Drosophila melanogaster inhabiting northern regions of European Russia are infected with Wolbachia which adversely affects their life span

Wolbachia is a genus of bacteria causing intracellular infection in the natural populations of Drosophila melanogaster on all continents. In D. melanogaster, Wolbachia affects various life history traits, behaviour, sensitivity to stress and viral infection. The phenotypic effects of Wolbachia might evolve to promote its further spreading, increasing the interest in exploring the spread of Wolbachia, in particular, at the boundar­ies of the D. melanogaster habitat, in association with the effects on vital traits of host species. In this paper, we present data on the level of Wolbachia infection in two D. melanogaster populations from the northern regions of European Russia: Alexandrov (56.41° N, 38.72° E) and Valday (58.02° N, 33.24° E). The flies were collected in private apple gardens located in two small hamlets without supermarkets or fruit markets, from 2010 to 2015. The both populations demonstrated the same level of infection: in average, 69.7 % of the inbred lines (ILs) obtained from single females of the Alexan­drov population and 68.4 % of ILs obtained from single females of the Valday population. The infection rate varied from year to year showing a tendency to reduc­tion, its overall level being within the range previously observed in other habitats. Life spans were compared in sub-lines of the same IL, one infected with Wolbachia and the other treated with tetracycline healing this infection. In four out of five ILs, the lifespan of both males and females was severely affected by Wolbachia; in different ILs, the mean life spans reduced from 1.8 to 5.4 times and from 1.4 to 2.4 times, respectively. Our results confirm that, despite D. melanogaster widespread distribution, the Wolbachia effect on their life span has been mostly negative.                                     

1. Alexandrov I.D., Alexandrova M.V., Goryacheva I.I., Rochina N.V., Shaikevich E.V., Zakharov I.A. Removing endosymbiotic Wolbachia specifically decreases lifespan of females and competitiveness in a laboratory strain of Drosophila melanogaster. Russ. J. Genet. 2007;43(10):1147-1152. DOI 10.1134/S1022795407100080.

2. Bi J., Sehgal A., Williams J.A., Wang Y.F. Wolbachia affects sleep behavior in Drosophila melanogaster. J. Insect Physiol. 2018;27:81-88. DOI 10.1016/j.jinsphys.2018.02.011.

3. Brownlie J.C., Cass B.N., Riegler M., Witsenburg J.J., Iturbe-Ormaetxe I., McGraw E.A., O’Neill S.L. Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog. 2009;5(4): e1000368. DOI 10.1371/journal.ppat.1000368.

4. Brummel T., Ching A., Seroude L., Simon A.F., Benzer S. Drosophila lifespan enhancement by exogenous bacteria. Proc. Natl. Acad. Sci. USA. 2004;101:12974-12979. DOI 10.1073/pnas.0405207101.

5. Bykov R.A., Ilinskii Yu.Yu., Voloshina M.A., Zakharov I.K. Prevalence and genotypic diversity of the symbiotic bacterium Wolbachia in the Drosophila melanogaster population of Nalchik. Vavilovskii Zhur-nal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2014;18(2):315-319. (in Russian)

6. Carey J.R. Longevity: The Biology and Demography of Life Span. Princeton, NT: Princeton Univ. Press, 2003.

7. Carrington L.B., Leslie J., Weeks A.R., Hoffmann A.A. The popcorn Wolbachia infection of Drosophila melanogaster: can selection alter Wolbachia longevity effects? Evolution. 2009;63(10):2648-2657. DOI 10.1111/j.1558-5646.2009.00745.x.

8. Falconer D.S., Mackay T.F.C. Introduction to Quantitative Genetics. 4th edn. Longman: Harlow, 1996.

9. Fry A.J., Palmer M.R., Rand D.M. Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity. 2004;93:379-389. DOI 10.1038/sj.hdy.6800514.

10. Grönke S., Clarke D.F., Broughton S., Andrews T.D., Partridge L. Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet. 2010;6(2):e1000857. DOI 10.1371/journal.pgen.1000857.

11. Hoffmann A.A., Clancy D.J., Merton E. Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics. 1994; 136:993-999.

12. Hoffmann A.A., Hercus M., Dagher H. Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster. Genetics. 1998;148:221-231.

13. Holden P.R., Jones P., Brookfield J.F. Evidence for a Wolbachia symbiont in Drosophila melanogaster. Genet. Res. 1993;62(1):23-29. DOI 10.1017/S0016672300031529.

14. Ikeya T., Broughton S., Alic N., Grandison R., Partridge L. The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proc. R. Soc. B. 2009;276(1674):3799-3807. DOI 10.1098/rspb.2009.0778.

15. Ilinsky Y.Y., Zakharov I.K. The endosymbiont Wolbachia in Eurasian populations of Drosophila melanogaster. Russ. J. Genet. 2007; 43(7):748-756. DOI 10.1134/S102279540707006X.

16. Jeyaprakash A., Hoy M.A. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76 % of sixty-three arthropod species. Insect. Mol. Biol. 2000;9(4):393-405. DOI 10.1046/j.13652583.2000.00203.x.

17. Lindsey A.R.I., Bhattacharya T., Newton I.L.G., Hardy R.W. Conflict in the intracellular lives of endosymbionts and viruses: A mechanistic look at Wolbachia-mediated pathogen-blocking. Viruses. 2018; 10(4):141. DOI 10.3390/v10040141.

18. Maistrenko O.M., Serga S.V., Vaiserman A.M., Kozeretska I.A. Effect of Wolbachia Infection on Aging and Longevity-Associated Genes in Drosophila. In: Vaiserman A.M., Moskalev A.A., Pasyukova E.G. (Eds.) Life Extension: Lessons from Drosophila. Vol. 3. Healthy Ageing and Longevity. Springer Int. Publ., 2015.

