Environmental and evolutionary drivers of the modular gene regulatory network underlying phenotypic plasticity for stress resistance in the nematode Caenorhabditis remanei

Abstract

In response to changing environmental conditions, organisms can acclimate through phenotypic plasticity or adapt by evolving mechanisms to cope with novel stressors. Changes in gene expression, whether dynamic or evolved, are an important way in which environmental responses are mediated; however, much is still unknown about how the molecular networks underlying plastic phenotypes evolve. Here, we compare transcriptional responses to acute heat stress among four populations of the nematode Caenorhabditis remanei--one selected to withstand heat stress, one selected under oxidative stress, an unselected control, and the ancestral population. We used a weighted gene coexpression network analysis within these lines to identify transcriptional modules, which are sets of genes that respond similarly to stress via plastic responses, evolutionary responses, or both. The transcriptional response to acute heat stress is dominated by a plastic response that is shared in the ancestor and all evolved populations. However, we also identified several modules that respond to artificial selection by (1) changing the baseline level of expression, (2) altering the magnitude of the plastic response, or (3) a combination of the two. Our findings reveal that while it is possible to perturb the nature of the transcriptional response network with short bouts of intense selection, the overall structure of transcriptional plasticity is dominated by inherent, ancestral regulatory systems.