Wolbachia infection in populations of the coniferous forest pest Dendrolimus superans sibiricus Tschetverikov, 1908 (Lepidoptera: Lasiocampidae)

Siberian silk moth (Dendrolimus superans sibiricus) is a very dangerous pest of coniferous trees, in particular, larch and various pine species. Outbreaks of this pest lead to defoliation and forest destruction in a vast area of the Asian part of Russia. Many biological agents, such as viruses, pathogenic microorganisms and parasitoids, prevent the growth of Siberian silk moth population. Here we consider non-pathogen symbiotic Wolbachia bacteria, which are transovarially transmitted between specimens from mother to offspring. This symbiont has an ability to affect biology of its host. In theory, Wolbachia can prevent the growth of population size or induce it, which determines the focus of interest in Wolbachia-host investigation. Two samples from a Siberian silk moth population collected in 2014 and 2016 in Khabarovsk area were studied for Wolbachia infection. We found a high Wolbachia prevalence in the population of Siberian silk moth, in particular, the sample of 2014 was totally infected and the sample of 2016 had 90 % infected specimens. There were at least two distinct Wolbachia strains reveled by analysis of two loci from the MLST protocol, namely f tsZ-36, f bpA-4 and f tsZ-22, f bpA-9. In this study, a possible role of Wolbachia in the symbiotic association with Siberian silk moth and general ways of investigation of this symbiosis are discussed.

1. Ahmed M.Z., Araujo-Jnr E.V., Welch J.J., Kawahara A.Y. Wolbachia in butterflies and moths: geographic structure in infection frequency. Frontiers Zoology. 2015;12(1):1.

2. Ahmed M.Z., Breinholt J.W., Kawahara A.Y. Evidence for common horizontal transmission of Wolbachia among butterflies and moths. BMC Evol. Biol. 2016;16(1):1.

3. 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. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl. Environ. Microbiol. 2006;72(11):7098-7110.

4. Choudhury R., Werren J.H. Unpublished primers. 2006. Available at http://troi.cc.rochester.edu/~wolb/FIBR/downloads.html#protocols.

5. Dedeine F., Vavre F., Fleury F., Loppin B., Hochberg M.E., Bouletreau M. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc. Natl. Acas. Sci. 2001;98(11): 6247-6252.

6. Dobson S.L., Bourtzis K., Braig H.R., Jones B.F., Zhou W., Rousset F., O’Neill S.L. Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem. Mol. Biology. 1999; 29(2):153-160.

7. Dobson S.L., Marsland E.J., Rattanadechakul W. Mutualistic Wolbachia infection in Aedes albopictus: Accelerating cytoplasmic drive. Genetics. 2002;160:1087-1094.

8. Dong P., Wang J.-J., Hu F., Jia F.-X. Influence of Wolbachia infection on the fitness of the stored-product pest Liposcelis tricolor (Psocoptera: Liposcelididae). J. Econ. Entomol. 2007;100(4):1476-1481.

9. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl. Acids Res. 2004;32(5):1792-1797.

10. Gninenko Y.I., Orlinskii A.D. Dendrolimus sibiricus in the coniferous forests of European Russia at the beginning of the twenty-first century. Eppo Bull. 2002;32(3):481-483.

11. Grodnitskiy D.L. Siberian silk moth and the fate of fir taiga. Priroda = Nature. 2004;11:49-56. (in Russian)

12. Harcombe W., Hoffmann A.A. Wolbachia effects in Drosophila melanogaster: in search of fitness benefits. J. Invertebrate Pathology. 2004;87:45-50.

13. Hosokawa T., Koga R., Kikuchi Y., Meng X.-Y., Fukatsu T. Wolbachia as a bacteriocyte- associated nutritional mutualist. Proc. Natl. Acad. Sci. 2010;107(2):769-774.

14. Huafeng L.F., Meizhen L.Z., Cui H. Pathogenic effect of Beauveria bassiana infected on Dendrolimus punctatus under different temperature and humidity. Chin. J. Appl. Ecol. 1998;9:195-200.

