Molecular phylogeny of the Acer-feeding aphid subfamily Drepanosiphinae (Insecta: Hemiptera: Aphididae) and the evolution of its endosymbiotic consortia.

The Drepanosiphinae is a Holarctic subfamily of Aphididae comprising six genera: Drepanaphis, Drepanosiphoniella, Drepanosiphum, Megalosiphonaphis, Shenahweum, and Yamatocallis, all of which exhibit strict host plant associations, primarily with Acer species. Despite long-standing taxonomic attention, evolutionary relationships within the group remain poorly resolved, and some important aspects of their biology, such as their patterns of association with symbionts, have been unexplored despite evidence that species in the subfamily might be involved in atypical nutritional symbioses. Here, we present a molecular phylogenetic reconstruction of this subfamily and investigate the evolution of its endosymbiotic consortia. Phylogenetic analyses were conducted using multiple DNA markers, employing both Bayesian inference (BI) and maximum likelihood (ML) approaches. Endosymbionts were characterized using high-throughput sequencing of a fragment of the bacterial 16S rRNA gene. The resulting phylogenies are largely congruent across markers and methods and consistently support the monophyly of Drepanosiphinae. Drepanaphis and Drepanosiphum form a well-supported clade as sister to Drepanosiphoniella, while Yamatocallis and Megalosiphonaphis form a distinct, more distantly related clade. Within Drepanaphis, species group according to host plant use rather than traditional morphological groupings, revealing three host-associated clades: rubrum, saccharum, and grandidentatum. Endosymbiont characterization revealed that, in addition to the obligate symbiont Buchnera aphidicola, most Drepanosiphinae species also host a Sodalis-like bacterium, consistent with previous genomic evidence for a dual nutritional symbiosis with this bacterium. However, Sodalis was absent in most Yamatocallis species, indicating a complex and potentially dynamic evolutionary history of symbiotic relationships within the subfamily. Patterns of association with Wolbachia, Rickettsia, Fukatsuia, Serratia and Arsenophonus suggest a limited role in nutrition. By integrating phylogenetic reconstruction with symbiont profiling, this study provides the most comprehensive evolutionary framework to date for Drepanosiphinae and reinforces the view that nutritional symbioses in aphids are evolutionarily dynamics.