Molecular phylogeny of the phytoparasitic mite family Phytoptidae (Acariformes: Eriophyoidea) identified the female geni

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Molecular phylogeny of the phytoparasitic mite family Phytoptidae (Acariformes: Eriophyoidea) identified the female genitalic anatomy as a major macroevolutionary factor and revealed multiple origins of gall induction Philipp E. Chetverikov, et al. [full author details at the end of the article] Received: 11 July 2020 / Accepted: 7 November 2020 © Springer Nature Switzerland AG 2020

Abstract Phytoptidae s.str. is a lineage of eriophyoid mites associated with angiosperms. Based on representative taxon sampling and four gene markers (COI, HSP70, 18S, and 28S), we inferred the molecular phylogeny of this group and performed comparative analyses of cuticle-lined female internal genitalia. Although basal relationships were unclear, several well supported clades were recovered. These clades were supported by geography, host associations, and female genital anatomy, but contradicted the current morphology-based systematics. The monophyly of each of five conventional supraspecific groupings (Fragariocoptes, Phytoptus, Phytoptinae, Sierraphytoptinae, and Sierraphytoptini) is rejected based on a series of statistical tests. Additionally, four morphological characters (the absence of tibial solenidion φ and opisthosomal seta c1, presence of telosomal pseudotagma, and ‘morphotype’) were found to be homoplasies that cannot be used to confidently delimit supraspecific lineages of phytoptids. However, our molecular topology was highly congruent with female genital characters. Eight molecular clades were unambiguously supported by the shapes and topography of the spermathecal apparatus and genital apodemes. This suggests that the female genital anatomy could be an important factor affecting cladogenesis in Phytoptidae, a conclusion contrasting with the general expectation that host characteristics should be a major macroevolutionary force influencing the evolution of host-specific symbionts. Indeed, despite the high host-specificity, there were no apparent cophylogenetic patterns. Furthermore, we show that gall-inducing ability evolved multiple times in phytoptids. Because gall formation creates nearly instantaneous niche partitioning and the potential loss or reduction of gene flow, we hypothesize that it could be an important evolutionary factor affecting speciation within different host-associated clades of phytoptid mites. Keywords  Spermatheca · Monocots · Eudicots · Rosaceae · Palms · Hazelnut mite · Galls · Confocal microscopy · rDNA

Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1049​ 3-020-00571​-6) contains supplementary material, which is available to authorized users.

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Experimental and Applied Acarology

Introduction Eriophyoidea are an ancient group of phytoparasitic acariform mites putatively derived from ancestral endostigmatan soil mites, having diversified in ancient biocenoses during the early evolution of higher vascular plants in the early Mesozoic or even late Paleozoic (Schmidt et al. 2012; Sidorchuk et al. 2015; Bolton et al. 2017,