Discordance between mitochondrial, nuclear, and symbiont genomes in aphid phylogenetics: who is telling the truth?

Abstract

Aphids (Aphididae) are intensively studied due to their significance as pests and their captivating biological traits. Despite this interest, the evolutionary history of this insect family is poorly understood. Recent phylogenomic analyses have produced conflicting topologies, complicating our understanding of aphid trait evolution. In this work, we aimed to unravel the backbone phylogeny of aphids. We sequenced partial and whole mitochondrial genomes from 87 species. We additionally sequenced 42 nuclear loci across 95 aphid species and sourced 146 genes from 12 new and 61 published genomes from aphid obligate endosymbiont, Buchnera aphidicola. We obtained data from these three sources for a subset of aphid species, facilitating a comparative analysis of their signal. Our analyses confirm the monophyly of most subfamilies, validating current taxonomic classifications. However, relationships between subfamilies remain contentious in both mitochondrial and nuclear phylogenies. The topologies obtained with Buchnera are fully resolved but disagree with host phylogenies at deep evolutionary scales and conflict with views on the evolution of aphid morphology. We discuss alternative hypotheses for these discrepancies. Finally, the paucity of phylogenetic information at deep timescales may stem from an initial rapid radiation. Though challenging to establish, this scenario may inherently hinder resolution in aphid phylogenetics.