Identification of Wolbachia Strains in Two Sibling Species of Neoseiulus Predatory Mites and Their Prey

Julia Malysh; Svetlana Malysh; Olga V. Trapeznikova; Sergey Timofeev; Natalia Belyakova; Yuri Tokarev

doi:10.29133/yyutbd.1805326

Identification of Wolbachia Strains in Two Sibling Species of Neoseiulus Predatory Mites and Their Prey

Abstract

Wolbachia screening in mites is necessary for understanding of how their biological functions can be affected, including development of approaches to induce parthenogenesis, making the predator’s cultures more effective and stable. Here we studied Wolbachia infection in two sibling species of Neoseiulus predatory mites (one thelytokous and another bisexual) as well as their feed mites to test two working hypotheses: 1) a thelytokous mite Neoseiulus agrestis harbors Wolbachia, unlike its bisexual sibling species Neoseiulus neoagrestis and 2) feed mites are not the source of Wolbachia detection in Neoseiulus. To test these hypotheses, we performed PCR screening and multilocus sequence typing. It showed Wolbachia infection in N. agrestis, but not N. neoagrestis. Since the former is a thelytokous species, and the latter is not, Wolbachia might contribute to this peculiarity. The Wolbachia isolate from N. agrestis belongs to the supergroup B, being similar to the strains from lepidopteran insects as well as Syrphidae (Diptera). Wolbachia infection status of the thelytokous species N. agrestis is shown for the first time. As for the feed mites, Wolbachia was not detected in Carpoglyphus lactis and Thyreophagus entomophagus, but occurred in Tyrophagus putrescentiae. That bacterial strain formed a basal branch in relation to the supergroup B and demonstrated only a partial genetic identity to the Czech isolate from T. putrescentiae. Thus, Wolbachia from the predatory and feed mites are genetically different. The new Wolbachia sequences are deposited to GenBank serving as an important source of molecular data for comparative studies of Wolbachia parasites.

Keywords

Project Number

The research is supported by Russian Science Foundation, project # 20-66-47010, and the State Assignment, project # FGEU-2025-0002.

Ethical Statement

Ethical approval is not required for this study as it doesn’t involve human or animal research.

Thanks

The authors are indebted to Alexander A. Khaustov (Tyumen State University, Institute of Environmental and Agricultural Biology (X-BIO), Russia) for providing the predatory mites N. agrestis and N. neoagrestis as a part of the collaboration on this project and Ken Smith (Santo Domingo, Dominican Republic) for English grammar and style correction of the manuscript. Yury Yu. Ilinsky (Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences) is gratefully acknowledged for criticism given on an early draft of the manuscript.

References

Andrianov, B. V. (2022). Bacterial symbionts and pathogens in populations of Phytoseiidae mites (Phytoseiidae, Mesostigmata). Biology Bulletin Reviews, 12(1), S78–84. https://doi.org/10.1134/S2079086422070027
Amano, H., & Chant, D. A. (1986). Laboratory studies on the feeding habits, reproduction and development of three phytoseiid species, Typhlodromus pomi, Phytoseius macropilis and Amblyseius finlandicus (Acari: Phytoseiidae), occurring on abandoned apple trees in Ontario, Canada. Experimental and Applied Acarology, 2(4), 299–313.
Amini, S., Fathipour, Y., Hoffmann, A., & Mehrabadi, M. (2024). Wolbachia affect female mate preference and offspring fitness in a parasitoid wasp. Pest Management Science, 80(10), 5432–5439. https://doi.org/10.1002/ps.8272
Ashraf, S. E., Asmaa, R. A., & Eman, H. W. (2023). Developmental and life table of Neoseiulus californicus (Acari: Phytoseiidae) fed on three astigmatid mites and Tetranychus urticae (Acari: Tetranychidae). Egyptian Journal of Plant Protection Research Institute, 6(1), 64–73.
Azevedo, L. H., Castilho, R. D. C., & De Moraes, G. J. (2016). Suitability of the litchi erineum mite, Aceria litchii (Keifer), as prey for the mite Phytoseius intermedius Evans & MacFarlane (Acari: Eriophyidae, Phytoseiidae). Systematic and Applied Acarology, 21(3), 270–278. https://doi.org/10.11158/saa.21.3.2
Bagheri, Z., Talebi, A. A., Asgari, S., & Mehrabadi, M. (2019). Wolbachia induce cytoplasmic incompatibility and affect mate preference in Habrobracon hebetor to increase the chance of its transmission to the next generation. Journal of Invertebrate Pathology, 163, 1–7. https://doi.org/10.1016/j.jip.2019.02.005
Bakr, A., Rezk, H. A., Abd El-Hamid, M. M., & Osman, S. I. (2021). Studying the biology of Carpoglyphus lactis (L.) reared on dried apricots and its control using plant oil extracts. Alexandria Science Exchange Journal, 42(2), 407–411. https://doi.org/10.21608/asejaiqjsae.2021.171640
Baldo, L., Bordenstein, S., Wernegreen, J. J., & Werren, J. H. (2006a). Widespread recombination throughout Wolbachia genomes. Molecular Biology and Evolution, 23(2), 437–449. https://doi.org/10.1093/molbev/msj049

