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

Authors: Owen, Christopher; Miller, Gary

Submitted to: Systematic Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/19/2022
Publication Date: 3/17/2022
Citation: Owen, C.L., Miller, G.L. 2022. Phylogenomics of the Aphidoidea: deep relationships between subfamilies clouded by gene tree discordance, introgression, and the gene tree anomaly zone. Systematic Entomology. 47(3):1-17. https://doi.org/10.1111/syen.12542.
DOI: https://doi.org/10.1111/syen.12542

Interpretive Summary: Aphids cause more than a billion dollars a year in crop damage by direct feeding on crops or via transmission of any one of the thousands of known plant pathogens they vector. Despite the agricultural importance of aphids, the evolutionary relationships between aphids have not been proposed using genomic data. This paper synthesizes all publicly available genome data for aphids, estimates their evolutionary relationships, and investigates the sharing of genes throughout the history of aphids. We demonstrate that the evolutionary history of aphids consists of three main groups. In addition, we show that some aphid species have shared genes millions of years ago, while some aphids associated with crops have more recently shared genes. These results are important because the genomic data to estimate evolutionary relationships and the evolutionary relationships themselves help aphid researchers define species boundaries to protect our ports of entry and borders from non-native species, while the sharing of genes often makes identifying species more difficult.

Technical Abstract: Aphids (Hemiptera: Aphidoidea) are a lineage of ~5,200 plant-feeding insects most abundant in temperate regions. The diversification of aphids is thought to be a rapid radiation, while 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 orthologs that included 3,162 genes to estimate a concatenated maximum likelihood and multi-species coalescent species trees. Our results suggest that there are three main clades of Aphidoidea subfamilies, which is 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 Aphidoidea subfamilies and a foundation for future molecular and morphological studies into this adaptive radiation of insects.