Systematics and evolutionary dynamics of insect-fern interactions in the specialized fern-spore feeding Cuprininae (Lepidoptera, Stathmopodidae)

• Published in: Molecular phylogenetics and evolution 2024-05, Vol.194, p.108040-108040, Article 108040
• Main Authors: Shen, Zong-Yu, Terada, Takeshi, Landry, Jean-François, Hoare, Robert J.B., Kuo, Li-Yaung, Chou, Ming-Hsun, Hsu, Yu-Feng, Huang, Jen-Pan
• Format: Article
• Language: English
• Subjects: Ancestral state reconstruction; extinction; family; Fern-spore-feeding (FSF); Gelechioidea; Lepidoptera; mitochondria; New Genus; New Species; Phylogeny; species; subfamily; taxonomic keys; taxonomic revisions
• ISSN: 1055-7903; 1095-9513
• DOI: 10.1016/j.ympev.2024.108040

[Display omitted] •The most comprehensive Stathmopodidae phylogeny to date, focusing on fern-spore-feeding Cuprininae.•Systematic revision of Cuprininae enhances understanding of insect-fern interactions, diverging from angiosperm-centric studies.•Despite fern spores being rare niche for Lepidoptera, no significant differences in Speciation/Extinction/State-transition rates between fern-spore feeders and others.•State-transition rate differs between specialists and oligophages; faster transition from oligophages to specialists observed. Fern-spore-feeding (FSF) is rare and found in only four families of Lepidoptera. Stathmopodidae is the most speciose family that contains FSF species, and its subfamily Cuprininae exclusively specializes on FSF. However, three species of Stathmopodinae also specialize on FSF. To better understand the evolutionary history of FSF and, more generally, the significance of specialization on a peculiar host, a phylogenetic and taxonomic revision for this group is necessary. We reconstructed the most comprehensive molecular phylogeny, including one mitochondrial and four nuclear genes, of Stathmopodidae to date, including 137 samples representing 62 species, with a particular focus on the FSF subfamily, Cuprininae, including 33 species (41% of named species) from 6 of the 7 Cuprininae genera. Species from two other subfamilies, Stathmopodinae and Atkinsoniinae, were also included. We found that FSF evolved only once in Stathmopodidae and that the previous hypothesis of multiple origins of FSF was misled by inadequate taxonomy. Moreover, we showed that (1) speciation/extinction rates do not differ significantly between FSF and non-FSF groups and that (2) oligophage is the ancestral character state in Cuprininae. We further revealed that a faster rate of accumulating specialists over time, and thus a higher number of specialists, was achieved by a higher transition rate from oligophagages to specialists compared to the transition rate in the opposite direction. We finish by describing three new genera, Trigonodagen. nov., Petalagen. nov., and Pediformisgen. nov., and revalidating five genera: Cuprina, Calicotis, Thylacosceles, Actinoscelis, Thylacosceloides in Cuprininae, and we provide an updated taxonomic key to genera and a revised global checklist of Cuprininae.