Prevalence rates of Wolbachia endosymbiotic bacterium in natural populations of Ostrinia Nubilalis and Ostrinia Scapulalis (Lepidoptera: Pyraloidea: Crambidae) in South-Western Russia

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Abstract


Background. Endosymbiotic bacteria of the genus Wolbachia are widespread in arthropods and often cause reproductive abnormalities in lepidopteran insects, including corn borers of the genus Ostrinia. Wolbachia-Ostrinia is a promising model for studies of parasite-host interactions yet parasite prevalence in natural insect host populations remains unknown.

Materials and Methods. Molecular genetic screening and statistical analysis is applied to evaluate prevalence rates of Wolbachia in sympatric populations of two corn borer species. Individual genomic DNA samples were extracted from last instar larvae collected in nature from different forage plants. For each sample of DNA showing positive signal with insect-specific primers the detection is performed using three diagnostic loci of Wolbachia: 16SrRNA, gatB and fbpA.

Results. Wolbachia-positive signal is obtained for 13.5% larvae of Ostrinia nubilalis (N = 141) and 31.9% larvae of Ostrinia scapulalis (N = 138). In different localities the Wolbachia prevalence ranged from 2.9% (N = 34) to 65.8% (N = 38). Significantly higher rates of Wolbachia prevalence in insects from mugwort and hemp (O. scapulalis) as compared to those from corn (O. nubilalis) are revealed in three out of four localities.

Conclusions. Endosymbiotic bacteria of the genus Wolbachia are revealed in natural populations of corn borers for the first time for Eastern Europe. The prevalence rates can be high and this should be taken into consideration when reproductive isolation is examined in population of these hosts as well as establishment of laboratory cultures is performed.


Yuri S Tokarev

Author for correspondence.
jumacro@yahoo.com
All-Russian Institute for Plant Protection
Russian Federation, Pushkin, Saint Petersburg, Russia

Senior researcher, Laboratory of microbiological control

Mariya A Yudina

maryjudina@gmail.com
Institute of Cytology and Genetics SB RAS
Russian Federation, Novosibirsk, Russia

Engineer, Department of Insect Genetics

Julia M Malysh

malyshjm@mail.ru
All-Russian Institute for Plant Protection
Russian Federation, Pushkin, Saint Petersburg, Russia

Researcher, Laboratory of agricultural entomology

Roman A Bykov

bykovra@bionet.nsc.ru
Institute of Cytology and Genetics SB RAS
Russian Federation, Novosibirsk, Russia

Researcher, Department of insect genetics

Andrei N Frolov

cornborer@gmail.com
All-Russian Institute for Plant Protection
Russian Federation, Pushkin, Saint Petersburg, Russia

Head of laboratory, Laboratory of agricultural entomology

Inna V Grushevaya

grushevaya_12@mail.ru
All-Russian Institute for Plant Protection
Russian Federation, Pushkin, Saint Petersburg, Russia

Junior researcher, Laboratory of agricultural entomology

Yury Y Ilinsky

paulee@bionet.nsc.ru
Institute of Cytology and Genetics SB RAS
Russian Federation, Novosibirsk, Russia

