Comprehensive Phylogeny of Acariform Mites (Acariformes) Provides MARK Insights on the Origin of the Four-Legged Mites (Eriophyoidea), a Long Branch ⁎ Pavel B
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Molecular Phylogenetics and Evolution 119 (2018) 105–117 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Comprehensive phylogeny of acariform mites (Acariformes) provides MARK insights on the origin of the four-legged mites (Eriophyoidea), a long branch ⁎ Pavel B. Klimova,b, , Barry M. OConnora, Philipp E. Chetverikovc, Samuel J. Boltond, Amir R. Pepatoe, Abdolazim L. Mortazavia, Andrey V. Tolstikovb, Gary R. Bauchanf, Ronald Ochoag a Department of Ecology and Evolutionary Biology, University of Michigan, 1109 Geddes Ave, Ann Arbor, MI 48109-1079, USA b Tyumen State University, Faculty of Biology, 10 Semakova Str., Tyumen 625003, Russia c Saint-Petersburg State University, Universitetskaya nab., 7/9, 199034 St. Petersburg, Russia d University of Arkansas, Fayetteville, AR 72701, USA e Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Brazil f USDA, ARS, Electron and Confocal Microscopy Unit, Beltsville, MD 20705, USA g USDA, ARS, Systematic Entomology Laboratory, Beltsville, MD 20705, USA ARTICLE INFO ABSTRACT Keywords: Eriophyoid, or four-legged mites, represent a large and ancient radiation of exclusively phytophagous organisms Acariformes known from the Triassic (230 Mya). Hypothesizing phylogenetic relatedness of Eriophyoidea among mites is a Gall mites major challenge due to the absence of unambiguous morphological synapomorphies, resulting in ten published Phylogenetic position hypotheses placing eriophyoids in various places in the acariform tree of life. Here we test the evolutionary Long branch relationships of eriophyoids using six genes and a representative taxonomic sampling of acariform mites. The Massive basal extinction total evidence analysis places eriophyoids as the sister group of the deep soil-dwelling, vermiform family Nematalycidae (Endeostigmata). This arrangement was supported by the rDNA and CO1 partitions. In contrast, the nuclear protein partition (genes EF1-α, SRP54, HSP70) suggests that Eriophyoidea is sister to a lineage including Tydeidae, Ereynetidae, and Eupodidae (Eupodina: Trombidiformes). On both of these alternative topologies, eriophyoids appear as a long branch, probably involving the loss of basal diversity in early evolution. We analyze this result by using phylogenetically explicit hypothesis testing, investigating the phylogenetic signal from individual genes and rDNA stem and loop regions, and removing long branches and rogue taxa. Regardless of the two alternative placements, (i) the cheliceral morphology of eriophyoids, one of the traits deemed phy- logenetically important, was likely derived directly from the plesiomorphic acariform chelicerae rather than from the modified chelicerae of some trombidiform lineages with a reduced fixed digit; and (ii) two potential synapomorphies of Eriophyoidea+Raphignathina (Trombidiformes) related to the reduction of genital papillae and to the terminal position of PS segment can be dismissed as result of convergent evolution. Our analyses substantially narrow the remaining available hypotheses on eriophyoid relationships and provide insights on the early evolution of acariform mites. 1. Introduction cells and sucking up their liquid contents (Lindquist and Amrine, 1996). Feeding activities of many species cause formation of characteristic Eriophyoid mites (3 extant families, over 350 described genera and galls and other plant tissue abnormalities (hence, another vernacular 4400 species) are an exclusively phytophagous lineage representing one name, 'gall mites'). Species that do not form galls are free-living on of the largest chelicerate radiations, with fossils known from the plant surfaces and, less often, live inside plant tissues (Chetverikov, Triassic (Schmidt et al., 2012). Morphologically, eriophyoids are dis- 2015; Chetverikov and Petanović, 2016; Keifer, 1975). The host plants tinguishable from other mites by being vermiform, four-legged organ- include mostly angiosperms (flowering plants) and gymnosperms (e.g., isms (hence, the vernacular name, 'four-legged mites'). The chelicerae conifers). Gymnosperms (Gerson, 1996), paleozoic progymnosperms or of eriophyoids are modified into stylets adapted for insertion into plant early seed ferns have been cited as ancestral host plants (Bagnjuk et al., ⁎ Corresponding author at: Department of Ecology and Evolutionary Biology, University of Michigan, 1109 Geddes Ave, Ann Arbor, MI 48109-1079, USA. E-mail address: [email protected] (P.B. Klimov). https://doi.org/10.1016/j.ympev.2017.10.017 Received 16 April 2017; Received in revised form 13 October 2017; Accepted 22 October 2017 Available online 23 October 2017 1055-7903/ © 2017 Elsevier Inc. All rights reserved. P.B. Klimov et al. Molecular Phylogenetics and Evolution 119 (2018) 105–117 Fig. 1. A member of Eriophyoidea, (A) wheat curl mite, Aceria erecti (female) and representatives of two acariform lineages considered to be closest relatives of eriophyoids: the deep soil mite (B) Cunliffea sp. (Endeostigmata: Nematalycidae) and the citrus yellow mite, (C) Brachytydeus formosa (Trombidiformes: Eupodina: Tydeidae). Photo credit: Gary Bauchan (USDA ARS Electron and Confocal Microscope Unit, Beltsville, Maryland), Ronald Ochoa (USDA ARS Systematic Entomology Laboratory, Beltsville, Maryland). 