Baldo, L., Dunning Hotopp, J. C., Jolley, K. A., Bordenstein, S. R., Biber, S. A., Choudhury, R. R., Hayashi, C., Maiden, M. C., Tettelin, H., & Werren, J. H. (2006b). Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Applied and Environmental Microbiology, 72(11), 7098–7110. https://doi.org/10.1128/AEM.00731-06
Baldo, L., Lo, N., & Werren, J. H. (2005). Mosaic nature of the Wolbachia surface protein. Journal of Bacteriology, 187(15), 5406–5418. https://doi.org/10.1128/jb.187.15.5406-5418.2005
Blommers, L. (1974). Species of the genus Amblyseius Berlese, 1914, from Tamatave, east Madagascar (Acarina: Phytoseiidae). Bulletin Zoologisch Museum, 3(19), 143–148.
Braig, H. R., Zhou, W., Dobson, S. L., & O’Neill, S. L. (1998). Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. Journal of Bacteriology, 180(9), 2373–2378. https://doi.org/10.1128/JB.180.9.2373-2378.1998
Breeuwer, J. A., & Jacobs, G. (1996). Wolbachia: intracellular manipulators of mite reproduction. Experimental and Applied Acarology, 20, 421–434. https://doi.org/10.1007/BF00053306
Burdina, E. V., & Gruntenko, N. E. (2022). Physiological aspects of Wolbachia pipientis–Drosophila melanogaster relationship. Journal of Evolutionary Biochemistry and Physiology, 58(2), 303–317. https://doi.org/10.1134/s0022093022020016
Bykov, R., Kerchev, I., Demenkova, M., Ryabinin, A., & Ilinsky, Y. (2020). Sex-specific Wolbachia infection patterns in populations of Polygraphus proximus Blandford (Coleoptera; Curculionidae: Scolytinae). Insects, 11(8), 547. https://doi.org/10.3390/insects11080547
Bykov, R., Yurlova, G., Demenkova, M., & Ilinsky, Y. (2021). Is Aporia crataegi unsuitable host of Wolbachia symbionts? Plant Protection News, 104(1), 53–60. https://doi.org/10.31993/2308-6459-2021-104-1-14945
Casiraghi, M., Bordenstein, S. R., Baldo, L., Lo, N., Beninati, T., Wernegreen, J. J., Werren, J. H., & Bandi, C. (2005). Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F super-group, and evidence for further diversity in the Wolbachia tree. Microbiology, 151(12), 4015–4022. https://doi.org/10.1099/mic.0.28313-0
Cavalcante, A. C., Demite, P. R., Amaral, F. S., Lofego, A. C., & De Moraes, G. J. (2017). Complementary description of Neoseiulus tunus (De Leon) (Acari: Mesostigmata: Phytoseiidae) and observation on its reproductive strategy. Acarologia, 57(3), 591–599. https://doi.org/10.24349/acarologia/20174178
Chmielewski, W. (1990). Bio-ecology and population development of Thyreophagus entomophagus - an acarid mite found in beehives. Pszczelnicze Zeszyty Naukowe. 34, 31–42.
Chmielewski, W. (2002). Acaro-entomological contaminations of propolis. Journal of Apicultural Science, 46, 17–23.
Çobanoğlu, S., & Güldali, B. (2017). Plant parasitic and predatory mites (Acari: Tetranychidae, Phytoseiidae) and population density fluctuation of two-spotted spider mite (Tetranychus urticae Koch) on strawberry in the Mersin province of Turkey. Journal of Zoological Sciences, 5(2), 57–67.
Duron, O., Binetruy, F., Noël, V., Cremaschi, J., McCoy, K. D., Arnathau, C., Plantard, O., Goolsby, J., Pérez de León, A. A., Heylen, D. J., & Van Oosten, A. R. (2017). Evolutionary changes in symbiont community structure in ticks. Molecular ecology, 26(11), 2905–2921. https://doi.org/10.1111/mec.14094
