Phenetic and phylogenetic relationships among Aceria spp. (Acari: Eriophyoidea) inhabiting species within the family Brassicaceae in Serbia

Abstract

We examined morphological and genetic differences among Aceria spp. inhabiting six Brassicaceae species in Serbia. Five of them have been already mentioned in the literature as original or alternate hosts of Aceria spp. (Berteroa incana (L.) DC., Capsella bursa-pastoris (L.) Medik., Cardamine hirsuta L., Lepidium draba L. and Sisymbrium orientale L.), whereas Aurinia petraea (Ard.) Schur was registered here for the first time as a host for Aceria sp. Results of morphometric analyses indicated clear differentiation of Aceria spp. from B. incana, L. draba, A. petraea and S. orientale, whereas the other two entities were less diverse and clustered together. Molecular analyses indicated that the average mean divergence over all sequence pairs was 18.3% (11.8–25.9%) and disclosed that the observed mtCOI distances between the six host-associated Aceria entities are large enough to represent differences between species. The Aceria sp. hosted by B. incana was morphologically and genetically most distinctive, whereas discrepancy between phenetic and phylogenetic relationships was found in the position of Aceria sp. hosted by L. draba when compared with those inhabiting C. hirsuta, S. orientale and C. bursa-pastoris.

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References

  1. Amrine JW, 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. Elsevier Science BV, Amsterdam, pp 383–396

    Google Scholar 

  2. Amrine JW Jr, Stasny TAH (1994) Catalog of the Eriophyoidea (Acarina, Prostigmata) of the world. Indira Publ. House, West Bloomfield, p 531

    Google Scholar 

  3. Chetverikov PE (2011) Phytoptus atherodes n. sp. (Acari: Eriophyoidea: Phytoptidae) and a supplementary description of Phytoptus hirtae Roivainen 1950 from sedges (Cyperaceae). Zootaxa 3045:26–44

    Google Scholar 

  4. Chetverikov PE (2015) Evolutionary placticity of highly specialized organisms: evolution of eriophyoid mites (Acariformes: Eriophyoidea) on plants. Acta Entomol Serb 20(1):151–161

    Google Scholar 

  5. Chetverikov PE, Cvrković T, Makunin A, Sukhareva S, Vidović B, Petanović R (2015) Basal divergence of Eriophyoidea (Acariformes, Eupodina) inferred from combined partia COI and 28S gene sequences and CLSM genital anatomy. Exp Appl Acarol 67:219–245

    CAS  Article  PubMed  Google Scholar 

  6. Cotte HJ (1912) Recherches sur les galles de provence. Paris Bull Soc Philomatique Ser 10 4(3):123–362

    Google Scholar 

  7. Cotte J (1924) Les cecidies des Alpes Maritimes et leurs producteurs. Mem de la Soc Linneenne de Provence Marseille 3:1–56

    Google Scholar 

  8. Couvreur TL, Franzke A, Al-Shehbaz IA, Bakker FT, Koch MA, Mummenhoff K (2010) Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Mol Biol Evol 27(1):55–71

    CAS  Article  PubMed  Google Scholar 

  9. Cvrković T, Chetverikov P, Vidović B, Petanović R (2016) Cryptic speciation within Phytoptus avellanae s.l. (Eriophyoidea: Phytoptidae) revealed by molecular data and observations on molting “Tegonotus-like” nymphs. Exp Appl Acarol 68:83–96

    Article  PubMed  Google Scholar 

  10. Davis R, Flechtmann CHW, Boczek JH, Barké HE (1982) Catalogue of eriophyid mites (Acari: Eriophyoidea). Warsaw Agricultural University Press, Warsaw, p 254

    Google Scholar 

  11. De Lillo E (2004) Fauna Europaea: Eriophyoidea. In: Magowski W (ed) Fauna Europaea: Acariformes. Fauna Europaea version 1.1, http://www.faunaeur.org

