Hybridisation has shaped a recent radiation of grass-feeding aphids

Aphids have evolved multiple times as grass-specialists and are important pests of cereal crops. Facultative parthenogenetic reproduction of these insects involves several rounds of clonal reproduction interspersed with an occasional sexual cycle. This not only increases the potential of rapid population growth, but it also has facilitated the rapid colonisation of crops globally. Here, we used chromosome-scale genome assemblies to disentangle the evolution of two of the most significant pests of cereals, the English (Sitobion avenae) and Indian (Sitobion miscanthi) grain aphids. We found that genome-wide divergence between S. avenae and S. miscanthi is low and that S. avenae sensu stricto is part of a larger cryptic species complex that includes multiple diverged S. miscanthi lineages. Moreover, comparison of haplotype-resolved assemblies reveals that the S. miscanthi isolate used for genome sequencing is likely a hybrid, with one of its diploid genome copies being closely related to S. avenae and the second being substantially more divergent. Analyses of published genotyping-by-sequencing (GBS) data of grain aphids from the UK and China revealed that S. avenae and S. miscanthi are part of a species complex with many highly differentiated lineages that predate the origins of agriculture. The complex consists of hybrid lineages that display a complex history of hybridisation and genetic introgression. These data demonstrate that hybridisation has substantially contributed to grain aphid diversity, and hence, to the evolutionary potential of this important pest species.