Canalisation and plasticity on the developmental manifold of Caenorhabditis elegans

Abstract

How do the same mechanisms that faithfully regenerate complex developmental programmes in spite of environmental and genetic perturbations also allow responsiveness to environmental signals, adaptation and genetic evolution? Using the nematode Caenorhabditis elegans as a model, we explore the phenotypic space of growth and development in various genetic and environmental contexts. Our data are growth curves and developmental parameters obtained by automated microscopy. Using these, we show that among the traits that make up the developmental space, correlations within a particular context are predictive of correlations among different contexts. Furthermore, we find that the developmental variability of this animal can be captured on a relatively low‐dimensional phenotypic manifold and that on this manifold, genetic and environmental contributions to plasticity can be deconvolved independently. Our perspective offers a new way of understanding the relationship between robustness and flexibility in complex systems, suggesting that projection and concentration of dimension can naturally align these forces as complementary rather than competing. image The fundamental principles that govern the emergence of robustness and flexibility in complex biological systems are explored by studying the structure of variability in the development of Caenorhabditis elegans in response to genetic and diet perturbations. Correlations in traits within populations of isogenic individuals in a single environment are predictive of correlations between populations that differ in genetic background or environment. Dimensionality reduction can yield representations of development that can separate genetic perturbations from environmental ones, and, among genetic perturbations, natural genetic variations from single gene mutations. These observations can be understood in the context of a projection operator‐based model for the generation and expression of phenotypic variability.