Many organisms can acclimate to new environments through phenotypic plasticity, a complex trait that can be heritable, subject to selection, and evolve. However, the rate and genetic basis of plasticity evolution remain largely unknown. We experimentally evolved outbred populations of the nematode Caenorhabditis remanei under an acute heat shock during early larval development. When raised in a nonstressful environment, ancestral populations were highly sensitive to a 36.8° heat shock and exhibited high mortality. However, initial exposure to a nonlethal high temperature environment resulted in significantly reduced mortality during heat shock (hormesis). Lines selected for heat shock resistance rapidly evolved the capacity to withstand heat shock in the native environment without any initial exposure to high temperatures, and early exposure to high temperatures did not lead to further increases in heat resistance. This loss of plasticity would appear to have resulted from the genetic assimilation of the heat induction response in the noninducing environment. However, analyses of transcriptional variation via RNA-sequencing from the selected populations revealed no global changes in gene regulation correlated with the observed changes in heat stress resistance. Instead, assays of the phenotypic response across a broader range of temperatures revealed that the induced plasticity was not fixed across environments, but rather the threshold for the response was shifted to higher temperatures over evolutionary time. These results demonstrate that apparent genetic assimilation can result from shifting thresholds of induction across environments and that analysis of the broader environmental context is critically important for understanding the evolution of phenotypic plasticity.

Parents encountering stress environments can influence the phenotype of their offspring in a form of transgenerational phenotypic plasticity that has the potential to be adaptive if offspring are thereby better able deal with future stressors. Here, we test for the existence of anticipatory parental effects in the heat stress response in the highly polymorphic nematode Caenorhabditis remanei. Rather providing an anticipatory response, parents subject to a prior heat stress actually produce offspring that are less able to survive a severe heat shock. Selection on heat shock resistance within the larvae via experimental evolution leads to a loss of sensitivity (robustness) to environmental variation during both the parental and larval periods. Whole genome transcriptional analysis of both ancestor and selected lines shows that there is weak correspondence between genetic pathways induced via temperature shifts during parental and larval periods. Parental effects can evolve very rapidly via selection acting directly on offspring.

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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.