Phylogenetic Position of a New Trisetacus Mite Species (Nalepellidae) Destroying Seeds of North American Junipers and New Hypotheses on Basal Divergence of Eriophyoidea

SIMPLE SUMMARY: Eriophyoid mites are microscopic herbivores associated with higher plants. Some of them are serious pests due to their ability to vector viruses and cause other damage to host plants. Mites of the genus Trisetacus are widespread parasites of conifers. They usually live in buds, cones, and rarely within needles of Pinaceae (pine family) and Cupressaceae (cypress family). We discovered a new species, Trisetacus indelis n. sp., severely damaging seeds of three North American junipers in the western USA. This species possesses two morphologically different forms of females and has two deletion mutations in the gene cytochrome oxidase subunit I (Cox1). Such mutations are rare in eriophyoids and were previously detected only in two pestiferous species from palms and hazelnut. Our molecular-phylogenetic analyses determine the closest known relatives of the new species and suggest that Old and New World Trisetacus independently transitioned to living in seeds of junipers. Additionally we show that reconstruction of the phylogeny of Eriophyoidea based on one gene, Cox1, produces a poorly-resolved but biologically consistent tree topology to hypothesize the evolution of Eriophyoidea. Overall, our study improves our understanding of the diversity of conifer-inhabiting mites and indicates further needs in investigating the phylogeny of Eriophyoidea. ABSTRACT: Eriophyoid mites of the genus Trisetacus Keifer are widespread parasites of conifers. A new oligophagous species, T. indelis n. sp., was discovered severely damaging seeds of North American junipers (Juniperus osteosperma, J. occidentalis, and J. californica) in the western USA. It has two codon deletions in the mitochondrial gene Cox1 rarely detected in Eriophyoidea and includes distinct morphological dimorphism of females. A phylogenetic analysis based on amino acid alignment of translated Cox1 sequences using a large set of out-groups (a) determined that two North American congeners, T. batonrougei and T. neoquadrisetus, were the closest known relatives of T. indelis n. sp., and (b) indicated that Old and New World seed-inhabiting Trisetacus from junipers do not form a distinct clade, suggesting a possible independent transition to living in seeds of junipers in America and Eurasia by Trisetacus spp. Our analysis produced a new topology consistent with a scenario assuming gradual reduction of prodorsal shield setation in Eriophyoidea and an ancient switch from gymnosperms to other hosts. Additionally, our analysis did not support monophyly of Trisetacus; recovered a new host-specific, moderately supported clade comprising Trisetacus and Nalepellinae (Nalepella + Setoptus) associated with Pinaceae; and questioned the monophyly of Trisetacus associated with Cupressaceae.