Skip to main content
Log in

Adaptive Radiation of Four-Legged Mites of the Family Phytoptidae (Acariformes, Eriophyoidea) on Dicotyledons: Host–Parasite Relationships and Ability to Induce Gallogenesis

  • Published:
Entomological Review Aims and scope Submit manuscript

Abstract

Four-legged mites of the family Phytoptidae (Acariformes, Eriophyoidea) are represented on eudicot plants by 31 species of two subfamilies: Phytoptinae (1 genus, 19 species) and Sierraphytoptinae (7 genera, 12 species). Most phytoptid species that are capable of inducing various growth abnormalities in plants (galls, erinea, bud growth, and other injuries) belong to the subfamily Phytoptinae. Analysis of the quantitative traits has shown that no groups of phytoptid species associated with eudicots can be outlined based on the currently available morphometric characters. The correlation between the prodorsal shield ornamentation, the presence of the tibial solenidion, and the geographic distribution of phytoptid mites is analyzed, and groups of phytoptine species with similar prodorsum topography are discussed. Analysis of host associations of phytoptids from eudicots has revealed no cophylogenetic patterns; many hosts of phytoptids are narrow-range endemics and relicts. It is supposed that phytoptids originated in the tropics or in the Southern Hemisphere. The current classification of phytoptids into subfamilies is probably artificial; it does not reflect the phylogeny of this group and needs a revision based on molecular phylogenetic data.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Amrine, J.W., Jr., Stasny, T.A., and Flechtmann, C.H.W., Revised Keys to the World Genera of the Eriophyoidea (Acari: Prostigmata), West Bloomfield, Michigan: Indira, 2003.

  2. Bagnjuk, I.G., Sukhareva, S.I., and Shevchenko, V.G., 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, 1998, vol. 6, no. 1, p. 59.

    Google Scholar 

  3. Basargin, E.A., Ecological-demographic characterization of Potentilla bifurca L. cenopopulations, Ekologiya, 2007, vol. 5, p. 350. https://elibrary.ru/item.asp?id=9553583

  4. Boczek, J., Shevchenko, V.G., and Davis, R., Generic Key to World Fauna of Eriophyoid Mites (Acarida: Eriophyoidea), Warsaw: Agricultural University Press, 1989.

  5. Bolton, S.J., Chetverikov, P.E., and Klompen, H., Morphological support for a clade comprising two vermiform mite lineages: Eriophyoidea (Acariformes) and Nematalycidae (Acariformes), Syst. Appl. Acarol., 2017, vol. 22, no. 8, p. 1096. https://doi.org/10.11158/saa.22.8.2

    Article  Google Scholar 

  6. Byng, J.W., Chase, M.W., Christenhusz, M.J., Fay, M.F., Judd, W.S., Mabberley, D.J., Sennikov, A.N., Soltis, D.E., Soltis, P.S., Stevens, P.F., Briggs, B., Brockington, S., Chautems, A., Clark, J.C., Conran, J., Haston, E., Möller, M., Moore, M., Olmstead, R., Perret, M., Skog, L., Smith, J., Tank, D., Vorontsova, M., and Weber, A., An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV, Bot. J. Linn. Soc., 2016, vol. 181, no. 1, p. 1. https://doi.org/10.1111/boj.12385

    Article  Google Scholar 

  7. Chen, Z. and Li, J., Phylogenetics and biogeography of Alnus (Betulaceae) inferred from sequences of nuclear ribosomal DNA ITS region, Int. J. Plant Sci., 2004, vol. 165, no. 2, p. 325.

  8. Chetverikov, P.E. and Craemer, C., Sierraphytoptines (Eriophyoidea: Phytoptidae) from relict eudicots: reassignment of Sierraphytoptus taiwanensus to a new genus Solenoplatilobus and refinement of generic diagnosis of Austracus, Syst. Appl. Acarol., 2016, vol. 21, no. 6, p. 745. https://doi.org/10.11158/saa.21.6.3

  9. Chetverikov, P.E., Cvrković, T., Makunin, A., Sukhareva, S., Vidović, B., and Petanović, R., Basal divergence of Eriophyoidea (Acariformes, Eupodina) inferred from combined partial COI and 28S gene sequences and CLSM genital anatomy, Exp. Appl. Acarol., 2015, vol. 67, no. 2, p. 219. https://doi.org/10.1007/s10493-015-9945-9

    Article  CAS  PubMed  Google Scholar 

  10. Coates-Palgrave, K., Drummond, R.B., Moll, E.J., and CoatesPalgrave, M., Trees of Southern Africa, Cape Town: Struik, 2002.

