Confocal Microscopy and Molecular Analyses Reveal Anal Secretory Apparatus in Immatures and Recover Transcontinental Clade of Gall Mites (Eriophyoidea) from Tamarisks

Abstract

Tamarisk is an invasive evergreen shrub native to arid regions of Africa and Eurasia and is considered a weed in some countries with dry climates. The complex of gall mites from tamarisks includes fourteen species from four genera of the family Eriophyidae. We reinvestigated the type species of the genus Dicruvasates, D. tamaricis from Egypt, described D. ngubani n. sp. from Tamarix usneoides from South Africa, and revised the generic concept of Dicruvasates. This genus possesses cuticular plates marking longitudinal opisthosomal ridges typical of various phyllocoptine genera, e.g., Echinacrus. We sequenced three genes of Dicruvasates and Phyllocoptes mites from Tamarix and Echinacrus from Frangula, combined our sequences with the data from GenBank, and performed single-gene phylogenetic analyses. All analyses inferred the following: (1) a transcontinental clade Tam comprising Dicruvasates + Aceria + Phyllocoptes from Tamarix; (2) Echinacrus distantly related to Dicruvasates, suggesting the homoplastic nature of the cuticular plates on the opisthosomal ridges, and (3) polyphyly of the genera Aceria and Phyllocoptes. We also investigated partially cleared specimens of Dicruvasates under CLSM and, for the first time, visualized a well-developed anal secretory apparatus (ASA) in the immatures of gall mites, which was previously shown to be a specialized system evolved in Eriophyoidea for silk production. We hypothesize that the ASA contributes to finding nymphs by conspecific males and advocate for the importance of the future molecular biology studies of gall mite silk for developing new methods for controlling mites based on the knowledge of their ecology, behavior, and silk gene genetics.