Erban, T., Klimov, P. B., Harant, K., Talacko, P., Nesvorna, M., & Hubert, J. (2021). Label-free proteomic analysis reveals differentially expressed Wolbachia proteins in Tyrophagus putrescentiae: Mite allergens and markers reflecting population-related proteome differences. Journal of Proteomics, 249, 104356. https://doi.org/10.1016/j.jprot.2021.104356
Famah Sourassou, N., Hanna, R., Breeuwer, J. A., Negloh, K., de Moraes, G. J., & Sabelis, M. W. (2014). The endosymbionts Wolbachia and Cardinium and their effects in three populations of the predatory mite Neoseiulus paspalivorus. Experimental and Applied Acarology, 64(2), 207–221. https://doi.org/10.1007/s10493-014-9820-0
Farazmand, A., Jalaeian, M., Kamali, H., Saboori, A., Tixier, M. S., & Kreiter, S. (2023). Phytoseiidae (Acari: Mesostigmata) in four provinces of Iran. Persian Journal of Acarology, 12(1), 21–58. https://doi.org/10.22073/pja.v12i1.77425
Folmer, O., Hoeh, W. R., Black, M. B., & Vrijenhoek, R. C. (1994). Conserved primers for PCR amplification of mitochondrial DNA from different invertebrate phyla. Molecular Marine Biology and Biotechnology, 3(5), 294–299.
Fu, X. T., Zeng, K. K., Huo, Z. J., Chang, J., & Meng, R. X. (2025). Demographic and predatory parameters of a thelytokous phytoseiid mite as a biocontrol agent for spider mites. Pest Management Science, 81(8), 4540–4547. https://doi.org/10.1002/ps.8811
Fukatsu, T., & Nikoh, N. (1998). Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Applied and Environmental Microbiology, 64(10), 3599–3606. https://doi.org/10.1128/AEM.64.10.3599-3606.1998
Gagalova, K. K., Whitehill, J. G., Culibrk, L., Lin, D., Lévesque-Tremblay, V., Keeling, C. I., Coombe, L., Yuen, M. M., Birol, I., Bohlmann, J. & Jones, S. J. (2022). The genome of the forest insect pest Pissodes strobi reveals genome expansion and evidence of a Wolbachia endosymbiont. G3 Genes Genomes Genetics, 12(4), jkac038. https://doi.org/10.1093/g3journal/jkac038
Gaponyuk, I. L. (1989). Discovery of thelytoky in the predatory mite Amblyseius aurescens (Parasitiformes, Phytoseiidae). Vestnik Zoologii, 4, 82.
Glowska, E., Dragun-Damian, A., Dabert, M., & Gerth, M. (2015). New Wolbachia supergroups detected in quill mites (Acari: Syringophilidae). Infection, Genetics and Evolution, 30, 140–146. https://doi.org/10.1016/j.meegid.2014.12.019
Gu, X. Y., Li, G. Y., & Zhang, Z. Q. (2020). Indirect effects in predator-prey interaction: development and predation rates by immature Neoseiulus cucumeris increased by odour from its prey (Tyrophagus putrescentiae). Systematic and Applied Acarology, 25(7), 1247–1256. https://doi.org/10.11158/saa.25.7.7
Hall, T. A. (1999). BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Hoy, M. A., & Jeyaprakash, A. (2005). Microbial diversity in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae) and its prey, Tetranychus urticae (Acari: Tetranychidae). Biological Control, 32(3), 427–441. https://doi.org/10.1016/j.biocontrol.2004.12.012
Hubert, J., Glowska-Patyniak, E., Dowd, S.E., & Klimov, P.B. (2025). Cardinium disrupts Wolbachia–host dynamics in the domestic mite Tyrophagus putrescentiae: evidence from manipulative experiments. MSystems, 10(5), e01769-24. https://doi.org/10.1128/msystems.01769-24
