Intra- and inter-specific variations of gene expression levels in yeast are largely neutral

It is commonly, although not universally, accepted that most intra- and inter-specific genome sequence variations are more or less neutral, whereas a large fraction of organism-level phenotypic variations are adaptive.  Gene expression levels are molecular phenotypes that bridge the gap between genotypes and corresponding organism-level phenotypes.  Yet, it is unknown whether natural variations in gene expression levels are mostly neutral or adaptive.  Here we address this fundamental question by genome-wide profiling and comparison of gene expression levels in nine yeast strains belonging to three closely related Saccharomyces species and originating from five different ecological environments. To answer whether variations in gene expression levels within and between species are largely neutral or adaptive, we compared the transcriptomes of nine yeast strains belonging to three closely related species sampled from five different ecological environments. Importantly, we selected strains such that their genomic phylogenetic relationships mismatch their relationships at the environmental level. For instance, some strains are phylogenetically relatively distant from one another but have similar ecological environments, whereas others are phylogenetically relatively close to one another but live in ecologically distinct environments. If gene expression variations among these strains result from the accumulation of neutral mutations, the relationships of their transcriptomes should mimic the genome-based phylogenetic tree. On the contrary, if the expression variations among these strains are largely shaped by adaptations to their respective environments, their transcriptomes should cluster according to their ecological environments. Thus, our design allows a distinction between the neutral and adaptive hypotheses. Raw short read data available on SRA under accession SRP074509.