Skip to main content
Log in

Factors Affecting the Strength of Cardinium-Induced Cytoplasmic Incompatibility in the Parasitic Wasp Encarsia pergandiella (Hymenoptera: Aphelinidae)

  • Invertebrate Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Bacteria that cause cytoplasmic incompatibility (CI) are among the most common maternally transmitted parasites of insects. In CI, uninfected females produce few or no offspring when they mate with infected males and, as a result, are often at a reproductive disadvantage relative to infected females. Two different bacteria are known to cause CI, Wolbachia and Cardinium. CI Cardinium was discovered more recently and has been little studied. Here, factors that could influence the reduction in reproductive output in a CI cross, or CI “strength,” were explored in the parasitic wasp Encarsia pergandiella. Cardinium in this wasp exhibits variable CI strength. Experiments tested the effect of male age, male size, male host species, Cardinium density, and male development time on CI strength. We found a striking effect of male development time, with males that took longer to develop exhibiting stronger CI when mated to uninfected females. Male age had little effect; although in one experiment, the oldest males exhibited stronger CI. Male size, host species, and bacterial density had no effect on the strength of CI. Identifying the factors that control CI are crucial for understanding the dynamics of infection, as well as the success of strategies that aim to use CI microbes to control insect pests and disease vectors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Atyame CM, Pasteur N, Dumas E, Tortosa P, Tantely ML, Pocquet N, Licciardi S, Bheecarry A, Zumbo B, Weill M, Duron O (2011) Cytoplasmic incompatibility as a means of controlling Culex pipiens quinquefasciatus mosquito in the islands of the South-Western Indian Ocean. PLOS Negl Trop Dis 5:e1440

    Article  PubMed Central  PubMed  Google Scholar 

  2. Avilla J, Copland MJW (1987) Effects of host stage on the development of the facultative autoparasitoid Encarsia tricolor (Hymenoptera, Aphelinidae). Ann Appl Biol 110:381–9

    Article  Google Scholar 

  3. Avilla J, Copland MJW (1988) Development rate, number of mature oocytes at emergence and adult size of Encarsia tricolor at constant and variable temperatures. Entomophaga 33:289–298

    Article  Google Scholar 

  4. Boivin G, Jacob S, Damiens D (2005) Spermatogeny as a life-history index in parasitoid wasps. Oecologia 143:198–202

    Article  PubMed  Google Scholar 

  5. Bordenstein SR, Uy JJ, Werren JH (2003) Host genotype determines cytoplasmic incompatibility type in the haplodiploid genus Nasonia. Genetics 164:223–233

    PubMed Central  CAS  PubMed  Google Scholar 

  6. Bourtzis K, Nirgianaki A, Markakis G, Savakis C (1996) Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144:1063–1073

    PubMed Central  CAS  PubMed  Google Scholar 

  7. Bressac C, Rousset F (1992) The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J Invert Pathol 61:226–230

    Article  Google Scholar 

  8. Chang J, Masters A, Avery A, Werren JH (2010) A divergent Cardinium found in daddy long-legs (Arachnida: Opiliones). J Invert Pathol 105:220–227

    Article  CAS  Google Scholar 

  9. Caspari E, Watson GS (1959) On the evolutionary importance of cytoplasmic sterility in mosquitoes. Evolution 13:568–570

    Article  Google Scholar 

  10. Clancy DJ, Hoffmann AA (1998) Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans. Entomol Exp Appl 86:13–24

    Article  Google Scholar 

  11. Clark ME, Veneti Z, Bourtzis K, Karr TL (2002) The distribution and proliferation of the intracellular bacteria Wolbachia during spermatogenesis in Drosophila. Mech Dev 111:3–15

    Article  CAS  PubMed  Google Scholar 

  12. Clark ME, Veneti Z, Bourtzis K, Karr TL (2003) Wolbachia distribution and cytoplasmic incompatibility during sperm development: the cyst as the basic cellular unit of CI expression. Mech Dev 120:185–198

    Article  CAS  PubMed  Google Scholar 

  13. Dallai R, Mercati D, Giusti F, Gottardo M, Carapelli A (2011) A Cardinium-like symbiont in the proturan Acerella muscorum (Hexapoda). Tissue Cell 43:151–156

    Article  CAS  PubMed  Google Scholar 

  14. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou LQ, Engelstadter J, Hurst GDD (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27