Johanowicz, D. L., & Hoy, M. A. (1996). Wolbachia in a predator–prey system: 16S ribosomal DNA analysis of two phytoseiids (Acari: Phytoseiidae) and their prey (Acari: Tetranychidae). Annals of the Entomological Society of America, 89(3), 435–441. https://doi.org/10.1093/aesa/89.3.435
Jolley, K. A., Bray, J. E., & Maiden, M. C. J. (2018). Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Research, 3, 124. https://doi.org/10.12688/wellcomeopenres.14826.1
Kazemi, S., Mohammad-Doustaresharaf, M., & Döker, I. (2022). An annotated checklist of the Iranian Phytoseiidae (Acari: Mesostigmata), with an updated key to the species. Systematic and Applied Acarology, 27(4), 697–748. https://doi.org/10.11158/saa.27.4.6
Kennett, C. E. (1958) Some predacious mites of the subfamilies Phytoseiinae and Aceosejinae (Acarina: Phytoseiidae, Aceosejidae) from Central California with descriptions of new species. Annals of the Entomological Society of America, 51(5), 471–479. https://doi.org/10.1093/aesa/51.5.471
Khaustov, V. A., Döker, I., Joharchi, O., Kazakov, D. V., Khaustov, A. A., Moradi, M., Fang, X-D., & Klimov, P. (2022). A new, broadly distributed species of predacious mites, Neoseiulus neoagrestis sp. nov. (Acari: Phytoseiidae) discovered through GenBank data mining and extensive morphological analyses. Systematic and Applied Acarology, 27(10), 2038–2061. https://doi.org/10.11158/saa.27.10.14
Khoo, J. J., Kurtti, T. J., Husin, N. A., Beliavskaia, A., Lim, F. S., Zulkifli, M. M. S., Al-Khafaji, A. M., Hartley, C., Darby, A. C., Hughes, G. L. et al. (2020). Isolation and propagation of laboratory strains and a novel flea-derived field strain of Wolbachia in tick cell lines. Microorganisms, 8, 988. https://doi.org/10.3390/microorganisms8070988
Klimov, P. B., Hubert, J., Erban, T., Perotti, M. A., Braig, H. R., Flynt, A., He, Q., & Cui, Y. (2024). Genomic and metagenomic analyses of the domestic mite Tyrophagus putrescentiae identify it as a widespread environmental contaminant and a host of a basal, mite-specific Wolbachia lineage (supergroup Q). International Journal for Parasitology, 54(13), 661–674. https://doi.org/10.1016/j.ijpara.2024.07.001
Klimov, P. B., Kolesnikov, V. B., Khaustov, A. A., Khaustov, V. A., Merckx, J., Duarte, M. V. A., Vangansbeke, D., Geudens, I., & Pepato, A. (2025). Typification of the economically important species Thyreophagus entomophagus (Acari: Astigmata: Acaridae) used for the industrial production of predatory mites: the designation of a neotype with detailed morphological and DNA sequence data. Animals, 15(3), 357. https://doi.org/10.3390/ani15030357
Klopfstein, S., van Der Schyff, G., Tierney, S., & Austin, A. D. (2018). Wolbachia infections in Australian ichneumonid parasitoid wasps (Hymenoptera: Ichneumonidae): evidence for adherence to the global equilibrium hypothesis. Biological Journal of the Linnean Society, 123(3), 518–534. https://doi.org/10.1093/biolinnean/blx157
Knapp, M., van Houten, Y., van Baal, E., & Groot, T. (2018). Use of predatory mites in commercial biocontrol: current status and future prospects. Acarologia, 58, 72–82. https://doi.org/10.24349/acarologia/20184275
Kolodochka, L. A. (1984). Analysis of some ecological characteristics of parthenogenetic and bisexual species of phytoseiid mites. Vestnik Zoologii, 5, 47–53 (in Russian).