Senior Researcher, Department of Insect Genetics

  • Williams KP, Sobral BW, Dickerman AW. A robust species tree for the alphaproteobacteria. J Bacteriol. 2007;189(13):4578-4586. doi: 10.1128/JB.00269-07.
  • Ilinsky Y. Coevolution of Drosophila melanogaster mtDNA and Wolbachia genotypes. PLoS One. 2013;8(1): e54373. doi: 10.1371/journal.pone.0054373.
  • Salunkhe RC, Narkhede KP, Shouche YS. Distribution and evolutionary impact of Wolbachia on butterfly hosts. Indian J Microbiol. 2014;54(3):249-254. doi: 10.1007/s12088-014-0448-x.
  • Darby AC, Armstrong SD, Bah GS, et al. Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res. 2012;22(12):2467-77. doi: 10.1101/gr.138420.112.
  • Ikeya T, Broughton S, Alic N, et al. The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proc Biol Sci. 2009;206:3799-3807. doi: 10.1098/rspb.2009.0778.
  • Wong ZS, Brownlie JC, Johnson KN. Oxidative Stress Correlates with Wolbachia-Mediated Antiviral Protection in Wolbachia-Drosophila Associations. Appl Environ Microbiol. 2015;81(9):3001-3005. doi: 10.1128/AEM.03847-14.
  • Fry AJ, Palmer MR, Rand DM. Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity. 2004;93:379-389. doi: 10.1038/sj.hdy.6800514.
  • Вайсман Н.Я., Илинский Ю.Ю., Голубовский М.Д. Популяционно-генетический анализ продолжительности жизни Drosophila melanogaster: сходные эффекты эндосимбионта Wolbachia и опухолевого супрессора lgl в условиях температурного стресса // Журнал общей биологии. – 2009. – Т. 70. – № 5. – С. 425–434. [Vaysman NYa, Ilinskiy YuYu, Golubovskiy MD. Population genetic analysis of Drosophila melanogaster longevity: similar effects of endosymbiont Wolbachia and tumor suppressor lgl under conditions of temperature stress. Zhurnal obschey biologii. 2009;70(5):425-434. (In Russ.)]
  • Salunke BK, Salunkhe RC, Dhotre DP, et al. Determination of Wolbachia diversity in butterflies from Western Ghats, India, by a multigene approach. Appl Environ Microbiol. 2012;78:4458-4467. doi: 10.1128/AEM.07298-11.
  • Tagami Y, Miura K. Distribution and prevalence of Wolbachia in Japanese populations of Lepidoptera. Insect Mol Biol. 2004;13(4),359-364. doi: 10.1111/j.0962-1075.2004.00492.x.
  • Baldo L, Hotopp JCD, Jolley KA, et al. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol. 2006;72 (11): 7098-7110. doi: 10.1128/AEM.00731-06.
  • Russell JA, Goldman-Huertas B, Moreau CS, et al. Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies. Evolution. 2009;63(3):624-640. doi: 10.1111/j.1558-5646.2008.00579.x.
  • Solovyev VI, Ilinsky Y, Kosterin OE. Genetic integrity of four species of Leptidea (Pieridae, Lepidoptera) as sampled in sympatry in West Siberia. Comparative Cytogenetics. 2015;9(3):299. doi: 10.3897/CompCytogen.v9i3.4636.
  • Frolov AN, Audiot P, Bourguet D, et al. “From Russia with lobe”: genetic differentiation in trilobed uncus Ostrinia spp. follows food plant, not hairy legs. Heredity. 2012;108(2):146-156. doi: 10.1038/hdy.2011.58.
  • Pelissie B, Ponsard S, Tokarev YS, et al. Did the introduction of maize into Europe provide enemy-free space to O. nubilalis? – parasitism differences between two sibling species of the genus Ostrinia. J Evol Biol. 2010;23:350-61. doi: 10.1111/j.1420-9101.2009.01903.x.
  • Werren JH. Biology of Wolbachia. Ann Rev Entomol. 1997;42:587-609. doi: 10.1146/annurev.entO.42.1.587.
  • Kageyama D, Nishimura G, Hoshizaki S, Ishikawa Y. Feminizing Wolbachia in an insect, Ostrinia furnacalis (Lepidoptera: Crambidae). Heredity. 2002;88(6):444-449. doi: 10.1038/sj.hdy.6800077.
  • Kageyama D, Traut W. Opposite sex-specific effects of Wolbachia and interference with the sex determination of its host Ostrinia scapulalis. Proc Biol Sci. 2004;271(1536):251-258. doi: 10.1098/rspb.2003.2604.
  • Kageyama D, Ohno S, Hoshizaki S, Ishikawa Y. Sexual mosaics induced by tetracycline treatment in the Wolbachia-infected adzuki bean borer, Ostrinia scapulalis. Genome. 2003;46(6):983-989. doi: 10.1139/g03-082.
  • Sakamoto H, Ishikawa Y, Sasaki T, et al. Transinfection reveals the crucial importance of Wolbachia genotypes in determining the type of reproductive alteration in the host. Genet Res. 2005;85(3):205-210. doi: 10.1017/S0016672305007573.
