Functional genomics of acclimation and adaptation in response to thermal stress in Daphnia

Abstract

Background: Gene expression regulation is one of the fundamental mechanisms of phenotypic plasticity and is expected to respond to selection in conditions favoring phenotypic response. The observation that many organisms increase their stress tolerance after acclimation to moderate levels of stress is an example of plasticity which has been long hypothesized to be based on adaptive changes in gene expression. We report genome-wide patterns of gene expression in two heat-tolerant and two heat-sensitive parthenogenetic clones of the zooplankton crustacean Daphnia pulex exposed for three generations to either optimal (18°C) or substressful (28°C) temperature.

Results: A large number of genes responded to temperature and many demonstrated a significant genotype-by-environment (GxE) interaction. Among genes with a significant GxE there were approximately equally frequent instances of canalization, i.e. stronger plasticity in heat-sensitive than in heat-tolerant clones, and of enhancement of plasticity along the evolutionary vector toward heat tolerance. The strongest response observed is the across-the-board down-regulation of a variety of genes occurring in heat-tolerant, but not in heat-sensitive clones. This response is particularly obvious among genes involved in core metabolic pathways and those responsible for transcription, translation and DNA repair.

Conclusions: The observed down-regulation of metabolism, consistent with previous findings in yeast and Drosophila, may reflect a general compensatory stress response. The associated down-regulation of DNA repair pathways potentially creates a trade-off between short-term benefits of survival at high temperature and long-term costs of accelerated mutation accumulation.

Figure 1

iPATH representation of differentially expressed genes in either Southern (A,B) or Northern (C,D) genotypes. A, C: metabolic pathways. B, D: regulatory pathways. Compare to Figure 2 for annotations of major pathways.

Figure 2

Annotated iPATH representation of differentially expressed genes (significant temperature effect in all data). A: metabolic pathways; B: regulatory pathways. Red: down-regulation at 28°C relative to 18°C, Green: up-regulation.

Figure 3

Genes with significant T*geo interaction (tested against the pooled random MS; FDR q < 0.05), for which the Southern (heat-tolerant) genotypes show greater absolute difference in expression at two temperatures (green symbols, Baldwin effect) or smaller absolute difference in expression at the two temperatures (red symbols, canalization) than the Northern (heat sensitive) genotypes.

Figure 4

Principal components analysis of differential expression of 29,212 genes represented on the array in 4 clones of Daphnia from Northern (open symbols) and Southern (solid symbols) acclimated to either 18°C (blue symbols) or 28°C (red symbols). A: RNA samples in the 3D space of the first three principal components, together explaining 42.2% of variance. B – D: the same on pairwise 2D planes of the first three principal components. Arrows connect the Euclidean centroids of 3 replicates for each clone at each temperature (thin blue-red gradient arrows) or the centroids of all replicates at each of the two temperatures (thick blue-red gradient arrows) or at each of the two geographic origins (N vs. S, white-black gradient arrows).