Phylogeny of <i>Rhus</i> gall aphids (Hemiptera: Aphididae) reveals an earlier origin than their primary host plants

Abstract Rhus gall aphids (Hemiptera: Aphididae: Eriosomatinae: Fordini) are obligate parasites that only use Rhus species (Anacardiaceae) as their primary host plants, and each aphid species feeds specifically on one or two sister Rhus species. Both aphids and Rhus hosts exhibit the same disjunct distribution pattern between East Asia and eastern North America. We assembled complete mitochondrial genomes and universal single‐copy nuclear genes for Rhus gall aphids using a genome skimming method and estimated their phylogeny from each dataset. Results strongly supported the monophyly of the Rhus gall aphids Fordini and two genera, Floraphis and Melaphis . However, the relationships among genera were inconsistent between the different datasets. We also estimated the relationships of Rhus host plants from published chloroplast genomes. The chloroplast phylogeny strongly supported Rhus monophyly and relationships among Rhus species. Dating analyses suggest that the most recent common ancestor of Rhus gall aphids was much older than that of their host plants. However, the divergence times and relationships among some Rhus gall aphid species, particularly those with more recent divergence times, were consistent with the ages and relationships of their corresponding primary host plants. This may suggest that Rhus gall aphids established an initial association with stem‐group ancestors of Anacardiaceae and acquired extant Rhus hosts as they evolved or through host switching from another plant group. Divergence time estimates implied that the separation of North America and Eurasia from the Laurasia supercontinent and the subsequent disappearance of the Bering Land Bridge, respectively, have played an important role in the divergence of the eastern North American Melaphis and the East Asian lineage. Our results provide new insights into the coevolution of insects and host plants.