Population and functional transcriptomics of host use evolution in the aphid Uroleucon ambrosiae.

Transitions in host range (from generalist to specialist and vice versa) in herbivorous insects may reflect a process of ecological speciation that helps to explain their immense diversity. Host range evolution also has a considerable economic dimension in the capacity of insects to evolve specialization on crop plants. Yet despite decades of research, the genomic basis of host-range evolution remains unclear, and nearly all studies to date (e.g. comparisons of the generalist Drosophila melanogaster to the specialist D. sechellia) concern species-level comparisons--where reproductive isolation is already complete, obscuring the evolutionary changes that may have initiated reproductive barriers in the first place. To help understand host-range evolution at the genomic level, we utilize a non-model species, the aphid Uroleucon ambrosiae, specialists in the eastern part of their North American range but generalists in the arid southwest. To characterize the functional genomics of host range evolution in this species, and to demonstrate an approach to functional genomics in non-model species, we carried out high-throughput sequencing on two libraries built from genes expressed across the transcriptome. The first library was constructed from field-collected, pooled, population-level samples, and the second from aphids grown in controlled conditions on three alternate host plants. The full set of expressed genes in these two libraries was analyzed for evidence of genetic differentiation (based on F_ST), elevated rates of non-synonymous substitutions (based on D_N/D_S ratios), and differential expression. The results point to candidate loci functionally involved in host-range evolution in a system with ongoing gene-flow and incomplete reproductive isolation.