    Article  PubMed Central  PubMed  Google Scholar 

  15. Duron O, Hurst GDD, Hornett EA, Josling JA, Engelstadter J (2008) High incidence of the maternally inherited bacterium Cardinium in spiders. Mol Ecol 17:1427–1437

    Article  CAS  PubMed  Google Scholar 

  16. Edlund A, Ek K, Breitholtz M, Gorokhova E (2012) Antibiotic-induced change of bacterial communities associated with the copepod Nitocra spinipes. PLoS ONE 7:e33107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Godfray HCJ (2004) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton

    Google Scholar 

  18. Gould JR, Bellows TS, Paine TR (1995) Preimaginal development, adult longevity and fecundity of Encarsia inaron (Hym: Aphelinidae) parasitizing Siphoninus phillyreae (Hom: Aleyrodidae) in California. Entomophaga 40:55–68

    Article  Google Scholar 

  19. Gotoh T, Noda H, Ito S (2007) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98:13–20

    Article  CAS  PubMed  Google Scholar 

  20. Harris LR, Kelly SE, Hunter MS, Perlman SJ (2010) Population dynamics and rapid spread of Cardinium, a bacterial endosymbiont causing cytoplasmic incompatibility in Encarsia pergandiella (Hymenoptera: Aphelinidae). Heredity 104:239–246

    Article  CAS  PubMed  Google Scholar 

  21. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH et al (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454–457

    Article  CAS  PubMed  Google Scholar 

  22. Hoffmann AA, Turelli M, Harshman LG (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126:933–948

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Hunter MS (1989) Suitability of stages of female Encarsia pergandiella [Hymenoptera, Aphelinidae] for development of conspecific male hyperparasites. Entomophaga 34:265–273

    Article  Google Scholar 

  24. Hunter MS, Kelly SE (1998) Hyperparasitism by an exotic autoparasitoid: secondary host selection and the window of vulnerability of conspecific and native heterospecific hosts. Entomol Exp Appl 89:249–259

    Article  Google Scholar 

  25. Hunter MS, Perlman SJ, Kelly SE (2003) A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc Biol Sci 270:2185–2190

    Article  PubMed Central  PubMed  Google Scholar 

  26. Hunter MS, Woolley JB (2001) Evolution and behavioral ecology of heteronomous aphelinid parasitoids. Ann Rev Ent 46:251–290

    Article  CAS  Google Scholar 

  27. Jamnongluk W, Kittayapong P, Baisley KJ, O’Neill SL (2000) Wolbachia infection and expression of cytoplasmic incompatibility in Armigeres subalbatus (Diptera: Culicidae). J Med Ent 37:53–57

    Article  CAS  Google Scholar 

  28. Kittayapong P, Mongkalangoon P, Baimai V, O’Neill SL (2002) Host age effect and expression of cytoplasmic incompatibility in field populations of Wolbachia superinfected Aedes albopictus. Heredity 88:270–274

    Article  CAS  PubMed  Google Scholar 

  29. Landmann F, Orsi GA, Loppin B, Sullivan W (2009) Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. PLoS Path 5:e1000343

    Article  Google Scholar 

  30. Laven H (1967) Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature 216:383–4

    Article  CAS  PubMed  Google Scholar 

  31. Nakamura Y, Kawai S, Yukuhiro F, Ito S, Gotoh T et al (2009) Prevalence of Cardinium bacteria in planthoppers and spider mites and taxonomic revision of “Candidatus Cardinium hertigii” based on detection of a new Cardinium group from biting midges. Appl Env Microbiol 75:6757–6763

    Article  CAS  Google Scholar 

  32. Nakamura Y, Yukuhiro F, Matsumura M, Noda H (2012) Cytoplasmic incompatibility involving Cardinium and Wolbachia in the white-backed planthopper Sogatella furcifera (Hemiptera: Delphacidae). Appl Ent Zool 47:273–283

    Article  Google Scholar 

  33. Penz T, Schmitz-Esser S, Kelly SE, Cass BN, Müller A, Woyke T, Malfatti SA, Hunter MS, Horn M (2012) Comparative genomics suggests an independent origin of cytoplasmic incompatibility in Cardinium hertigii. PLoS Genet 8:e1003012

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Perlman SJ, Kelly SE, Hunter MS (2008) Population biology of cytoplasmic incompatibility: maintenance and spread of Cardinium symbionts in a parasitic wasp. Genetics 178:1003–1011

