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Basal divergence of Eriophyoidea (Acariformes, Eupodina) inferred from combined partial COI and 28S gene sequences and CLSM genital anatomy

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Abstract

Eriophyoids are an ancient group of highly miniaturized, morphologically simplified and diverse phytoparasitic mites. Their possible numerous host-switch events have been accompanied by considerable homoplastic evolution. Although several morphological cladistic and molecular phylogenetic studies attempted to reconstruct phylogeny of Eriophyoidea, the major lineages of eriophyoids, as well as the evolutionary relationships between them, are still poorly understood. New phylogenetically informative data have been provided by the recent discovery of the early derivative pentasetacine genus Loboquintus, and observations on the eriophyoid reproductive anatomy. Herein, we use COI and D1-2 rRNA data of 73 eriophyoid species (including early derivative pentasetacines) from Europe, the Americas and South Africa to reconstruct part of the phylogeny of the superfamily, and infer on the basal divergence of eriophyoid taxa. In addition, a comparative CLSM study of the female internal genitalia was undertaken in order to find putative apomorphies, which can be used to improve the taxonomy of Eriophyoidea. The following molecular clades, marked by differences in genital anatomy and prodorsal shield setation, were found in our analyses: Loboquintus(Pentasetacus((Eriophyidae + Diptilomiopidae)(Phytoptidae-1, Phytoptidae-2))). The results of this study suggest that the superfamily Eriophyoidea comprises basal paraphyletic pentasetacines (Loboquintus and Pentasetacus), and two large monophyletic groups: Eriophyidae s.l. [containing paraphyletic Eriophyidae sensu Amrine et al. 2003 (=Eriophyidae s.str.) and Diptilomiopidae sensu Amrine et al. 2003] and Phytoptidae s.l. [containing monophyletic Phytoptidae sensu Boczek et al. 1989 (=Phytoptidae s.str.) and Nalepellidae sensu Boczek et al. 1989]. Putative morphological apomorphies (including genital and gnathosomal characters) supporting the clades revealed in molecular analyses are briefly discussed.

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References

  • Amrine JW Jr, Manson DCM (1996) Preparation, mounting and descriptive study of eriophyoid mites. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies and control (World Crop Pests). Elsevier Science, Amsterdam, pp 383–396

    Chapter  Google Scholar 

  • Amrine JW Jr, Stasny TA, Flechtmann CHW (2003) Revised keys to world genera of Eriophyoidea (Acari: Prostigmata). Indira Publishing House, West Bloomfield

    Google Scholar 

  • Bagnjuk IG, Sukhareva SI, Shevchenko VG (1998) Major trends in the evolution of four-legged mites as a specialized group (using families Pentasetacidae Shev., Nalepellidae Roiv. and Phytoptidae Murray (Acari: Tetrapodili) as examples). Acarina 6(1–2):59–76

    Google Scholar 

  • Baker EW, Kono T, Amrine JW Jr, Delfinado-Baker M, Stasny TA (1996) Eriophyoid mites of the United States. Indira Publishing House, West Bloomfield

    Google Scholar 

  • Boczek J, Shevchenko VG, Davis R (1989) Generic key to world fauna of eriophyoid mites (Acarida: Eriophyoidea). Warsaw Agricultural University Press, Warsaw

    Google Scholar 

  • Bouneb M, de Lillo E, Roversi PF, Simoni S (2014) Molecular detection assay of the bud mite Trisetacus juniperinus on Cupressus sempervirens in nurseries of central Italy. Exp Appl Acarol 62(2):161–170

    Article  CAS  PubMed  Google Scholar 

  • Castagnoli M (1973) Contributo alla conoscenza degli acari Eriofidi viventi sul gen. Pinus Italia Redia 54:1–22

    Google Scholar 

  • Chetverikov PE (2012) Confocal laser scanning microscopy technique for the study of internal genitalia and external morphology of eriophyoid mites (Acari: Eriophyoidea). Zootaxa 3453:56–68

