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The ghost of the Cretaceous terrestrial revolution in the evolution of fern–sawfly associations


Utilization of ferns by phytophagous insects is widely considered to be less common and less specialized compared to the phytophagous insect community feeding on angiosperms. In this study, this assumption is challenged by exploring the evolution of pteridophagy (fern-feeding) in the larval stages of sawflies (Symphyta). To achieve this, phylogenetic frameworks were assembled based on published phylogenetic studies and newly reconstructed phylogenies based on cytochrome oxidase subunit I (COI) barcoding data that allowed the reconstruction of the ancestral feeding preferences by plotting reported host plants of sawflies. Evidence was found for two exclusively pteridophagous lineages of sawflies that probably originated before the Cretaceous Terrestrial Revolution, whereas the third lineage comprising several exclusively pteridophagous sawfly genera is nested in the derived sawfly clade feeding predominantly on eudicots. Thus, the evolution of pteridophagy in the clade was probably connected with the transformation of terrestrial habitats associated with the rise of angiosperms during the Cretaceous. The observed phylogenetic patterns are consistent with the hypothesis of “larval diet conservatism” resulting in the establishment of genera and lineages that feed exclusively, or at least predominantly, on conifers, eudicots, ferns, and monocots. Only a small percentage of sawfly genera were found to be polyphylophagous. The results suggest a low frequency of switches between host plants belonging to different major plant lineages such as angiosperms, conifers, and ferns. Successful switches between hosts belonging to different major lineages of land plants coincide with the reorganization of the phylogenetic composition of terrestrial vegetation in the late Mesozoic.