, 2020 ). These divergent early morphological include variable patterns of cell specification that need to be coordinated with patterns of aggregation of germ plasm components.…”