Kolodochka, L. A., & Bondarev, V. Yu. (2014). To the species composition of plant-dwelling phytoseiid mites (Parasitiformes, Phytoseiidae) of the Lugansk region of Ukraine. Ukrainian Entomological Journal, 2, 52–56 (in Russian).
Krasavina, L., & Trapeznikova, O. (2020). Assessment of different species of fodder mites for mass rearing of the predatory mites Amblyseius swirskii and Neoseiulus cucumeris (Mesostigmata, Phytoseiidae) under laboratory conditions. Plant Protection News, 103(3), 177–181. https://doi.org/10.31993/2308-6459-2020-103-3-13943 (in Russian).
Krasavina, L., & Trapeznikova, O. (2022). Improvement of breeding methods of predatory mites Neoseiulus cucumeris and Transeius montdorensis for biological plant protection. Plant Protection News, 105(2), 87–93. https://doi.org/10.31993/2308-6459-2022-105-2-15269 (in Russian).
Kryukova, N. A., Kryukov, V. Y., Polenogova, O. V., Chertkova, Е. А., Tyurin, M. V., Rotskaya, U. N., Alikina, T., Kabilov, М. R., & Glupov, V. V. (2023). The endosymbiotic bacterium Wolbachia (Rickettsiales) alters larval metabolism of the parasitoid Habrobracon hebetor (Hymenoptera: Braconidae). Archives of Insect Biochemistry and Physiology, 114(4), e22053. https://doi.org/10.1002/arch.22053
Laidoudi, Y., Levasseur, A., Medkour, H., Maaloum, M., Ben Khedher, M., Sambou, M., Bassene, H., Davoust, B., Fenollar, F., Raoult, D., & Mediannikov, O. (2020). An earliest endosymbiont, Wolbachia massiliensis sp. nov., strain PL13 from the bed bug (Cimex hemipterus), type strain of a new supergroup T. International Journal of Molecular Sciences, 21(21), 8064. https://doi.org/10.3390/ijms21218064
Malferrari, G., Monferini, E., DeBlasio, P., Diaferia, G., Saltini, G., Del Vecchio, E., Rossi-Bernardi, L., & Biunno, I. (2002). High-quality genomic DNA from human whole blood and mononuclear cells. BioTechniques, 33(6), 1228–1230. https://doi.org/10.2144/02336bm09
Malik, A., Gulati, R., Duhan, K., & Poonia, A. (2018). Tyrophagus putrescentiae (Schrank) (Acari: Acaridae) as a pest of grains: A review. Journal of Entomology and Zoology Studies, 6(2543), e2550.
Malysh, J., Malysh, S., Kireeva, D., Kononchuk, A., & Demenkova, M. (2020). Detection of Wolbachia in larvae of Loxostege sticticalis (Pyraloidea: Crambidae) in European and Asian parts of Russia. Plant Protection News, 103(1), 49–52. https://doi.org/10.31993/2308-6459-2020-103-1-49-52
Minwuyelet, A., Petronio, G. P., Yewhalaw, D., Sciarretta, A., Magnifico, I., Nicolosi, D., Di Marco, R., & Atenafu, G. (2023). Symbiotic Wolbachia in mosquitoes and its role in reducing the transmission of mosquito-borne diseases: updates and prospects. Frontiers in Microbiology, 14, 1267832. https://doi.org/10.3389/fmicb.2023.1267832
Momen, F., Fahim, S., & Barghout, M. (2020). Mass production of predatory mites and their efficacy for controlling pests. In N. El-Wakeil, M. Saleh & M. Abu-hashim (Eds.), Cottage industry of biocontrol agents and their applications: Practical aspects to deal biologically with pests and stresses facing strategic crops (pp. 157–200). Cham: Springer International Publishing.
Moradi, M., Misharova, Y. V., Snigirev, V. V., Döker, I., Joharchi, O., & Khaustov, V. A. (2023a). Life history of Neoseiulus agrestis (Karg) (Acari: Phytoseiidae) fed on the storage mite, Thyreophagus sp. (Acari: Acaridae) at different temperatures. Acarologia, 63(3), 817–825. https://doi.org/10.24349/6x1q-8mmr
