Disentangling the Evolution of a Developmental Switch Network that Regulates Phenotypic Plasticity in a Morphological Novelty: a Nematode Evo-Devo Perspective

Abstract

Phenotypic plasticity describes the ability of a single genotype to produce different phenotypes in response to distinct environmental conditions. It has been proposed to be a diving force of morphological evolution and a trailblazer for the emergence of individualized novelties - new traits which progressively evolved from one or more preexisting ones and acquired a new qualitative dimension. Yet, in order to reconstruct such character transformations and the facilitator role phenotypic plasticity may have played, we need model systems that allow comparative morphological and genetic investigations in organisms that display plastic novelties, as well as in their out-group relatives that do not exhibit these novel traits. Nematodes belonging to the Diplogastridae, such as Pristionchus pacificus, and their paraphyletic out-group "Rhabditidae", such as Caenorhabditis elegans, fulfill these requirements. "Rhabditids" have tube-shaped mouths with immovable cuticular feeding structures, called flaps, that act as valves preventing the regurgitation of food. In contrast, Diplogastridae, which emerged from "rhabditids", evolved moveable cuticular teeth from these flaps. Intriguingly, the flap-to-tooth transformation that accompanied the "rhabditid"-to- diplogastrid transition was tightly linked to phenotypic plasticity, and most Diplogastridae display stable polyphenisms in their tooth-like feeding structures. Previous research identified that a modular switch network underlies the development of these plastic feeding structures in P. pacificus. In my thesis work, I aimed to expand the knowledge of the switch network by identifying molecular players involved in the production of the cuticular teeth, and to reconstruct its evolutionary history by studying the functions of its conserved constituents in the "rhabditid" C. elegans, which has non-plastic flaps. First, to facilitate quantitative morphological studies in nematodes, I established a computational pipeline that combines landmark-based geometric morphometrics with unsupervised clustering methods. Using this pipeline, I demonstrated that DPY-6 is required for proper feeding-structure development in "rhabditids" and diplogastrids, confirming this mucin-type protein as the first known structural component of the nematode mouth. Furthermore, I discovered that feeding- structure development, which is known to be controlled by the two transcription factors NHR-1 and NHR-40 in P. pacificus, is regulated by a different genetic module in C. elegans. I also revealed that NHR-10, unlike its sister paralogs NHR-1 and NHR-40, is not involved in mouth morphogenesis, but required for starvation resistance in P. pacificus. Together, this research suggests that NHR-1 and NHR-40 were co-opted for mouth morphogenesis during the evolution of novel teeth in Diplogastridae. Altogether, my work highlights the complexities of the developmental genetic processes which accompany the evolution of new traits.