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. R Development Core Team (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/

  37. Rasgon JL, Scott TW (2003) Wolbachia and cytoplasmic incompatibility in the California Culex pipiens mosquito species complex: parameter estimates and infection dynamics in natural populations. Genetics 165:2029–2038

    PubMed Central  PubMed  Google Scholar 

  38. Reynolds KT, Hoffmann AA (2002) Male age, host effects and the weak expression or non-expression of cytoplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia. Genet Res 80:79–87

    Article  PubMed  Google Scholar 

  39. Ros VI, Breeuwer JA (2009) The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni. Heredity 102:413–422

    Article  CAS  PubMed  Google Scholar 

  40. Turelli M (1994) Evolution of incompatibility-inducing microbes and their hosts. Evolution 48:1500–1513

    Article  Google Scholar 

  41. Turelli M, Hoffmann AA (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353:440–442

    Article  CAS  PubMed  Google Scholar 

  42. Turelli M, Hoffmann AA (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140:1319–1338

    PubMed Central  CAS  PubMed  Google Scholar 

  43. Veneti Z, Clark ME, Zabalou S, Karr TL, Savakis C, Bourtzis K (2003) Cytoplasmic incompatibility and sperm cyst infection in different Drosophila-Wolbachia associations. Genetics 164:545–552

    PubMed Central  PubMed  Google Scholar 

  44. Weeks AR, Velten R, Stouthamer R (2003) Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc Biol Sci 270:1857–1865

    Article  PubMed Central  PubMed  Google Scholar 

  45. Werren JH (1997) Biology of Wolbachia. Ann Rev Ent 42:587–609

    Article  CAS  Google Scholar 

  46. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751

    Article  CAS  PubMed  Google Scholar 

  47. Williams T (1995) The biology of Encarsia tricolor – an autoparasitid of whitefly. Biol Control 5:209–217

    Article  Google Scholar 

  48. Wu KE, Hoy MA (2012) Cardinium is associated with reproductive incompatibility in the predatory mite Metaseiulus occidentalis (Acari: Phytoseiidae). J Invert Pathol 110:359–365

    Article  Google Scholar 

  49. Xie RR, Zhou LL, Zhao ZJ, Hong XY (2010) Male age influences the strength of Cardinium-induced cytoplasmic incompatibility expression in the carmine spider mite Tetranychus cinnabarinus. Appl Ent Zool 45:417–423

    Article  Google Scholar 

  50. Yamada R, Floate KD, Riegler M, O’Neill SL (2007) Male development time influences the strength of Wolbachia-induced cytoplasmic incompatibility expression in Drosophila melanogaster. Genetics 177:801–808

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  51. Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13:2009–2016

    Article  CAS  PubMed  Google Scholar 

  52. Zhang XF, Zhao DX, Hong XY (2012) Cardinium-the leading factor of cytoplasmic incompatibility in the planthopper Sogatella furcifera doubly infected with Wolbachia and Cardinium. Environ Ent 41:33–840

    Google Scholar 

  53. Zhu LH, Zhang KJ, Zhang YK, Ge Y, Gotoh T et al (2012) Wolbachia strengthens Cardinium-induced cytoplasmic incompatibility in the spider mite Tetranychus piercei McGregor. Curr Microbiol 65:516–523

    Article  CAS  PubMed  Google Scholar 

  54. Zug R, Hammerstein P (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40 % of terrestrial arthropod species are infected. PLoS ONE 7:e38544

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by an NSF DEB grant (DEB-0542961) to MSH and SP, NSF (DEB-1020460) and USDA AFRI grants (2010- 03752) to MSH, an NSERC Canada Graduate Scholarship to LH, and the University of Arizona’s Undergraduate Biology Research program (UBRP), which provided support for NJD. SP is a member of the Integrated Microbial Biodiversity Program of the Canadian Institute for Advanced Research. We thank Finn Hamilton for making Fig. 1.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Steve J. Perlman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Perlman, S.J., Dowdy, N.J., Harris, L.R. et al. Factors Affecting the Strength of Cardinium-Induced Cytoplasmic Incompatibility in the Parasitic Wasp Encarsia pergandiella (Hymenoptera: Aphelinidae). Microb Ecol 67, 671–678 (2014). https://doi.org/10.1007/s00248-013-0359-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0359-0

Keywords

Navigation