  11. Cvrković, T., Chetverikov, P., Vidović, B., and Petanović, R., Cryptic speciation within Phytoptus avellanae s. l. (Eriophyoidea: Phytoptidae) revealed by molecular data and observations on molting Tegonotus-like nymphs, Exp. Appl. Acarol., 2016, vol. 68, p. 83. https://doi.org/10.1007/s10493-015-9981-5

  12. Douda, J., Doudová, J., Drašnarová, A., Kuneš, P., Hadincová, V., Krak, K., Zákravský, P., and Mandák, B., Migration patterns of subgenus Alnus in Europe since the last glacial maximum: a systematic review, PLOS ONE, 2014, vol. 9, no. 2, p. 688. https://doi.org/10.1371/journal.pone.0088709

  13. Ex, S.A., DeRose, R.J., and Long, J.N., Stand development and population dynamics of curlleaf mountain mahogany (Cercocarpus ledifolius Nutt.) woodlands in Utah’s Bear River Mountains, West. J. Appl. For., 2011, vol. 26, no. 4, p. 183. https://doi.org/10.1093/wjaf/26.4.183

  14. Gehrke, B., Bräuchler, C., Romoleroux, K., Lundberg, M., Heubl, G., and Eriksson, T., Molecular phylogenetics of Alchemilla, Aphanes and Lachemilla (Rosaceae) inferred from plastid and nuclear intron and spacer DNA sequences, with comments on generic classification, Mol. Phyl. Evol., 2008, vol. 47, p. 1030. https://doi.org/10.1016/j.ympev.2008.03.004

  15. Grimm, G.W. and Renner, S.S., Harvesting Betulaceae sequences from Genbank to generate a new chronogram for the family, Bot. J. Linn. Soc., 2013, vol. 175, p. 465. https://doi.org/10.1111/boj.12065

    Article  Google Scholar 

  16. Hall, C.C. Jr., The Eriophyoidea of Kansas, Univ. Kans. Sci. Bull., 1967, vol. 47, no. 9, p. 601.

    Google Scholar 

  17. Heenan, P.B. and Smissen, R.D., Revised circumscription of Nothofagus and recognition of the segregate genera Fuscospora, Lophozonia and Trisyngyne (Nothofagaceae), Phytotaxa, 2013, vol. 146, no. 1, p. 1. https://doi.org/10.11646/phytotaxa.146.1.1

  18. Howard, T.M., Studies in the ecology of Nothofagus cunninghamii Oerst. I. Natural regeneration on the Mt. Donna Buang massif, Victoria, Aust. J. Bot., 1973, vol. 21, p. 67. https://doi.org/10.1071/BT9730067

  19. Huang, S.F. and Lin, T.P., Migration of Trochodendron aralioides (Trochodendraceae) in Taiwan and its adjacent areas, Bot. Stud., 2006, vol. 47, p. 83.

  20. Hügin, G., Die Gattung Alchemilla im Schwarzwald und seinen Nachbargebirgen (Vogesen, Nord-Jura, Schwäbische Alb), in Berichte der Botanischen Arbeitsgemeinschaft Südwestdeutschland Karlsruhe. Beiheft 2, Karlsruhe: Botanische Arbeitsgemeinschaft Südwestdeutschland, 2006, p. 2.

  21. Keifer, H.H., Eriophyid studies III, Bull. Calif. Dep. Agric., 1939, vol. 28, p. 144.

    Google Scholar 

  22. Keifer, H.H., Eriophyid studies XIV, Bull. Calif. Dep. Agric., 1944, vol. 33, p. 18.

    Google Scholar 

  23. Klimov, P.B., O’Connor, B.M., Chetverikov, P.E., Bolton, S.J., Pepato, A.R., Mortazavi, A.L., Tolstikov, A.V., Bauchan, G.R., and Ochoa, R., Comprehensive phylogeny of acariform mites (Acariformes) provides insights on the origin of the four-legged mites (Eriophyoidea), a long branch, Mol. Phyl. Evol., 2018, vol. 119, p. 105. https://doi.org/10.1016/j.ympev.2017.10.017

    Article  Google Scholar 

  24. Krasnov, A.N., An essay on the history of the flora in the south of the Eastern Tien Shan, Zap. Russ. Geogr. Ob-va, 1888, vol. 19, p. 1.