19. Markov A.V., Lazebny O.E., Goryacheva I.I., Antipin M.I., Kulikov A.M. Symbiotic bacteria affect mating choice in Drosophila melanogaster. Anim. Behav. 2009;77(5):1011-1017. DOI 10.1016/j. anbehav.2009.01.011.

20. Martinez J., Ok S., Smith S., Snoeck K., Day J.P., Jiggins F.M. Should symbionts be nice or selfish? Antiviral effects of Wolbachia are costly but reproductive parasitism is not. PLoS Pathog. 2015;11(7): e1005021. DOI 10.1371/journal.ppat.1005021.

21. Min K.T., Benzer S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl. Acad. Sci. USA. 1997;94(20):10792-10796. DOI 10.1073/pnas.94.20.10792.

22. Olsen K., Reynolds K.T., Hoffmann A.A. A field cage test of the effects of the endosymbiont Wolbachia on Drosophila melanogaster. Heredity. 2001;86(6):731-737. DOI 10.1046/j.1365-2540.2001.t011-00892.

23. Richardson M.F., Weinert L.A., Welch J.J., Linheiro R.S., Magwire M.M., Jiggins F.M., Bergman C.M. Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLoS Genet. 2012;8(12):e1003129. DOI 10.1371/journal.pgen.1003129.

24. Riegler M., Sidhu M., Miller W.J., O’Neill S.L. Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr. Biol. 2005;15(15):1428-1433. DOI 10.1016/j.cub.2005.06.069.

25. Rohrscheib C.E., Bondy E., Josh P., Riegler M., Eyles D., van Swinderen B., Weible II M.W., Brownlie J.C. Wolbachia influences the production of octopamine and affects Drosophila male aggression. Appl. Environ. Microbiol. 2015;81(14):4573-4580. DOI 10.1128/AEM.00573-15.

26. Rohrscheib C.E., Frentiu F.D., Horn E., Ritchie F.K., van Swinderen B., Weible M.W., Brownlie J.C. Intensity of mutualism break¬down is determined by temperature not amplification of Wolbachia genes. PLOS Pathog. 2016;12(9):e1005888. DOI 10.1371/journal.ppat.1005888.

27. Roshina N.V., Symonenko A.V., Krementsova A.V., Trostnikov M.V., Pasyukova E.G. Embryonic expression of shuttle craft, a Drosophila gene involved in neuron development, is associated with adult lifespan. Aging (Albany NY). 2014;6(12):1076-1093. DOI 10.18632/aging.100712.

28. Serga S., Maistrenko O., Rozhok A., Mousseau T., Kozeretska I. Fecundity as one of possible factors contributing to the dominance of the wMel genotype of Wolbachia in natural populations of Drosophila melanogaster. Symbiosis. 2014;63(1):11-17. DOI 10.1007/s13199014-0283-1.

29. Sharon G., Segal D., Ringo J.M., Hefetz A., Zilber-Rosenberg I., Rosenberg E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 2010; 107(46):20051-20056. DOI 10.1073/pnas.1009906107.

30. Solignac M., Vautrin D., Rousset F. Widespread occurrence of the proteobacteria Wolbachia and partial cytoplasmic incompatibility in Drosophila melanogaster. C. R. Acad. Sci. III. 1994;317:461-470.

31. Teixeira L., Ferreira Á., Ashburner M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 2008;6(12):e1000002. DOI 10.1371/journal.pbio.1000002.

32. Toivenen J.M., Walker G.A., Martinez-Diaz P., Bjedov I., Driege Y., Jacobs H.T., Gems D., Partridge L. No influence of Indy on lifespan in Drosophila after correction for genetic and cytoplasmic back-ground effects. PLoS Genet. 2007;3(16):e95. DOI 10.1371/journal.pgen.0030095.

33. Ventura I.M., Martins A.B., Lyra M.L., Andrade C.A., Carvalho K.A., Klaczko L.B. Spiroplasma in Drosophila melanogaster popula¬tions: prevalence, male-killing, molecular identification, and no as-sociation with Wolbachia. Microb. Ecol. 2012;64(3):794-801. DOI 10.1007/s00248-012-0054-6.

34. Versace E., Nolte V., Pandey R.V., Tobler R., Schlötterer C. Experimental evolution reveals habitat-specific fitness dynamics among Wolbachia clades in Drosophila melanogaster. Mol. Ecol. 2014;23(4):802-814. DOI 10.1111/mec.12643.

35. Verspoor R.L., Haddrill P.R. Genetic diversity, population structure and Wolbachia infection status in a worldwide sample of Drosophila melanogaster and D. simulans populations. PLoS One. 2011;6:e26318. DOI 10.1371/journal.pone.0026318.

36. Werren J.H., Baldo L., Clark M.E. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 2008;6:741-751. DOI 10.1038/nrmicro1969.

37. Werren J.H., Guo L., Windsor D.W. Distribution of Wolbachia among neotropical arthropods. Proc. R. Soc. B. 1995;262:197-204. DOI 10.1098/rspb.1995.0196.

38. Werren J.H., Windsor D.M. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc. R. Soc. B. 2000;267:1277-1285. DOI 10.1098/rspb.2000.1139.

39. Wilmoth J.R., Horiuchi S. Rectangularization revisited: variability of age at death within human populations. Demography. 1999;36:475-495. DOI 10.2307/2648085.

40. Zug R., Hammerstein P. Still a host of hosts for Wolbachia: Analysis of recent data suggests that 40 % of terrestrial arthropod species are infected. PLoS One. 2012;7(6):e38544. DOI 10.1371/journal.pone. 0038544.