  12. 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 3:294–299

    CAS  PubMed  Google Scholar 

  13. Hinz HL, Diaconu A, Talmaciu M, Nastasa V, Grecu M (2008) Testing the efficacy of specialist herbivores to control Lepidium draba in combination with different management practices. In: Proceedings of the XII international symposium on biological control of weeds. CAB International Wallingford. 278–282

  14. Keifer HH (1975) Eriophyoidea Nalepa. Injurious eriophyoid mites. In: Jeppson LR, Keifer HH, Baker EW (eds) Mites injurious to economic plants. University of California Press, Berkeley, California, pp 327–533

    Google Scholar 

  15. Larson L, Kiemnec G, Smergut T (2000) Hoary cress reproduction in a sagebrush ecosystem. J Range Manag 53(5):556–559

    Article  Google Scholar 

  16. Lewandowski M, Skoracka A, Szydło W, Kozak M, Druciarek T, Griffiths DA (2014) Genetic and morphological diversity of Trisetacus species (Eriophyoidea: Phytoptidae) associated with coniferous trees in Poland: phylogeny, barcoding, host and habitat specialization. Exp Appl Acarol 63:497–520

    Article  PubMed  PubMed Central  Google Scholar 

  17. Lindquist EE (1996) External anatomy and notation of structures. In: Lindquist EE, Sabelis MW, Bruin J (eds) World crop pests, vol 6., Eriophyoid mites—their biology, natural enemies and controlElsevier, Amsterdam, pp 3–31

    Google Scholar 

  18. Lipa JJ (1978) Preliminary studies on the species Aceria drabae (Nal.) (Acarina, Eriophyiidae) and its potential for the biological control of the weed Cardaria draba L. (Cruciferae). Prace Naukowe Inst Ochrony Rosl 20(1):139–155

    Google Scholar 

  19. Liro JI (1940) Neue Eriophyiden aus Finland. Ann Zool Soc Zool Bot Fenn Venamo 8(1):1–68

    Google Scholar 

  20. Monfreda R, De Lillo E (2012) Eriophyoid mites (Acari: Eriophyoidea) on Brassicaceae: a new species of Metaculus from Turkey and remarks on other species associated with brassicaceous plants. Zootaxa 3154:47–60

    Google Scholar 

  21. Monfreda R, Nuzzaci G, De Lillo E (2007) Detection, extraction, and collection of Eriophyoid mites. Zootaxa 1662:35–43

    Google Scholar 

  22. Nalepa A (1890a) Über neue Gallmilben. Anz der Kais Akad Wiss Math naturwissenschaftliche Klasse Wien 27(1):2

    Google Scholar 

  23. Nalepa A (1890b) Zur Systematik der Gallmilben. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften. Math Naturwissenschaftliche Klasse Wien 99(2):40–69

    Google Scholar 

  24. Nalepa A (1891) Neue Gallmilben. Nova acta. Kaiserlich Leopoldinisch-Carolinische Deutsche Akademie der Naturforscher 55(6):363–395

    Google Scholar 

  25. Nalepa, A (1898) Acarina. Eriophyidae (Phytoptidae). Das Tierreich. Eine Zusammenstellung und Kennzeichnung de rezenten Tierformen. Walter de Gruyter & Co., Berlin. 4. Lief., pp ix + 74

  26. Nalepa A (1929) Neuer Katalog der bisher Beschriebenen Gallmilben, ihrer Gallen und Wirtspflanzen. Marcellia 25(1–4):67–183

    Google Scholar 

  27. Navajas M, Ochoa R (2013) Integrating ecology and genetics to address Acari. Exp Appl Acarol 59:1–10

    Article  PubMed  Google Scholar 

  28. Navia D, Ferreira CBS, Reis AC, Gondim MG Jr (2015) Traditional and geometric morphometrics supporting the differentiation of two new Retracrus (Phytoptidae) species associated with heliconias. Exp Appl Acarol 67:87–121