    Google Scholar 

  25. Kurtto, A., Uotila, P., and Sennikov, A., Alchemilla in Mediterranean Europe as revealed by Atlas Florae Europaeae, Bocconea, 2009, vol. 23, p. 221.

  26. Levin, D.A., The Origin, Expansion, and Demise of Plant Species, New York–London: Oxford University Press, 2000.

  27. Li, H., Tsuchimoto, S., Harada, K., Yamasaki, M., Sakai, H., Wada, N., Alipour, A., Sasai, T., Tsunekawa, A., Tsujkumoto, H., Ando, T., Tomemori, H., Sato, S., Hirakawa, H., Quintero, V., Zamarripa, A., Santos, P., Hegazy, A., Ali, A., and Fukui, K., Genetic tracing of Jatropha curcas L. from its Mesoamerican origin to the World, Front. Plant Sci., 2017, vol. 8, p. 1539. https://doi.org/10.3389/fpls.2017.01539

  28. Manson, D.C.M., Eriophyinae (Arachnida: Acari: Eriophyoidea). Fauna of New Zealand No. 5, Wellington: Department of Science and Industrial Research, 1984.

  29. Metkalfe, D.J., Biological flora of the British Isles. Hedera helix L., J. Ecol. (Br. Ecol. Soc.), 2005, vol. 93, no. 3, p. 632.

  30. Nalepa, A., Zur Systematik der Gallmilben, Sitzungsber. Kaiser. Akad. Wiss. Math.-Naturwiss. Kl., 1890, vol. 99, no. 2, p. 40.

    Google Scholar 

  31. Nalepa, A., Neue Gallmilben, Fortsetzung 36, Anz. Akad. Wiss. Wien, 1918, vol. 55, p. 351.

    Google Scholar 

  32. Nalepa, A., Die Phytoptocecidien von Tilia und ihre Erzeuger, Verh. Kaiser-König. Zool.-Bot. Ges. Wien, 1920, vol. 70, p. 49.

  33. Nyffeler, R., Bayer, C., Alverson, W.S., Yen, A., Whitlock, B.A., Chase, M.W., and Baum, D.A., Phylogenetic analysis of the Malvadendrina clade (Malvaceae s. l.) based on plastid DNA sequences, Org. Divers. Evol., 2005, vol. 5, p. 109. https://doi.org/10.1016/j.ode.2004.08.001

    Article  Google Scholar 

  34. Paule, J., Sharbel, T.F., and Dobeš, C., Apomictic and sexual lineages of the Potentilla argentea L. group (Rosaceae): cytotype and molecular genetic differentiation, Taxon, 2011, vol. 60, no. 3, p. 721. https://doi.org/10.1002/tax.603008

  35. Petanović, R., Eriophidne grinje u Jugoslaviji, Beograd: Naucna Knjiga, 1988.

  36. Pfeil, B.E., Brubaker, C.L., Craven, L.A., and Crisp, M.D., Phylogeny of Hibiscus and the tribe Hibisceae (Malvaceae) using chloroplast DNA sequences of ndhF and the rp116 intron, Syst. Bot., 2002, vol. 27, no. 2, p. 333. https://doi.org/10.1043/0363-6445-27.2.333

  37. Pigg, K.B., Wehr, W.C., and Ickert-Bond, S.M., Trochodendron and Nordenskioldia (Trochodendraceae) from the middle Eocene of Washington State, USA, Int. J. Plant Sci., 2001, vol. 162, no. 5, p. 1187. https://doi.org/10.1086/321927

  38. Ponomareva, R.E., Chetyrekhnogie kleshchi orekhovo-plodovykh lesov Kirgizii (Eriophyoid Mites in the Nut Forests of Kirghizia), Frunze: Ilim, 1978.

  39. Redzic, S., Morphological variability, ecological, chorologic and phenological characteristics of the populations of the species Potentilla tommasiana F.W. Schultz in Bosnia and Herzegovina, Stud. Bot., 1994, vol. 12, p. 219.

  40. Shevchenko, V.G., Bagnyuk, I.G., and Sukhareva, S.I., A new family of Pentasetacidae (Acariformes, Tetrapodili) and its role in treatment of the origin and evolution of the group, Zool. Zh., 1991, vol. 70, no. 5, p. 47.