15. Ilinskiy Yu.Yu., Yudina M.A., Kalmykova Ye.A., Bykov R.A., Vysochina N.P., Vinarskaya N.P., Zakharov I.K. Wolbachia infection among fleas (Siphonaptera: Insecta) of Sverdlovsk region and Khabarovsk territory. Ekologicheskaya genetika = Ecological genetics. 2013;11(1):32-35. (in Russian)

16. Koltunov E.V., Erdakov L.N. Features of the long-term cyclic occurrence of outbreaks of different Siberian moth (Dendrolimus superans sibiricus Tschetv.) populations in Siberia. Sovremennye problemy nauki i obrazovaniya = Modern Problems of Science and Education. 2013;6. (in Russian)

17. Kondakov Yu.P. Massovye razmnozhenija sibirskogo shelkoprjada v lesah Krasnojarskogo kraja [Population booms of Siberian silk moth in the forests of the Krasnoyarsk Kray]. Entomologicheskie issledovaniya v Sibiri [Entomological Studies in Siberia]. Krasnoyarsk, 2002;2:25-74. (in Russian)

18. Kremer N., Voronin D., Charif D., Mavingui P., Mollereau B., Vavre F. Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog. 2009;5(10):e1000630.

19. McCall J.W., Kramer L., Genchi C., Guerrero J., Dzimianski M.T., Mansour A., McCall S.D., Carson B. Effects of doxycycline on heartworm embryogenesis, transmission, circulating microfilaria, and adult worms in microfilaremic dogs. Vet. Parasitol. 2014;206(1): 5-13.

20. Mikkola K., Stahls G. Morphological and molecular taxonomy of Dendrolimus sibiricus Chetverikov stat. rev. and allied lappet moths (Lepidoptera: Lasiocampidae), with description of a new species. Entomol. Fennica. 2008;19(2):65.

21. Osborne S.E., Leong Y.S., O’Neill S.L., Johnson K.N. Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog. 2009;5(11):1- 9.

22. Rozhkov A.S. Sibirskiy shelkopryad [Siberian silk moth]. Moscow, AN SSSR Publ., 1963. (in Russian)

23. Rozhkov A.S. Massovoe razmnozhenie sibirskogo shelkopryada i mery borby s nim [Population booms of Siberian silk moth and methods for controlling them]. Moscow, Nauka Publ., 1965. (in Russian)

24. Salunke B.K., Salunkhe R.C., Dhotre D.P., Walujkar S.A., Khandagale A.B., Chaudhari R., Chandode R.K., Ghate H.V., Patole M.S., Werren J.H., Shouche Y.S. Determination of Wolbachia diversity in butterflies from Western Ghats, India, by a multigene approach. Appl. Environ. Microbiol. 2012;78:4458–4467.

25. Salunkhe R.C., Narkhede K.P., Shouche Y.S. Distribution and evolutionary impact of Wolbachia on butterfly hosts. Indian J. Microbiol. 2014;54(3):249-254.

26. Starr D.J., Cline T.W. A host parasite interaction rescues Drosophila oogenesis defects. Nature. 2002;418:76-79.

27. Sungpradit S., Nuchprayoon S. Wolbachia of arthropods and filarial nematodes: biology and applications. Chula Med. J. 2010;54:605-621.

28. Tagami Y., Miura K. Distribution and prevalence of Wolbachia in Japanese populations of Lepidoptera. Insect Mol. Biol. 2004;13(4): 359-364.

29. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 2013;30:2725-2729.

30. Teixeira L., Ferreira A., Ashburner M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 2008;6(12):2753-2763.

31. van Nouhuys S., Kohonen M., Duplouy A. Wolbachia increases the susceptibility of a parasitoid wasp to hyperparasitism. J. Exp. Biol. 2016;219(19):2984-2990.

32. Weisman N.Ya., Ilinskiy Yu.Yu., Golubovskiy M.D. Population genetic analysis of Drosophila melanogaster lifespan: similar effects of Wolbachia endosymbiont and tumor suppressor lgl under temperature stress. Zhurnal obshchey biologii = Journal of General Biology. 2009;70(5):425-434. (in Russian)

33. Werren J.H., Windsor D. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc. Roy. Soc. Lond. 2000;267: 1277-1285.

34. Werren J.H., Baldo L., Clark M.E. Wolbachia: master manipulators of invertebrate biology. Nature Rev. Microbiol. 2008;6(10):741-751.

35. Zabal-Aguirre M., Arroyo F., Bella J.L. Distribution of Wolbachia infection in Chorthippus parallelus populations within and beyond a Pyrenean hybrid zone. Heredity. 2010;104(2):174-184.

36. Zolotukhin V.V. Kokonopryady (Lepidoptera: Lasiocampidae) fauny Rossii i sopredelnyh territoriy [Lasiocampidae (Lepidoptera) of Russia and adjacent territories]. Ulyanovsk, Korporatsiya tehnologiy prodvizheniya Publ., 2015. (in Russian)