An integrative analysis of nematode germline plasticity and evolution in different environments: from development to ecology – GermlineEcoEvoDevo

Understanding how developmental systems respond to environmental variation is of central significance in developmental and evolutionary biology. While both genetic and environmental factors contribute to the expression of phenotypic features, the role of the environment during development has been largely ignored. Studying the role of the environment in affecting developmental processes is, however, of particular importance since (a) all organisms develop in complex and highly variable environments, (b) the environment may have dramatic effects on normal and pathological development, and (c) environmental variation is a key selective force in shaping the evolution of developmental systems.

Our project aims to study the interaction between development and the environment using the germline of Caenorhabditis nematodes as a model system: we study how molecular and cellular processes underlying the reproductive system adjust their functioning in response to environmental variation, and how such environmental responses evolve. The overall project objective is to conduct an integrative and quantitative analysis of such germline plasticity and its evolution by characterizing the key processes of germ cell proliferation, gamete differentiation, and maturation, which ultimately define the reproductive output of the organism. The specific objectives of this project are:

(1) to quantify plasticity and genotype-by-environment interactions for molecular and life history phenotypes in multiple experimental environments in different Caenorhabditis species and isolates. We will quantify the coordinated plastic response of the germline system when exposed to ecologically relevant environmental variation. Using developmental genetic tools and quantitative imaging methods, we test how different environments impact germ cell proliferation, the differentiation from mitosis to meiosis and the switch from sperm to oocyte production, and how plasticity in these processes ultimately affects the reproductive output.

(2) to determine the precise mechanisms underlying plastic phenotypic responses to environmental variation. We will analyze how specific environmental signals affect molecular and cellular patterning events in the germline. In particular, we will be focusing on the fine-tuned control of germ stem cell proliferation and germ cell apoptosis in response to ecologically relevant environments.

(3) to map natural genetic variation underlying reproductive plasticity among different C. elegans isolates using QTL and association mapping. This will allow the identification of genetic factors underlying variation in the plastic response of different genotypes. In addition, we will perform classic developmental genetic analyses in different Caenorhabditis species.

(4) to complement our evolutionary and mechanistic analyses of genotype-by-environment interactions in germline and reproductive system (objectives 1-3) by analyzing C. elegans experimental evolution populations that have adapted to experimental regimes with different degrees of environmental variation. Experimental evolution, unlike comparative approaches, allows researchers to use trajectories of phenotype change in the lab to infer the process of adaptation. Specifically, we will aim to dissect the mechanistic changes in germline processes explaining plasticity and genotype-environment interactions in fitness parameters during the adaptation to constant versus variable environments.

--The primary innovation of this project lies in the combined analysis of the different objectives, which will allow us to integrate both proximate and ultimate causes of plasticity and genotype-by-environment interaction. We believe that this project at the interface of developmental genetics and evolutionary ecology will not only add to our understanding of the evolutionary relevance of biological system features but also help to reveal the full functional repertoire of developmental mechanisms.