Skip to main content
NCBI home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1998 Jun 22;265(1401):1075–1080. doi: 10.1098/rspb.1998.0401

Wolbachia-induced thelytoky in the rose gallwasp Diplolepis spinosissimae (Giraud) (Hymenoptera: Cynipidae), and its consequences on the genetic structure of its host

O Plantard, J-Y Rasplus, G Mondor, I Le Clainche, M Solignac
PMCID: PMC1689174

Abstract

Cynipids are known to use various reproductive modes (arrhenotoky, thelytoky and strict cyclical parthenogenesis), but the mechanism remains unknown. We have studied the reproductive system of a rose gallwasp, Diplolepis spinosissimae, which was found to exhibit two different reproductive systems according to the population. In eight out of the ten populations studied, all along the Atlantic coast, D. spinosissimae is thelytokous. Males are extremely rare, and all females are homozygous at three microsatellite loci. 'Obligate homozygous parthenogenesis' was found to be strictly associated with the presence of the endosymbiotic bacterium Wolbachia sp. In the two remaining populations, deprived of Wolbachia, D. spinosissimae reproduced by arrhenotoky as indicated by the larger frequency of males and heterozygosity of females. Allelic diversity, although not zero, was highly reduced in the coastal populations, as a consequence of thelytoky and gamete duplication. We hypothesize that mating of uninfected males with infected females during the first generations after an infection event could explain the small but significant amount of polymorphism observed in those populations. The high level of differentiation indicates a low gene flow, even between geographically close coastal populations.

Full Text

The Full Text of this article is available as a PDF (157.0 KB).

Selected References

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

  1. Barr A. R. Cytoplasmic incompatibility in natural populations of a mosquito, Culex pipiens L. Nature. 1980 Jan 3;283(5742):71–72. doi: 10.1038/283071a0. [DOI] [PubMed] [Google Scholar]
  2. Fine P. E. On the dynamics of symbiote-dependent cytoplasmic incompatibility in culicine mosquitoes. J Invertebr Pathol. 1978 Jan;31(1):10–18. doi: 10.1016/0022-2011(78)90102-7. [DOI] [PubMed] [Google Scholar]
  3. Hoffmann A. A., Turelli M. Unidirectional incompatibility in Drosophila simulans: inheritance, geographic variation and fitness effects. Genetics. 1988 Jun;119(2):435–444. doi: 10.1093/genetics/119.2.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Kocher T. D., Thomas W. K., Meyer A., Edwards S. V., Päbo S., Villablanca F. X., Wilson A. C. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6196–6200. doi: 10.1073/pnas.86.16.6196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. O'Neill S. L., Giordano R., Colbert A. M., Karr T. L., Robertson H. M. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2699–2702. doi: 10.1073/pnas.89.7.2699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Rousset F., Bouchon D., Pintureau B., Juchault P., Solignac M. Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc Biol Sci. 1992 Nov 23;250(1328):91–98. doi: 10.1098/rspb.1992.0135. [DOI] [PubMed] [Google Scholar]
  7. Rousset F., Solignac M. Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6389–6393. doi: 10.1073/pnas.92.14.6389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Rousset F., Vautrin D., Solignac M. Molecular identification of Wolbachia, the agent of cytoplasmic incompatibility in Drosophila simulans, and variability in relation with host mitochondrial types. Proc Biol Sci. 1992 Mar 23;247(1320):163–168. doi: 10.1098/rspb.1992.0023. [DOI] [PubMed] [Google Scholar]
  9. Rousset F., de Stordeur E. Properties of Drosophila simulans strains experimentally infected by different clones of the bacterium Wolbachia. Heredity (Edinb) 1994 Apr;72(Pt 4):325–331. doi: 10.1038/hdy.1994.48. [DOI] [PubMed] [Google Scholar]
  10. Schilthuizen M., Stouthamer R. Horizontal transmission of parthenogenesis-inducing microbes in Trichogramma wasps. Proc Biol Sci. 1997 Mar 22;264(1380):361–366. doi: 10.1098/rspb.1997.0052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Stevens L. Environmental factors affecting reproductive incompatibility in flour beetles, genus Tribolium. J Invertebr Pathol. 1989 Jan;53(1):78–84. doi: 10.1016/0022-2011(89)90076-1. [DOI] [PubMed] [Google Scholar]
  12. Stouthamer R., Breeuwert J. A., Luck R. F., Werren J. H. Molecular identification of microorganisms associated with parthenogenesis. Nature. 1993 Jan 7;361(6407):66–68. doi: 10.1038/361066a0. [DOI] [PubMed] [Google Scholar]
  13. Stouthamer R., Luck R. F., Hamilton W. D. Antibiotics cause parthenogenetic Trichogramma (Hymenoptera/Trichogrammatidae) to revert to sex. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2424–2427. doi: 10.1073/pnas.87.7.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Subbarao S. K., Krishnamurthy B. S., Curtis C. F., Adak T., Chandrahas R. K. Segregation of cytoplasmic incompatibility properties in Culex pipiens fatigans. Genetics. 1977 Oct;87(2):381–390. doi: 10.1093/genetics/87.2.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Werren J. H., Zhang W., Guo L. R. Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc Biol Sci. 1995 Jul 22;261(1360):55–63. doi: 10.1098/rspb.1995.0117. [DOI] [PubMed] [Google Scholar]
  17. Zchori-Fein E., Faktor O., Zeidan M., Gottlieb Y., Czosnek H., Rosen D. Parthenogenesis-inducing microorganisms in Aphytis (Hymenoptera: Aphelinidae). Insect Mol Biol. 1995 Aug;4(3):173–178. doi: 10.1111/j.1365-2583.1995.tb00023.x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES