Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2002 Mar 22;269(1491):623–629. doi: 10.1098/rspb.2001.1927

Deleterious Wolbachia in the ant Formica truncorum.

T Wenseleers 1, L Sundström 1, J Billen 1
PMCID: PMC1690935  PMID: 11916479

Abstract

Wolbachia is a maternally inherited bacterium that may manipulate the reproduction of its arthropod hosts. In insects, it is known to lead to inviable matings, cause asexual reproduction or kill male offspring, all to its own benefit, but to the detriment of its host. In social Hymenoptera, Wolbachia occurs widely, but little is known about its fitness effects. We report on a Wolbachia infection in the wood ant Formica truncorum, and evaluate whether it influences reproductive patterns. All 33 colonies of the study population were infected, suggesting that Wolbachia infection is at, or close to, fixation. Interestingly, in colonies with fewer infected workers, significantly more sexuals are produced, indicating that Wolbachia has deleterious effects in this species. In addition, adult workers are shown to have significantly lower infection rates (45%) than worker pupae (87%) or virgin queens (94%), suggesting that workers lose their infection over life. Clearance of Wolbachia infection has, to our knowledge, never been shown in any other natural system, but we argue that it may, in this case, represent an adaptive strategy to reduce colony load. The cause of fixation requires further study, but our data strongly suggest that Wolbachia has no influence on the sex ratio in this species.

Full Text

The Full Text of this article is available as a PDF (119.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Braig H. R., Zhou W., Dobson S. L., O'Neill S. L. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol. 1998 May;180(9):2373–2378. doi: 10.1128/jb.180.9.2373-2378.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Breeuwer J. A., Werren J. H. Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics. 1993 Oct;135(2):565–574. doi: 10.1093/genetics/135.2.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chapuis M, Keller L. Testing kin selection with sex allocation data in eusocial hymenoptera . Heredity (Edinb) 1999 May;82(Pt 5):473–478. doi: 10.1038/sj.hdy.6885340. [DOI] [PubMed] [Google Scholar]
  4. Cheng Q., Ruel T. D., Zhou W., Moloo S. K., Majiwa P., O'Neill S. L., Aksoy S. Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp. Med Vet Entomol. 2000 Mar;14(1):44–50. doi: 10.1046/j.1365-2915.2000.00202.x. [DOI] [PubMed] [Google Scholar]
  5. 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 Biol. 1999 Feb;29(2):153–160. doi: 10.1016/s0965-1748(98)00119-2. [DOI] [PubMed] [Google Scholar]
  6. Fialho R. F., Stevens L. Male-killing Wolbachia in a flour beetle. Proc Biol Sci. 2000 Jul 22;267(1451):1469–1473. doi: 10.1098/rspb.2000.1166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fleury F., Vavre F., Ris N., Fouillet P., Boulétreau M. Physiological cost induced by the maternally-transmitted endosymbiont Wolbachia in the Drosophila parasitoid Leptopilina heterotoma. Parasitology. 2000 Nov;121(Pt 5):493–500. doi: 10.1017/s0031182099006599. [DOI] [PubMed] [Google Scholar]
  8. Hoffmann A. A., Turelli M., Harshman L. G. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics. 1990 Dec;126(4):933–948. doi: 10.1093/genetics/126.4.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hurst G. D., Johnson A. P., Schulenburg J. H., Fuyama Y. Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics. 2000 Oct;156(2):699–709. doi: 10.1093/genetics/156.2.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hurst L. D., Atlan A., Bengtsson B. O. Genetic conflicts. Q Rev Biol. 1996 Sep;71(3):317–364. doi: 10.1086/419442. [DOI] [PubMed] [Google Scholar]
  11. 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 Aug;9(4):393–405. doi: 10.1046/j.1365-2583.2000.00203.x. [DOI] [PubMed] [Google Scholar]
  12. Jiggins F. M., Bentley J. K., Majerus M. E., Hurst G. D. How many species are infected with Wolbachia? Cryptic sex ratio distorters revealed to be common by intensive sampling. Proc Biol Sci. 2001 Jun 7;268(1472):1123–1126. doi: 10.1098/rspb.2001.1632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lang B. F., Gray M. W., Burger G. Mitochondrial genome evolution and the origin of eukaryotes. Annu Rev Genet. 1999;33:351–397. doi: 10.1146/annurev.genet.33.1.351. [DOI] [PubMed] [Google Scholar]
  14. Müller M., Martin W. The genome of Rickettsia prowazekii and some thoughts on the origin of mitochondria and hydrogenosomes. Bioessays. 1999 May;21(5):377–381. doi: 10.1002/(SICI)1521-1878(199905)21:5<377::AID-BIES4>3.0.CO;2-W. [DOI] [PubMed] [Google Scholar]
  15. doi: 10.1098/rspb.1997.0173. [DOI] [PMC free article] [Google Scholar]
  16. doi: 10.1098/rspb.1999.0698. [DOI] [PMC free article] [Google Scholar]
  17. Perrot-Minnot M. J., Guo L. R., Werren J. H. Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis: effects on compatibility. Genetics. 1996 Jun;143(2):961–972. doi: 10.1093/genetics/143.2.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Reed K. M., Werren J. H. Induction of paternal genome loss by the paternal-sex-ratio chromosome and cytoplasmic incompatibility bacteria (Wolbachia): a comparative study of early embryonic events. Mol Reprod Dev. 1995 Apr;40(4):408–418. doi: 10.1002/mrd.1080400404. [DOI] [PubMed] [Google Scholar]
  19. Sicheritz-Pontén T., Kurland C. G., Andersson S. G. A phylogenetic analysis of the cytochrome b and cytochrome c oxidase I genes supports an origin of mitochondria from within the Rickettsiaceae. Biochim Biophys Acta. 1998 Jul 20;1365(3):545–551. doi: 10.1016/s0005-2728(98)00099-1. [DOI] [PubMed] [Google Scholar]
  20. Stouthamer R., Breeuwer J. A., Hurst G. D. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol. 1999;53:71–102. doi: 10.1146/annurev.micro.53.1.71. [DOI] [PubMed] [Google Scholar]
  21. Sundstrom L, Chapuisat M, Keller L. Conditional Manipulation of Sex Ratios by Ant Workers: A Test of Kin Selection Theory. Science. 1996 Nov 8;274(5289):993–995. doi: 10.1126/science.274.5289.993. [DOI] [PubMed] [Google Scholar]
  22. Sundström L., Boomsma J. J. Reproductive alliances and posthumous fitness enhancement in male ants. Proc Biol Sci. 2000 Jul 22;267(1451):1439–1444. doi: 10.1098/rspb.2000.1161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Trivers R. L., Hare H. Haploidploidy and the evolution of the social insect. Science. 1976 Jan 23;191(4224):249–263. doi: 10.1126/science.1108197. [DOI] [PubMed] [Google Scholar]
  24. Van Meer M. M., Witteveldt J., Stouthamer R. Phylogeny of the arthropod endosymbiont Wolbachia based on the wsp gene. Insect Mol Biol. 1999 Aug;8(3):399–408. doi: 10.1046/j.1365-2583.1999.83129.x. [DOI] [PubMed] [Google Scholar]
  25. Vandekerckhove T. T., Watteyne S., Willems A., Swings J. G., Mertens J., Gillis M. Phylogenetic analysis of the 16S rDNA of the cytoplasmic bacterium Wolbachia from the novel host Folsomia candida (Hexapoda, Collembola) and its implications for wolbachial taxonomy. FEMS Microbiol Lett. 1999 Nov 15;180(2):279–286. doi: 10.1111/j.1574-6968.1999.tb08807.x. [DOI] [PubMed] [Google Scholar]
  26. Vavre F., Fleury F., Varaldi J., Fouillet P., Boulétreau M. Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences. Evolution. 2000 Feb;54(1):191–200. doi: 10.1111/j.0014-3820.2000.tb00019.x. [DOI] [PubMed] [Google Scholar]
  27. Wenseleers T., Ito F., Van Borm S., Huybrechts R., Volckaert F., Billen J. Widespread occurrence of the micro-organism Wolbachia in ants. Proc Biol Sci. 1998 Aug 7;265(1404):1447–1452. doi: 10.1098/rspb.1998.0456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Werren J. H. Biology of Wolbachia. Annu Rev Entomol. 1997;42:587–609. doi: 10.1146/annurev.ento.42.1.587. [DOI] [PubMed] [Google Scholar]
  29. Zhou W., Rousset F., O'Neil S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci. 1998 Mar 22;265(1395):509–515. doi: 10.1098/rspb.1998.0324. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES