Genetic Gene Expression Changes during Environmental Adaptations Tend to Reverse Plastic Changes Even after the Correction for Statistical Nonindependence.

Organismal adaptations to new environments often begin with plastic phenotypic changes followed by genetic phenotypic changes, but the relationship between the two types of changes is controversial. Contrary to the view that plastic changes serve as steppingstones to genetic adaptations, recent transcriptome studies reported that genetic gene expression changes more often reverse than reinforce plastic expression changes in experimental evolution. However, it was pointed out that this trend could be an artifact of the statistical nonindependence between the estimates of plastic and genetic phenotypic changes, because both estimates rely on the phenotypic measure at the plastic stage. Using computer simulation, we show that indeed the nonindependence can cause an apparent excess of expression reversion relative to reinforcement. We propose a parametric bootstrap method and show by simulation that it removes the bias almost entirely. Analyzing transcriptome data from a total of 34 parallel lines in 5 experimental evolution studies of Escherichia coli, yeast, and guppies that are amenable to our method confirms that genetic expression changes tend to reverse plastic changes. Thus, at least for gene expression traits, phenotypic plasticity does not generally facilitate genetic adaptation. Several other comparisons of statistically nonindependent estimates are commonly performed in evolutionary genomics such as that between cis- and trans-effects of mutations on gene expression and that between transcriptional and translational effects on gene expression. It is important to validate previous results from such comparisons, and our proposed statistical analyses can be useful for this purpose.