  • Sakamoto H, Kageyama D, Hoshizaki S, Ishikawa Y. Sex-specific death in the Asian corn borer moth (Ostrinia furnacalis) infected with Wolbachia occurs across larval development. Genome. 2007;50(7):645-52. doi: 10.1139/G07-041.
  • Hebert PDN, Penton EH, Burns JM, et al. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA. 2004;101:14812-14817. doi: 10.1073/pnas.0406166101.
  • Choudhury R, Werren JH. 2006. Unpublished primers.
  • Werren JH, Windsor D. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc Biol Sci. 2000;267:1277-1285. doi: 10.1098/rspb.2000.1139.
  • Юдина М.А., Дубатолов В.В., Быков Р.А., Илинский Ю.Ю. Симбиотическая бактерия Wolbachia в популяциях вредителя хвойных лесов Dendrolimus superans sibiricus Tschetverikov, 1908 (Lepidoptera: Lasiocampidae) // Вавиловский журнал генетики и селекции. – 2016. – Т. 20. – № 6. – С. 899–903. [Yudina MA, Dubatolov VV, Bykov RA, Ilinsky YuYu. Symbiotic bacteria Wolbachia in populations of the coniferous forests pest Dendrolimus superans sibiricus Tschetverikov, 1908 (Lepidoptera: Lasiocampidae). Vavilovskii Zhurnal Genetiki i Selektsii (Vavilov Journal of Genetics and Breeding). 2016;20(6):899-903. (In Russ.)]. doi: 10.18699/VJ16.208.
  • Jiggins FM, Hurst GDD, Dolman CE, Majerus MEN. High prevalence male-killing Wolbachia in the butterfly Acraea encedana. J Evol Biol. 2000;13:495-501. doi: 10.1046/j.1420-9101.2000.00180.x.
  • Dyson EA, Kamath MK, Hurst GDD. Wolbachia infection associated with all-female broods in Hypolimnas bolina (Lepidoptera: Nymphalidae): evidence for horizontal transmission of a butterfly male killer. Heredity. 2002;88(3):166-171. doi: 10.1038/sj.hdy.6800021.
  • Rasgon JL, Scott TW. Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: parameter estimates and infection dynamics in natural populations. Genetics. 2003;165(4):2029-2038.
  • Khrabrova NV, Bukhanskaya ED, Sibataev AK, Volkova TV. The distribution of strains of endosymbiotic bacteria Wolbachia pipientis in natural populations of Culex pipiens mosquitoes (Diptera: Culicidae). European Mosquito Bulletin. 2009;(27):18-22.
  • Shaikevich EV, Vinogradova EB, Bouattour A, de Almeida APG. Genetic diversity of Culex pipiens mosquitoes in distinct populations from Europe: contribution of Cx. quinquefasciatus in Mediterranean populations. Parasites & Vectors. 2016;9(1):47. doi: 10.1186/s13071-016-1333-8.
  • Hoffmann AA, Clancy DJ, Merton E. Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics. 1994;136(3):993-999.
  • Илинский Ю.Ю., Захаров И.К. Эндосимбионт Wolbachia в евразийских популяциях Drosophila melanogaster // Генетика. – 2007. – Т. 43. – № 7. – С. 905–915. [Ilinsky YY, Zakharov IK. The endosymbiont Wolbachia in Eurasian populations of Drosophila melanogaster. Russ J Genet. 2007;43:748. doi: 10.1134/S102279540707006X.
  • Yamada R, Floate KD, Riegler M, O’Neill SL. Male development time influences the strength of Wolbachia-induced cytoplasmic incompatibility expression in Drosophila melanogaster. Genetics. 2007;177(2):801-8. doi: 10.1534/genetics.106.068486.
  • Ilinsky YY, Zakharov IK. Cytoplasmic incompatibility in Drosophila melanogaster is caused by different Wolbachia genotypes. Russian Journal of Genetics: Applied Research. 2011;1(5):458.
  • Wallau GL, da Rosa MT, De Ré FC, Loreto ELS. Wolbachia from Drosophila incompta: just a hitchhiker shared by Drosophila in the New and Old World? Insect Molecular Biology. 2016;25(4):487-499. doi: 10.1111/imb.12237.

Supplementary files

Supplementary Files Action
1. Fig. 1. Locations of insect samples in Krasnodar Territory (1 – hamlet Slobodka; 2 – town Slavyansk-na-Kubani; 3 – settlement Botanika) and Belgorod Territory (4 – settlement Maiskiy) View (597KB) Indexing metadata
2. Table 1 Wolbachia prevalence rates in local populations of corn borer of the Ostrinia genus Download (14KB) Indexing metadata
3. Table 2 A summary of Wolbachia prevalence rates in corn borer Ostrinia from different forage plants Download (41KB) Indexing metadata

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Copyright (c) 2017 Tokarev Y.S., Yudina M.A., Malysh J.M., Bykov R.A., Frolov A.N., Grushevaya I.V., Ilinsky Y.Y.

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