    Google Scholar 

  • Chetverikov PE (2014a) Distal oviduct and genital chamber of eriophyoids (Acariformes, Eriophyoidea): refined terminology and remarks on CLSM technique for studying musculature of mites. Exp Appl Acarol 64(4):407–428. doi:10.1007/s10493-014-9840-9

    Article  PubMed  Google Scholar 

  • Chetverikov PE (2014b) Comparative confocal microscopy of internal genitalia of phytoptine mites (Eriophyoidea, Phytoptidae): new generic diagnoses reflecting host-plant associations. Exp Appl Acarol 62(2):129–160. doi:10.1007/s10493-013-9734-2

    Article  PubMed  Google Scholar 

  • Chetverikov PE, Craemer C (2015) Gnathosomal interlocking apparatus and remarks on functional morphology of frontal lobes of eriophyoid mites (Acariformes, Eriophyoidea). Exp Appl Acarol 66(2):187–202. doi:10.1007/s10493-015-9906-3

    Article  PubMed  Google Scholar 

  • Chetverikov PE, Beaulieu F, Cvrković T, Vidović B, Petanović R (2012) Oziella sibirica (Eriophyoidea: Phytoptidae), a new eriophyoid mite species described using confocal microscopy and COI barcoding. Zootaxa 3560:41–60

    Google Scholar 

  • Chetverikov PE, Cvrković T, Vidović B, Petanović RU (2013) Description of a new relict eriophyoid mite, Loboquintus subsquamatus n. gen. & n. sp. (Eriophyoidea, Phytoptidae, Pentasetacini) based on confocal microscopy, SEM, COI barcoding and novel CLSM anatomy of internal genitalia. Exp Appl Acarol 61(1):1–30. doi:10.1007/s10493-013-9685-7

    Article  PubMed  Google Scholar 

  • Chetverikov PE, Beaulieu F, Beliavskaia AY, Rautian MS, Sukhareva SI (2014a) Redescription of an early-derivative mite, Pentasetacus araucariae (Eriophyoidea, Phytoptidae), and new hypotheses on the eriophyoid reproductive anatomy. Exp Appl Acarol 63:123–125. doi:10.1007/s10493-014-9774-2

    Article  PubMed  Google Scholar 

  • Chetverikov PE, Craemer C, Vishnyakov AE, Sukhareva SI (2014b) CLSM anatomy of internal genitalia of Mackiella reclinata n. sp. and systematic remarks on eriophyoid mites from the tribe Mackiellini Keifer, 1946 (Eriophyoidea, Phytoptidae). Zootaxa 3860(3):261–279

    Article  PubMed  Google Scholar 

  • Chetverikov PE, Desnitskiy AG, Navia D (2015) Confocal microscopy refines generic concept of a problematic taxon: rediagnosis of the genus Neoprothrix and remarks on female anatomy of eriophyoids (Acari: Eriophyoidea). Zootaxa 3919(1):179–191

    Article  PubMed  Google Scholar 

  • Craemer C (2010) A systematic appraisal of the Eriophyoidea (Acari: Prostigmata). PhD Dissertation, Faculty of Natural and Agricultural Sciences, University of Pretoria, Pretoria, South Africa, November 2010

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Method 9(8):772

    Article  CAS  Google Scholar 

  • Farkas HK (1965) Some problems of eriophyid mites phylogeny (Acarina, Eriophyoidea). Zeszyty Problemowe Posterow Nauk Rolniczych 65:189–194

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294

    CAS  PubMed  Google Scholar 

  • Gerson U (1996) Secondary associations: Eriophyoid mites on ferns. In: Lindquist EE, Sabelius MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies and control. World Crop Pests 6. Elsevier, Amsterdam, pp 227–230

    Chapter  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755

    Article  CAS  PubMed  Google Scholar 

  • Keifer HH (1939) Eriophyid studies VI. Bull Calif Dept Agr 28:416–426

    Google Scholar 

  • Keifer HH (1940) Eriophyid studies VIII. Bull Calif Dept Agr 29(1):21–46

    Google Scholar 

  • Keifer HH (1966) Eriophyid studies B-20. Bur Ent Calif Dept Agric 1–20

  • Li H-S, Xue X-F, Hong X-Y (2014) Homoplastic evolution and host association of Eriophyoidea (Acari, Prostigmata) conflict with the morphological-based taxonomic system. Mol Phylogenet Evol 78:185–198. doi:10.1016/j.ympev.2014.05.014

