Phylogenetic position of a new Trisetacus mite species (Nalepellidae) destroying seeds of North American junipers and new hypotheses on basal divergence of Eriophyoidea

Authors: CHETVERIKOV, PHILIPP - St Petersburg State University; Rector, Brian; Tonkel, Kirk; DIMITRI, LINDSAY - Former ARS Employee; CHEGLAKOV, DENIS - St Petersburg State University; ROMANOVICH, ANNA - St Petersburg State University; AMRINE, JAMES - West Virginia University

Submitted to: Insects
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/11/2022
Publication Date: 2/15/2022
Citation: Chetverikov, P.E., Rector, B.G., Tonkel, K.C., Dimitri, L., Cheglakov, D.S., Romanovich, A.E., Amrine, J. 2022. Phylogenetic position of a new Trisetacus mite species (Nalepellidae) destroying seeds of North American junipers and new hypotheses on basal divergence of Eriophyoidea. Insects. 13(2). Article 201. https://doi.org/10.3390/insects13020201.
DOI: https://doi.org/10.3390/insects13020201

Interpretive Summary: Several species of native junipers have recently increased their geographic ranges and population densities in the Intermountain West, invading economically and culturally important grazing areas and prompting studies of their seed ecology to understand the causes of this encroachment. In the course of these studies, numerous species of arthropods were recorded infesting the seeds of western, Utah, and California junipers, including a new species of mite that is described for the first time in this report. In addition, comparison of DNA sequences of this new species to sequences from other mite species has provided insight into their phylogenetic relationships and evolutionary history. The results of this study may provide tools for slowing or reversing the recent encroachment of juniper species into economically and culturally important rangelands.

Technical 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 the North American junipers Juniperus osteosperma, J. occidentalis and J. californica, in the western USA. It possesses distinct morphological dimorphism of females and has two codon deletions in the mitochondrial gene, Cox1. Such mutations are rare in Eriophyoidea and were previously detected only in two phytoptid taxa, Retracrus spp. and Phytoptus avellanae s.l., collected from palms and hazelnut, respectively. Cox1 sequences of T. indelis n. sp. (GenBank accession nos. OK624364'OK624370) collected from cones of three geographically remote host populations were almost identical (K2P distances = 0.000–0.001) with a single synonymous substitution observed in mites from J. osteosperma. A phylogenetic analysis based on amino acid alignment of translated Cox1 sequences using a large set of closely related and distant out-groups (a) determined that two North American congeners, T. batonrougei and T. neoquadrisetus, that infest seeds of J. scopulorum and J. virginiana, respectively, 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. Although a Cox1 amino-acid phylogenetic tree of Eriophyoidea was poorly resolved, it 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. Further analyses based on mitogenomic and genomic datasets should test these hypotheses and better resolve the phylogeny of Eriophyoidea.