Integrative Taxonomy of the Gall Mite Nothopoda todeica n. sp. (Eriophyidae) from the Disjunct Afro-Australasian Fern Todea barbara: Morphology, Phylogeny, and Mitogenomics †

SIMPLE SUMMARY: Plant-feeding gall mites of the superfamily Eriophyoidea are serious pests in agriculture because they are capable of transmitting viruses and causing growth abnormalities in plants. Evolutionary archaic gall mites are associated with ancient conifer hosts, while more derived forms inhabit flowering plants. In this study, we investigate the morphology and phylogeny of a new species of the subfamily Nothopodinae, Nothopoda todeica n. sp., collected in South Africa from a fern, Todea barbara. This fern has an ancient distribution in Africa and Australasia and belongs to the Gondwanan royal fern family Osmundaceae. We show that the new species is not in a basal position in Nothopodinae. It is very similar and closely related to other members of Nothopoda, associated with derived groups of Asian flowering plants. This contradicts the expectation that the ancient host plant (fern) should be associated with a primitive mite. We also obtained a complete sequence of the mitochondrial DNA of N. todeica n. sp. And demonstrated that it has the same, but differently ordered, mitochondrial genes that were previously found in other eriophyoid mites. Our study contributes to the problem of the history of symbiotic relations of eriophyoid mites with plants, and provides new data that are important for better understanding their evolution. ABSTRACT: Eriophyoidea is a group of phytoparasitic mites with poorly resolved phylogeny. Previous studies inferred Eriophyidae s.l. as the largest molecular clade of Eriophyoidea, and Nothopodinae as the basal divergence of Eriophyidae s.l. We investigate the morphology and molecular phylogeny of Nothopoda todeica n. sp. (Nothopodinae, Nothopodini), associated with a disjunct Afro-Australasian fern Todea barbara (Osmundaceae) from South Africa. Our analyses (1) determine new erroneous sequences (KF782375, KF782475, KF782586) wrongly assigned to Nothopodinae instead of Phyllocoptinae, (2) confirm the basal position of Nothopodinae in Eriophyoidea s.l., (3) question the monophyly of the Colopodacini and Nothopodini tribes, and (4) show the nested position of African fern-associated Nothopoda within a clade dominated by Asian nothopodines from angiosperms, which implies (a) a secondary association of nothopodines with ferns and (b) no relation between geography (continents) and the phylogenetic relationships of Nothopodinae species. Finally, we obtained a first complete mitochondrial genome for Nothopodinae and revealed a new gene order in the mitogenome of N. todeica n. sp., notably deviating from those in other investigated eriophyoids. Our results contribute to resolving the phylogeny of Eriophyoidea and provide an example of an integrative study of a new taxon belonging to an economically important group of acariform mites.