Regulatory and sequence evolution in response to selection for improved associative learning ability in Nasonia vitripennis

BACKGROUND: Selection acts on the phenotype, yet only the genotype is inherited. While both the phenotypic and genotypic response to short-term selection can be measured, the link between these is a major unsolved problem in evolutionary biology, in particular for complex behavioural phenotypes.RESULTS: Here we characterize the genomic and the transcriptomic basis of associative learning ability in the parasitic wasp Nasonia vitripennis and use gene network analysis to link the two. We artificially selected for improved associative learning ability in four independent pairs of lines and identified signatures of selection across the genome. Allele frequency diverged consistently between the selected and control lines in 118 single nucleotide polymorphisms (SNPs), clustering in 51 distinct genomic regions containing 128 genes. The majority of SNPs were found in regulatory regions, suggesting a potential role for gene expression evolution. We therefore sequenced the transcriptomes of selected and control lines and identified 36 consistently differentially expressed transcripts with large changes in expression. None of the differentially expressed genes also showed sequence divergence as a result of selection. Instead, gene network analysis showed many of the genes with consistent allele frequency differences and all of the differentially expressed genes to cluster in a single co-expression network. At a functional level, both genomic and transcriptomic analyses implicated members of gene networks known to be involved in neural plasticity and cognitive processes.CONCLUSIONS: Taken together, our results reveal how specific cognitive abilities can readily respond to selection via a complex interplay between regulatory and sequence evolution.