1998; Schmidt et al., 2012). Secondary associations, resulting from proposing an array of disparate acariform sister groups: Alycidae, recent host shifts from one of the main host lineages, involve modern Nematalycidae (Endeostigmata), tydeoid families Tydeidae horsetails and ferns (Gerson, 1996; Petanović et al., 2015). The eco- +Ereynetidae, Penthaleidae, Tarsonemoidea, Raphignathae, nomic importance of eriophyoid mites is linked to their ability to Demodecidae, Tenuipalpidae, Tetranychoidea (Trombidiformes), or transmit pathogenic viruses among hosts plants (Oldfield and Proeseler, Astigmata (Sarcoptiformes) (reviewed in Lindquist, 1996, 1998). Some 1996) and to the formation of galls (e. g., erineum patches, deformation of these hypotheses were based on a single, conspicuous morphological of buds), and other symptoms (e.g., leaf spotting), which are associated character or ecological characteristic. These include: the reduction of with changes in plant physiology (Westphal and Manson, 1996). The the posterior legs (hence Tarsonemoidea and Tenuipalpidae), vermi- most important pests attack grain, bulb, berry and nut crops as well as form shape (hence Demodecidae and Nematalycidae), the absence of a an array of ornamental plants (Lindquist and Amrine, 1996). tracheal system (hence Astigmata), or obligate phytophagy (hence The general morphology of eriophyoids is highly specialized for Tetranychoidea). Other hypotheses involve more in-depth analyses of plant feeding, especially the mouthparts; eriophyoids also developed a multiple character states and their evolutionary polarities (e.g., En- distinctly vermiform body (Fig. 1A), a feature known for a few other deostigmata and the trombidiform families belonging to Eupodina). specialized mite linages, e.g., those mimicking ant larvae (Perperipes, However, all evidence comes from ambiguous synapomorphies, in- Larvamima), living in mammalian hair follicles or dermal glands (De- cluding characters representing evolutionary transformation series, modecidae), interstitial spaces of deep soil (Nematalycidae) or the hy- where the eriophyoid state is the hypothetical ultimate evolutionary porheic zone of rivers (Pseudowandesia, Stygothrombium). At the same step (e.g., evolutionary “trend” toward elongation of chelicerae in time, the eriophyoid morphology is highly simplified, especially with presumably derived Alycidae), characters where the ancestral state regard to the number of legs (two pairs instead of four) and funda- cannot be determined based on comparison with other lineages (e.g., mental setae/solenidia, probably due to the mites’ remarkably small the absence of a tracheal system), using characters with too broad or size (100–500, although usually 150–250 µm). As a result, eriophyoids perhaps imprecise definitions (suppression of eugenital setae in females display a combination of numerous autapomorphies and plesiomor- but not in males), or ones that may be highly correlated with the ver- phies, some of which may be due to reductive character losses influ- miform body and hence are likely to be homoplastic due to functional enced by extreme miniaturization. There is no unambiguous morpho- constraints (e.g., the presence of opisthosomal annuli). The currently logical synapomorphy allowing placement of Eriophyoidea in a major accepted classification, which suggests that the Eriophyoidea and Ty- acariform lineage, such as Trombidiformes or any monophyletic group deoidea are related superfamilies, places both of these superfamilies of Endeostigmata (Lindquist, 1996, 2017). into Eupodina, a higher-level lineage in Trombidiformes (Lindquist For over a century, phylogenetic placement of Eriophyoidea has et al., 2009; Zhang et al., 2011). been a major challenge and the subject of active debates, with authors Recent molecular studies have presented contradictory evidence on 106 P.B. Klimov et al. Molecular Phylogenetics and Evolution 119 (2018) 105–117 the origin of eriophyoids. Mitochondrial DNA suggested that erio- 28S); three are nuclear protein-coding (EF1-α, SRP54, HSP70); and one phyoids are either a basal divergence from all acariform mites (Xue (CO1) is a mitochondrial, protein-coding