Host-race formation in phytophagous insects is thought to provide the opportunity for local adaptation and subsequent ecological speciation. Studying gene expression differences amongst host races may help to identify phenotypes under (or resulting from) divergent selection and their genetic, molecular and physiological bases. The pea aphid (Acyrthosiphon pisum) comprises host races specializing on numerous plants in the Fabaceae and provides a unique system for examining the early stages of diversification along a gradient of genetic and associated adaptive divergence. In this study, we examine transcriptome-wide gene expression both in response to environment and across pea aphid races selected to cover the range of genetic divergence reported in this species complex. We identify changes in expression in response to host plant, indicating the importance of gene expression in aphid–plant interactions. Races can be distinguished on the basis of gene expression, and higher numbers of differentially expressed genes are apparent between more divergent races; these expression differences between host races may result from genetic drift and reproductive isolation and possibly divergent selection. Expression differences related to plant adaptation include a subset of chemosensory and salivary genes. Genes showing expression changes in response to host plant do not make up a large portion of between-race expression differences, providing confirmation of previous studies’ findings that genes involved in expression differences between diverging populations or species are not necessarily those showing initial plasticity in the face of environmental change.

raw_countScript used to calculate the number of reads mapped to each gene from the Official Gene Set annotation from AphidBase (Legeai et al. 2010), by summing each read that overlaps at least one exon of any particular gene.A. pisum raw countsTranscriptome data from 52 aphid genotypes, reared both on Vicia faba and on their preferred host plant. Illumina sequencing performed using HiSeq2000 using 75 bp paired-end reads (v3 chemistry). Reads mapped to the pea aphid reference genome (IAGC) for each sample separately using TopHat2 (v2.08). The number of reads mapped to each gene from the Official Gene Set annotation from AphidBase (http://aphidbase.com/) was calculated by summing each read that overlaps at least one exon of any particular gene. Read counts reported for 36,401 genes.ApisumRawCounts.csv