Phylogenomics of the Aphididae: Deep relationships between subfamilies clouded by gene tree discordance, introgression and the gene tree anomaly zone

Abstract

Aphids (Hemiptera: Aphididae) are a lineage of ~5200 plant-feeding insects most abundant in temperate regions. The diversification of aphids is thought to be a rapid radiation, whereas abiotic and biotic factors heavily influence the morphologies. These factors have clouded the taxonomy at all taxonomic ranks, and the effect can be viewed in many incongruent molecular and morphological phylogenies. In this study, we address this problem using both genome and transcriptome data to estimate the phylogenomic relationships between 12 subfamilies with 48 ingroup taxa. We predicted a novel well-curated dataset of phylogenetically consistent orthologues that included 3162 genes to estimate a concatenated maximum likelihood and multi-species coalescent species trees. Our results suggest that there are three main clades of Aphididae subfamilies, which are congruent with a previous Sanger sequencing-based phylogenetic study. However, the relationship between the three clades of subfamilies is clouded by gene tree discordance, introgression and parent–child branches along the backbone that fall within the gene tree anomaly zone. In addition, our results suggest an introgression event between two agriculturally important species of aphids within the subfamily Aphidinae. Our research provides the first phylogenomic study of the Aphididae subfamilies and a foundation for future molecular and morphological studies into this adaptive radiation of insects.