Moradi, M., Joharchi, O., Döker, I., Khaustov, V. A., Salavatulin, V. M., Popov, D. A., & Belyakova, N. A. (2023b). Effects of temperature on life table parameters of a newly described phytoseiid predator, Neoseiulus neoagrestis (Acari: Phytoseiidae) fed on Tyrophagus putrescentiae (Acari: Acaridae). Acarologia, 63(1), 31–40. https://doi.org/10.24349/n3ej-nn6s
Moran, N. A., & Baumann, P. (2000). Bacterial endosymbionts in animals. Current opinion in microbiology, 3(3), 270–275. https://doi.org/10.1016/S1369-5274(00)00088-6
Muro, T., Hikida, H., Fujii, T., Kiuchi, T., & Katsuma, S. (2023). Two complete genomes of male-killing Wolbachia infecting Ostrinia moth species illuminate their evolutionary dynamics and association with hosts. Microbial Ecology, 86(3), 1740–1754. https://doi.org/10.1007/s00248-023-02198-7
Pekas, A., De Craecker, I., Boonen, S., Wäckers, F. L., & Moerkens, R. (2020). One stone; two birds: concurrent pest control and pollination services provided by aphidophagous hoverflies. Biological Control, 149, 104328. https://doi.org/10.1016/j.biocontrol.2020.104328
Pekas, A., Palevsky, E., Sumner, J. C., Perotti, M. A., Nesvorna, M., & Hubert, J. (2017). Comparison of bacterial microbiota of the predatory mite Neoseiulus cucumeris (Acari: Phytoseiidae) and its factitious prey Tyrophagus putrescentiae (Acari: Acaridae). Scientific Reports, 7(1), 1–12. https://doi.org/10.1038/s41598-017-00046-6
Popov, D., & Belyakova, N. (2022). World experience in the production and use of phytoseiid mites. Plant Protection News, 105(2), 68–86. https://doi.org/10.31993/2308-6459-2022-105-2-15282 (in Russian).
Pournajafi, H., Khanjani, M., & Soltani, J. (2023). Sex-ratio deviation and sex-determining bacteria detected by multiplex PCR in the predatory mite Amblyseius swirskii (Acari: Phytoseiidae). Persian Journal of Acarology, 12(2), 337–344. https://doi.org/10.22073/pja.v12i2.77489
Romanov, D. A., & Zakharov, I. A. (2023). Distribution of symbiotic bacteria Spiroplasma, Rickettsia, Wolbachia in populations of Adalia bipunctata (Linnaeus, 1758). Symbiosis, 9, 11–13 https://doi.org/10.1007/s13199-023-00942-8
Sambrook, J., Fritsch, E., & Maniatis, T. (1989). Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory. Cold Spring Harbor, New York.
Sampson, C., Bennison, J., & Kirk, W. D. J. (2021). Overwintering of the western flower thrips in outdoor strawberry crops. Journal of Pest Science, 94, 143–152. https://doi.org/10.1007/s10340-019-01163-z
Sánchez-Ramos, I., & Castañera, P. (2000). Acaricidal activity of natural monoterpenes on Tyrophagus putrescentiae (Schrank), a mite of stored food. Journal of Stored Products Research, 37(1), 93–101. https://doi.org/10.1016/S0022-474X(00)00012-6
Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., & Sahl, J. W. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23), 7537–7541. https://doi.org/10.1128/AEM.01541-09
Sciarappa, W. J., & Swift, F. C. (1977). Biological studies of Typhlodromips sessor (Acarina: Phytoseiidae). Annals of the Entomological Society of America, 70(2), 285–288. https://doi.org/10.1093/aesa/70.2.285
Shaikevich, E., Bogacheva, A., Rakova, V., Ganushkina, L., & Ilinsky, Y. (2019). Wolbachia symbionts in mosquitoes: Intra- and intersupergroup recombinations, horizontal transmission and evolution. Molecular phylogenetics and evolution, 134, 24–34. https://doi.org/10.1016/j.ympev.2019.01.020