    Article  PubMed  Google Scholar 

  • Lindquist EE (1996a) 1.1.1. External anatomy and notation of structures. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies and control. World Crop Pests 6. Elsevier Science, Amsterdam, pp 3–31

    Chapter  Google Scholar 

  • Lindquist EE (1996b) 1.5.2 phylogenetic relationships. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies and control. World Crop Pests 6. Elsevier Science, Amsterdam, pp 301–327

    Chapter  Google Scholar 

  • Lindquist EE, Amrine JW (1996) 1.1.2 Systematics, diagnoses for major taxa, and keys to families and genera with species on plants of economic importance. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies and control. World Crop Pests 6. Elsevier Science, Amsterdam, pp 33–87

    Chapter  Google Scholar 

  • Lindquist EE, Zacharda M (1987) A new genus and species of Rhagidiidae (Acari: Prostigmata) from Chihuahuan Desert litter in New Mexico. Can J Zool 65(9):2149–2158

    Article  Google Scholar 

  • Lindquist EE, Krantz GW, Walter DE (2009) Chapter 8. Classification. In: Krantz GW, Walter DE (eds) A manual of acarology, 3rd edn. Texas Tech University Press, Texas, pp 97–103

  • Loytynoja A, Goldman N (2005) An algorithm for progressive multiple alignment of sequences with insertions. PNAS 102:10557–10562

    Article  PubMed Central  PubMed  Google Scholar 

  • Müller K (2005) SeqState. Appl bioinform 4(1):65–69

    Article  Google Scholar 

  • Nalepa A (1898). Zur Kenntnis der Gattung Trimerus Nal. Zool. Jahrb., Abt. Syst., Geogr., Biol. Tiere, Jena 11(5):405–411

  • Nuzzaci G, Alberti G (1996) Internal anatomy and physiology. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies and control. World Crop Pests 6. Elsevier Science, Amsterdam, pp 101–150

    Chapter  Google Scholar 

  • Roivainen H (1953) Some gall mites (Eriophyidae) from Spain. Arch Inst Aclim 1:9–43

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP, van der Mark P (2005) MrBayes v. 3.1 Manual. http://mrbayes.csit.fsu.edu/wiki/index.php/Manual. Accessed 5 Nov 2014

  • Schliesske J (1985) Zur Verbrietung und Ökologie einer neunen ursprünglichen Gallmilbenart (Acari: Eriophyoidea) an Araucaria araucana (molina) K. Koch Entomologische Mitteilungen zoologische Museum Hamburg 8:97–106

    Google Scholar 

  • Shevchenko VG, Bagnyuk IG, Sukhareva SI (1991) A new family of Pentasetacidae (Acariformes, Tetrapodili) and its role in treatment of the origin and evolution of the group. Zool Zhurnal 70(5):47–53

    Google Scholar 

  • Schmidt AR, Janckeb S, Lindquist EE, Ragazzi E, Roghi G, Nascimbene PC, Schmidt KTW, Grimaldi DA (2012) Arthropods in amber from the Triassic Period. Proc Natl Acad Sci USA 109(37):14796–14801

  • Sidorchuk EA, Schmidt AR, Ragazzi E, Roghi G, Lindquist EE (2014) Plant-feeding mite diversity in triassic amber (Acari: Tetrapodili). J Syst Paleontol. doi:10.1080/14772019.2013.867373

    Google Scholar 

  • Silvestro D, Michalak I (2011) raxmlGUI: a graphical front-end for RAxML. Organ Divers Evol. doi:10.1007/s13127-011-0056-0

    Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49(2):369–381

    Article  CAS  PubMed  Google Scholar 

  • Skoracka A, Dabert M (2010) The cereal rust mite Abacarus hystrix (Acari: Eriophyoidea) is a complex of species: evidence from mitochondrial and nuclear DNA sequences. Bull Entomol Res 100(3):263–272