    Google Scholar 

  41. Sidorchuk, E.A., Schmidt, A.R., Ragazzi, E., Roghi, G., and Lindquist, E., Plant-feeding mite diversity in Triassic amber (Acari: Tetrapodili), J. Syst. Palaeontol., 2015, vol. 13, no. 2, p. 129. https://doi.org/10.1080/14772019.2013.867373

    Article  Google Scholar 

  42. Soika, G. and Kozak, M., Problems with the taxonomy of Phytoptus tetratrichus Nalepa 1890 (Acari: Eriophyoidea) inhabiting Tilia spp.: Analysis based on morphological variation among individuals, Zootaxa, 2011, vol. 2988, p. 37. https://doi.org/10.11646/zootaxa.2988.1.3

  43. Staudt, G., The species of Fragaria, their taxonomy and geographical distribution, Acta Hortic., 1989, vol. 265, p. 23.

  44. Stevens, P.F., Angiosperm Phylogeny Website. Version 12, 2001 (accessed June 20, 2018). http://www.mobot.org/MOBOT/research/APweb/

  45. Sukhareva, S.I., Family Phytoptidae Murray, 1877 (Acari: Tetrapodili), its consisting, structure and suggested ways of evolution, Acarina, 1994, vol. 2, no. 1, p. 47.

    Google Scholar 

  46. Sukhareva, S.I. and Chetverikov, P.E., Morphological differences between protogyne and deutogyne females of eriophyoid mites (Acari, Eriophyoidea), Vestn. S.-Peterb. Univ., 2013, vol. 3, no. 1, p. 3. https://elibrary.ru/item.asp?id=18894148

    Google Scholar 

  47. Sukhareva, S.I., Pautov, A.A., Dodueva, I.E., and Chetverikov, P.E., Eriophyoid mites (Acariformes, Eriophyoidea) from Rosaceae: taxonomic diversity, host-parasite relationships, and ability to cause galls, Entomol. Obozr., 2017, vol. 96, no. 4, p. 854. https://elibrary.ru/item.asp?id=30738756

    Google Scholar 

  48. Svenning, J.C., Normand, S., and Kageyama, M., Glacial refugia of temperate trees in Europe: insights from species distribution modeling, J. Ecol., 2008, vol. 96, p. 1117. https://doi.org/10.1111/j.1365-2745.2008.01422.x

    Article  Google Scholar 

  49. Tang, Y. and Zhuge, R., Geographical distribution of Tilia Linn., Acta Phytotaxon. Sin., 1996, vol. 34, no. 3, p. 254.

  50. Topel, M., Antonelli, A., Yesson, C., and Eriksen, B., Past climate change and plant evolution in Western North America: A case study in Rosaceae, PLOS ONE, 2012, vol. 7, no. 12: e50358. https://doi.org/10.1371/journal.pone.0050358

  51. Van Hinsbergen, D.J.J., Edwards, D.J.J., and Govers, R., Eds., Collision and Collapse at the Africa–Arabia–Eurasia Subduction Zone. Geological Society Special Publication 311, London: Geological Society, 2009.

  52. Yembaturova, E.Y., van Wyk, B.E., and Tilney, P.M., A review of the genus Curtisia (Curtisiaceae), Bothalia, 2009, vol. 39, no. 1, p. 87. https://doi.org/10.4102/abc.v39i1.232

  53. Zhou, L., Su, Y.C., Thomas, D.C., and Saunders, R.M., “Out‐of‐Africa” dispersal of tropical floras during the Miocene climatic optimum: evidence from Uvaria (Annonaceae), J. Biogeogr., 2012, vol. 39, no. 2, p. 322. https://doi.org/10.1111/j.1365-2699.2011.02598.x

Download references

Funding

This work was carried out within the framework of research assignment AAAA-A19-119020790133-6 of the Russian Academy of Sciences and supported by the Russian Foundation for Basic Research, project 19-04-00127.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. I. Sukhareva.

Ethics declarations

The authors declare that they have no conflict of interest. All the applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All the procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sukhareva, S.I., Chetverikov, P.E. Adaptive Radiation of Four-Legged Mites of the Family Phytoptidae (Acariformes, Eriophyoidea) on Dicotyledons: Host–Parasite Relationships and Ability to Induce Gallogenesis. Entmol. Rev. 100, 863–880 (2020). https://doi.org/10.1134/S0013873820060135

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0013873820060135

Keywords:

Navigation