Shaikevich, E. V., Gorbacheva, A. A., & Romanov, D.A. (2023). Ectoparasitic mites: Vectors of bacterial symbionts among insects. Biology Bulletin of the Russian Academy of Sciences, 50, 338–347. https://doi.org/10.1134/S1062359023700231
Shaikevich, E. V., Romanov, D. A., & Zakharov, I. A. (2021). The diversity of Wolbachia and its effects on host reproduction in a single Adalia bipunctata (Coleoptera: Coccinellidae) population. Symbiosis, 85(2), 249–257. https://doi.org/10.1007/s13199-021-00808-x
Su, J., Dong, F., Liu, S. M., Lu, Y. H., & Zhang, J. P. (2019). Productivity of Neoseiulus bicaudus (Acari: Phytoseiidae) reared on natural prey, alternative prey, and artificial diet. Journal of Economic Entomology, 112(6), 2604–2613. https://doi.org/10.1093/jee/toz202
Szabo, A., & Penzes, B. (2013). A new method for the release of Amblyseius andersoni (Acari: Phytoseiidae) in young apple orchards. European Journal of Entomology, 110(3), 477–482. https://doi.org/10.14411/eje.2013.063
Tixier, M. S., Okassa, M., & Kreiter, S. (2012). An integrative morphological and molecular diagnostics for Typhlodromus pyri (Acari: Phytoseiidae). Zoologica Scripta, 41, 68–78. https://doi.org/10.1111/j.1463-6409.2011.00504.x
Tokarev, Y. S., Yudina, M. A., Malysh, J. M., Bykov, R. A., Frolov, A. N., Grushevaya, I. V., & Ilinsky, Y. Y. (2018). Prevalence rates of the endosymbiotic bacterium of the Wolbachia genus in natural populations of Ostrinia nubilalis and Ostrinia scapulalis (Lepidoptera: Pyraloidea: Crambidae) in Southwestern Russia. Russian Journal of Genetics: Applied Research, 8, 172–177. https://doi.org/10.1134/S2079059718020119
Toyoshima, S. (2021). A tool to survey predatory phytoseiid species against Thrips. Japanese Journal of Applied Entomology and Zoology, 65(4), 173–180. https://doi.org/10.1303/jjaez.2021.173
Tsolakis, H., Sinacori, M., Ragusa, E., & Lombardo, A. (2019). Biological parameters of Neoseiulus longilaterus (Athias-Henriot) (Parasitiformes, Phytoseiidae) fed on prey and pollen in laboratory conditions. Systematic and Applied Acarology, 24(9), 1757–1768. https://doi.org/10.11158/saa.24.9.12
Tuovinen, T., & Lindqvist, I. (2014). Effect of introductions of a predator complex on spider mites and thrips in a tunnel and an open field of pesticide-free everbearer strawberry. Journal of Berry Research, 4(4), 203–216. https://doi.org/10.3233/JBR-140081
Utkuzova, A. M., Chertkova, E. A., Kryukova, N. A., Malysh, J. M., & Tokarev, Y. S. (2025). “Hostbusters”: The bacterial endosymbiont Wolbachia of the parasitoid wasp Habrobracon hebetor improves its ability to parasitize lepidopteran hosts. Insects, 16(5), 464. https://doi.org/10.3390/insects16050464
Vicente dos Santos, V., & Tixier, M. S. (2017). Which molecular markers for assessing which taxonomic level? The case study of the mite family Phytoseiidae (Acari: Mesostigmata). Cladistics, 33(3), 251–267. https://doi.org/10.1111/cla.12166
Vogelstein, B., & Gillespie, D. (1979). Preparative and analytical purification of DNA from agarose. Proceedings of the National Academy of Sciences USA, 76(2), 615–619. https://doi.org/10.1073/pnas.76.2.615