    Article  CAS  PubMed  Google Scholar 

  • Skoracka A, Kuczynski L, de Mendonca R, Dabert M, Szydlo W, Knihinicki D, Truol G, Navia D (2012) Cryptic species within the wheat curl mite Aceria tosichella (Keifer) (Acari, Eriophyoidea) revealed by mitochondrial, nuclear and morphometric data. Invertebr Syst 26:417–433

    Article  Google Scholar 

  • Skoracka A, Kuczyński L, Rector B, Amrine JW Jr (2014) Wheat curl mite and dry bulb mite: untangling a taxonomic conundrum through a multidisciplinary approach. Biol J Linnean Soc 111:421–436

    Article  Google Scholar 

  • Sonnenberg R, Nolte AW, Tautz D (2007) An evaluation of LSU rDNA D1–D2 sequences for their use in species identification. Front Zool 4(1):6

    Article  PubMed Central  PubMed  Google Scholar 

  • Stekolnikov AA, Carranza S, Gomez-Diaz E (2012) A new genus and species of Apoloniinae (Acari: Trombiculidae) from Oman. Zootaxa 3499:74–80

    Google Scholar 

  • Sukhareva SI (1994) Family Phytoptidae Murray 1877 (Acari: Tetrapodili), its consisting, structure and suggested ways of evolution. Acarina 2(1–2):47–72

    Google Scholar 

  • Takhtajan AL (1959) Die evolution der angiospermen. Jena 344 Seiten

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Walter DE (2009) Chapter 14. suborder endeostigmata. In: Krantz GW, Walter DE (eds) A manual of acarology, 3rd edn. Texas Tech University Press, Texas, pp. 421–429

  • Walter DE, Lindquist EE, Smith IM, Cook DR, Krantz GW (2009) Chapter 13. Order trombidiformes. In: Krantz GW, Walter DE (eds) A manual of acarology, 3rd edn. Texas Tech University Press, Texas, pp. 233–420

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Acknowledgments

We are grateful to Prof. J.W. Amrine (USA, West Virginia University), Drs. C. Craemer (ARC–Plant Protection Research Institute, South Africa), D. Navia (Embrapa Recursos Genéticos e Biotecnologia, Brazil) and G.A. Sánchez-Monge (Universidad de Costa Rica) for their help in collecting samples for DNA analyses in remote regions. All the steps of this study performed in Serbia by RP, TC and BV were supported by Grant # III 43001 of Serbian Ministry of Science and partly by Grant #F-195 of Serbian Academy of Sciences and Arts. Field work, comparative CLSM study and molecular phylogenetic analyses performed by PC in Russia were supported by the Russian Science Foundation (RSCF Grant #14-14-00621).

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Authors and Affiliations

  1. Department of Invertebrate Zoology, Saint-Petersburg State University, Universitetskaya nab., 7/9, 199034, St. Petersburg, Russia

    P. E. Chetverikov & S. Sukhareva

  2. Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, 199034, St. Petersburg, Russia

    P. E. Chetverikov

  3. Institute for Plant Protection and Environment Belgrade, Banatska 33, Zemun, Serbia

    T. Cvrković

  4. Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, Sredniy Pr. V.O. 41-43, 199004, St. Petersburg, Russia

    A. Makunin

  5. Department of Entomology and Agricultural Zoology, Faculty of Agriculture Belgrade, University of Belgrade, Nemanjina 6, 11080, Zemun, Serbia

    B. Vidović & R. Petanović

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  1. P. E. Chetverikov
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Correspondence to P. E. Chetverikov.

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Supplementary figure 1.

ML tree of mitochondrial COI. Statistical supports indicate ML bootstrap for amino acid dataset/ML bootstrap for nucleotide dataset/Bayesian posterior probabilities for nucleotide dataset. (TIFF 29651 kb)

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Chetverikov, P.E., Cvrković, T., Makunin, A. et al. Basal divergence of Eriophyoidea (Acariformes, Eupodina) inferred from combined partial COI and 28S gene sequences and CLSM genital anatomy. Exp Appl Acarol 67, 219–245 (2015). https://doi.org/10.1007/s10493-015-9945-9

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