    Article  PubMed  Google Scholar 

  29. Oldfield GN (1996) Diversity and host plant specificity. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites—their biology, natural enemies and control. Elsevier, Amsterdam, pp 199–216

    Google Scholar 

  30. Oldfield G (2005) Biology of Gall-inducing Acari. In: Raman A, Schaefer CW, Withers TM (eds) Biology, ecology and evolution of gall-inducing arthropods. Science Publishers Inc, Enfield, pp 35–57

    Google Scholar 

  31. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    CAS  Article  PubMed  Google Scholar 

  32. Roivainen H (1950) Eriophyid news from Sweden. Acta Entomol Fenn 7:1–51

    Google Scholar 

  33. 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 100:263–272

    CAS  Article  PubMed  Google Scholar 

  34. Skoracka A, Kucynski L, Magowski W (2002) Morphological variation in different host populations of Abacarus hystrix (Acari: Prostigmata: Eriophyoidea). Exp Appl Acarol 26:187–193

    Article  PubMed  Google Scholar 

  35. Skoracka A, Smith L, Oldfield G, Cristofaro M, Amrine JW Jr (2010) Host-plant specificity and specialization in eriophyoid mites and their importance for the use of eriophyoid mites as biocontrol agents of weeds. Exp Appl Acarol 51:93–113

    Article  PubMed  Google Scholar 

  36. Skoracka A, Kuczynski L, Santos de Mendonca R, Dabert M, Szydło 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 

  37. Skoracka A, Kuczyński L, Szydło W, Rector B (2013) The wheat curl mite Aceria tosichella (Acari: Eriophyoidea) is a complex of cryptic lineages with divergent host ranges: evidence from molecular and plant bioassay data. Biol J Linn Soc 109(1):165–180

    Article  Google Scholar 

  38. Smith L, De Lillo E, Amrine JW (2010) Effectiveness of eriophyid mites for biological control of weedy plants and challenges for future research. Exp Appl Acarol 51(1–3):115–149

    CAS  Article  PubMed  Google Scholar 

  39. StatSoft, Inc. (2001) STATISTICA (data analysis software), version 6. http//www.statsoft.com

  40. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. The Plant List Database (2016). A working list of all plant species. http://www.theplantlist.org. Accessed 29 Jan 2016

  42. Vidović B, Stanisavljević LJ, Petanović R (2010) Phenotypic variabilility in five Aceria spp. (Acari: Eriophyoidea) inhabiting Cirsium species (Asteraceae) in Serbia. Exp Appl Acarol 52:169–181

    Article  PubMed  Google Scholar 

  43. Vidović B, Cvrković T, Marić I, Chetverikov PE, Cristofaro M, Rector BG, Petanović R (2015) A new Metaculus species (Acari: Eriophyoidea) on Diplotaxis tenuifolia (Brassicaceae) from Serbia: a combined description using morphology and DNA barcode data. Ann Entomol Soc Am 108(5):922–931

    Article  Google Scholar 

  44. Warwick SI, Francis A, Al-Shehbaz IA (2006) Brassicaceae: species checklist and database on CD-Rom. Plant Syst Evol 259(2–4):249–258

    Article  Google Scholar 

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Acknowledgements

This work was partly supported by research Grants from the Ministry of Education, Science and Technological Development of Serbia (Grant Nos. III 43001 and 173003).

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Correspondence to Radmila Petanović.

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Živković, Z., Vidović, B., Jojić, V. et al. Phenetic and phylogenetic relationships among Aceria spp. (Acari: Eriophyoidea) inhabiting species within the family Brassicaceae in Serbia. Exp Appl Acarol 71, 329–343 (2017). https://doi.org/10.1007/s10493-017-0128-8

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Keywords

  • Eriophyidae
  • Aceria spp.
  • Aurinia petraea
  • Eriophyoid mites
  • mtDNA COI
  • Traditional morphometrics