Evolutionary host shifts across plant orders despite high host specificity in tree stem surface-living Stomaphis aphids inferred from molecular phylogeny

Abstract

We reconstructed Stomaphis phylogeny and analyzed evolutionary host-plant shifts. The molecular phylogeny revealed 23 well-supported lineages, each specialized to use specific host plant family, whilst host plants of Stomaphis aphids ranged across 6 orders, 11 families, 21 genera, and 28 species. This combination of high host specificity with evolutionarily distant host shifts is exceptional in herbivores. To explain this pattern, we propose one hypothesis among several possibilities: Stomaphis aphids are generalists with respect to the defensive chemicals produced by the plant, but specialists with respect to the stem surface structure of the host tree. This hypothesis predicts that tree taxa having stem surface structures preferred by Stomaphis would be used again and again by genetically distinct Stomaphis lineages. Consistent with this prediction, we found that different (occasionally phylogenetically distant) Stomaphis lineages shared the same host plant genera such as Alnus and Betula. This result suggests that, in the course of their evolutionary history, Japanese Stomaphis aphids have repeatedly colonized a limited number of host plant genera.