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

Abstract

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.

A global review and network analysis of phytophagous insect interactions with ferns and lycophytes

“…However, since Schneider et al (2004) it became clear that 90% of extant fern lineages are comprised of groups of much more recent phylogenetic origin (e.g., Polypodiales), and may have evolved even later in the shade of angiosperm evolution. In recent contributions, several authors have found examples of fern-insect coevolution occurring in some insect groups with different feeding habits such as spore-feeding microlepidoptera (Oecophoridae, Sawamura et al, 2009), sap-sucking-bugs (Miridae, Konstantinov & Knyshov, 2015), and leaf-chewing saw ies (Symphyta Isaka & Sato, 2014Schneider, 2016). Host plant switching from older fern taxa or angiosperms to more modern fern groups must have occurred before such newer adaptive radiations.…”

“…Finally, other studies indicate cases of adaptive radiation and coevolution of fern-insects after host plant switching. Over 90% of the saw y genera (Hymenoptera, Symphyta) feed only on one of the major clades of vascular plants: conifers, monocots, eudicots, or ferns (Schneider 2016). Two of the three clades of fern-feeding genera (Heptamelidae and Selandriineae) may have switched from angiosperms to ferns, because they have evolved after the evolution of angiosperms, and the subfamily Selandriinae diverged at the same time as their host plants in the monocots and ferns (Isaka and Sato 2014; Isaka and Sato 2015).…”

“…Historically, most ferns have been assumed to be of Paleozoic origins, to possess a low nutritional value, and to be well protected by high ber and tannin content (Mehltreter 2010). However, most of the extant fern species evolved after the angiosperms (Schneider 2016), can have similar nutrient contents in their tissues as do angiosperms (Wright et al 2004; Richardson and Walker 2010), and do not possess the most developed defense strategies (Farias et al 2020). After a revision of the scienti c literature, several authors found about 400 fern-feeding insect species worldwide and concluded that this record of fern-insect interactions suffers from both sampling bias and insu cient data (Balick et al 1978;Cooper-Driver 1978;Hendrix 1980).…”

Systematics and evolution of lycophytes and ferns

“…Fungal associations, including mycorrhizal associations, have been studied for a long time, but, as the authors carefully document, many key aspects are still in need of clarification. This contribution will hopefully inspire similar critical investigations into other associations with pteridophytes, such as that of phytophagous insects utilizing ferns as their core food supply (Schneider, 2016). Much like fern-fungus associations, fern-insect associations have been long-studied but careful exploration of existing evidence, combined with new evidence, will certainly lead to additional insights (Schneider, 2016).…”

Revision and Phylogeny of the Fern-Inhabiting Genus Felisacus Distant (Insecta: Heteroptera: Miridae: Bryocorinae)

“…Felisacus is noteworthy because of its associations with ferns, which is atypical for insects (e.g., Weintraub et al, 1995;Jensen and Holman, 2000;Konstantinov and Knyshov, 2015;Schneider, 2016). Within the Miridae, fernassociated taxa include Felisacus, species of the tribe Bryocorini (Konstantinov and Knyshov, 2015) and a single Macrolophus Fieber, 1858, species which belongs to the tribe Dicyphini (Wheeler et al, 1979).…”