Werren, J. H., & Windsor, D. M. (2000). Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proceedings of the Royal Society B: Biological Sciences, 267, 1277–1285. https://doi.org/10.1098/rspb.2000.1139
Werren, J. H., Zhang, W., & Guo, L. R. (1995). Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proceedings of the Royal Society B: Biological Sciences, 261, 55–63. https://doi.org/10.1098/rspb.1995.0117
White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky & T. J. White (Eds.), PCR Protocols: A Guide to Methods and Applications (pp. 315–322). Academic Press, New York, https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Wysoki, M. (1973). Further studies on karyotypes and sex determination of phytoseiid mites (Acarina: Mesostigmata). Genetica, 44, 139–145. https://doi.org/10.1007/BF00155967
Wysoki, M., & Bolland, H. R. (1983). Chromosome studies of phytoseiid mites (Acari: Gamasida). International Journal of Acarology, 9(2), 91–94. https://doi.org/10.1080/01647958308683319
Yu, C-H., Tsai, J-J., Lin, Y-H., Yu, S-J., & Liao, E-C. (2020). Identification the cross-reactive or species-specific allergens of Tyrophagus putrescentiae and development molecular diagnostic kits for allergic diseases. Diagnostics, 10, 665. https://doi.org/10.3390/diagnostics10090665
Zhang, K., Cao, J., Li, X., & Zhang, Z-Q. (2025). Investigating interspecific mating in the thelytokous predatory mite Amblyseius herbicolus (Chant) (Acari: Phytoseiidae), with comparative observations from three sexually reproducing phytoseiid species. Experimental and Applied Acarology, 95(8). https://doi.org/10.1007/s10493-025-01034-6
Zhang, K., & Zhang, Z. Q. (2021). The dried fruit mite Carpoglyphus lactis (Acari: Carpoglyphidae) is a suitable alternative prey for Amblyseius herbicolus (Acari: Phytoseiidae). Systematic and Applied Acarology, 26(11), 2167–2176. https://doi.org/10.11158/saa.26.11.15
Zhou, W. G., Rousset, F., & O’Neill, S. (1998). Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society B: Biological Sciences, 265, 509–515. https://doi.org/10.1098/rspb.1998.0324
Zhou, Y., Klimov, P. B., Gu, X., Yu, Z., Cui, X., Li, Q., Pan, R., Yuan, C., Cai, F., & Cui, Y. (2023). Chromosome-level genomic assembly and allergome inference reveal novel allergens in Tyrophagus putrescentiae. Allergy, 78(6), 1691–1695. https://doi.org/10.1111/all.15656

Details

Primary Language

English

Subjects

Entomology

Journal Section

Research Article

Authors

Julia Malysh ^*
0000-0002-7353-421X
Russian Federation

Svetlana Malysh
0000-0002-4749-6221
Russian Federation

Olga V. Trapeznikova
0000-0003-1353-467X
Russian Federation

Sergey Timofeev
0000-0001-6664-3971
Russian Federation

Natalia Belyakova
0000-0002-9192-5871
Russian Federation

Yuri Tokarev
0000-0003-0524-0778
Russian Federation

Publication Date

January 19, 2026

Submission Date

October 19, 2025

Acceptance Date

December 11, 2025

Published in Issue

Year 2026 Number: 1

DOI

https://doi.org/10.29133/yyutbd.1805326

IZ

https://izlik.org/JA49NR82GF

Cite

RIS / Bibtex

APA

Malysh, J., Malysh, S., Trapeznikova, O. V., Timofeev, S., Belyakova, N., & Tokarev, Y. (2026). Identification of Wolbachia Strains in Two Sibling Species of Neoseiulus Predatory Mites and Their Prey. Yuzuncu Yıl University Journal of Agricultural Sciences, 1, 1805326. https://doi.org/10.29133/yyutbd.1805326