Manipulation of oviposition choice of the parasitoid wasp, Encarsia pergandiella, by the endosymbiotic bacterium Cardinium

Journal of Evolutionary Biology

Volumn 20, Issue 2, 2007, Pages 707-716

  Kenyon, Sarah G ^a,c   Hunter, M S ^b  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

Arrhenotoky; Autoparasitism; Behaviour; Haplodiploid; Hymenoptera; Parthenogenesis; Superparasitism; Symbiont; Thelytoky; Wolbachia

Indexed keywords

ANTIINFECTIVE AGENT; RIFAMPICIN;

BACTERIUM; ENDOSYMBIONT; HOST-PARASITE INTERACTION; OVIPOSITION; PARASITOID; PARTHENOGENESIS; REPRODUCTIVE BEHAVIOR; SUPERPARASITISM; SYMBIONT; THELYTOKY; WASP;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BACTEROIDETES; DRUG EFFECT; EGG LAYING; FEMALE; HEMIPTERA; HISTOLOGY; MALE; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; WASP;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTEROIDETES; BEHAVIOR, ANIMAL; FEMALE; HEMIPTERA; MALE; OVIPOSITION; RIFAMPIN; WASPS;

ALEYRODIDAE; BACTERIA (MICROORGANISMS); CANDIDATUS CARDINIUM; ENCARSIA PERGANDIELLA; HYMENOPTERA; WOLBACHIA;

EID: 33847065565     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2006.01238.x     Document Type: Article

References (45)

1. Arakaki, N., Noda, H. & Yamagishi, K. 2000. Wolbachia-induced parthenogenesis in the egg parasitoid Telenomus nawai. Entomol. Exp. Appl. 96: 177-184.
2. Ardeh, M.J., de Jong, P.W. & van Lenteren, J.C. 2005. Intra- and interspecific host discrimination in arrhenotokous and thelytokous Eretmocerus spp. Biol. Control 33: 74-80.
3. Bandi, C., Dunn, A.M., Hurst, D.D.H. & Rigaud, T. 2001. Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends Parasitol. 17: 88-94.
4. Bográn, C.E. & Heinz, K.M. 2002. Host selection by the heteronomous hyperparasitoid Encarsia pergandiella: multiple-choice tests using Benisia argentifolii as a primary host. Entomol. Exp. Appl. 103: 11-21.
5. Bull, J.J. 1983. Evolution of Sex Determining Mechanisms. The Benjamin Cummins Pub. Co., London.
6. DeBarro, P.J. & Hart, P.J. 2001. Antibiotic curing of parthenogenesis in Eretmocerus mundus (Australian parthenogenetic form). Entomol. Exp. Appl. 99: 225-230.
7. Gerling, D. 1966. Studies with whitefly parasites of Southern California. I. Encarsia pergandiella Howard (Hymenoptera: Aphelinidae). Can. Entomol. 98: 707-724.
8. Giorgini, M. 2001. Induction of males in thelytokous populations of Encarsia meritoria and Encarsia protransvena: a systematic tool. BioControl. 46: 427-438.
9. Gottlieb, Y. & Zchori-Fein, E. 2001. Irreversible thelytokous reproduction in Muscidifurax uniraptor. Entomol. Exp. Appl. 100: 271-278.
10. Gottlieb, Y., Zachori-Fein, E., Werren, J.H. & Karr, T.L. 2002. Diploidy restoration in Wolbachia-infected Muscidifurax uniraptor (Hymenoptera: Pteromalidae). J. Invertebr. Pathol. 81: 166-174.
11. Hunter, M.S. 1989. Sex allocation and egg distribution of an autoparasitoid, Encarsia pergandiella, (Hymenoptera: Aphelinidae). Ecol. Entomol. 14: 57-67.
12. Hunter, M.S. 1999. The influence of parthenogenesis-inducing Wolbachia on the oviposition behaviour and sex-specific developmental requirements of autoparasitoid wasps. J. Evol. Biol. 12: 735-741.
13. Hunter, M.S. & Godfray, H.C.J. 1995. Ecological determinants of sex allocation in an autoparasitoid wasp. J. Anim. Ecol. 64: 95-106.
14. Hunter, M.S. & Kelly, S.E. 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.
15. Hunter, M.S. & Woolley, J.B. 2001. Evolution and behavioral ecology of heteronomous Aphelinid parasitoids. Annu. Rev. Entomol. 46: 251-290.
16. Hunter, M.S. & Zchori-Fein, E. 2006. Inherited Bacteroidetes symbionts in arthropods. In: Insect Symbiosis, Vol. 2 (K. Bourtzis & T.A. Miller, eds), pp. 39-56. CRC Press, Boca Raton, FL.
17. Hunter, M.S., Nur, U. & Werren, J.H. 1993. Origin of males by genome loss in an autoparasitoid wasp. Heredity 70: 162-171.
18. Hunter, M.S., Perlman, S.J. & Kelly, S.E. 2003. A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc. R. Soc. Lond. B Biol. Sci. 270: 2185-2190.
19. Jeyaprakash, A. & Hoy, M.A. 2000. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol. Biol. 9: 393-405.
20. Kajita, H. 1993. Induction of males in the thelytokous wasp Encarsia formosa (Gahan) (Hymenoptera: Aphelinidae). Appl. Entomol. Zool. 28: 115-117.
21. Moore, J. 2002. Parasites and Behavior of Animals. Oxford University Press, Oxford.
22. O'Neill, S.L., Hoffmann, A.A. & Werren, J.H. eds. 1997. Influential Passengers. Oxford University Press, Oxford.
23. Pannebakker, B.A., Pijnacker, L.P., Zwaan, B.J. & Beukeboom, L.W. 2004. Cytology of Wolbachia-induced parthenogenesis in Leptopilina clavipes (Hymenoptera: Figitidae). Genome 47: 299-303.
24. Pannebakker, B.A., Schidlo, N.S., Boskamp, G.J.F., Dekker, L., van Dooren, T.J.M., Beukeboom, L.W., Zwaan, B.J., Brakefield, P.M. & van Alphen, J.J.M. 2005. Sexual functionality of Leptopilina clavipes (Hymenoptera: Figitidae) after reversing Wolbachia-induced parthenogenesis. J. Evol. Biol. 18: 1019-1028.
25. Pedata, P.A., Giorgini, M. & Guerrieri, E. 2002. Interspecific host discrimination and within-host competition between Encarsia formosa and E. pergandiella (Hymenoptera: Aphelinidae), two endoparasitoids of whiteflies (Hemiptera: Aleyrodidae). Bull. Entomol. Res. 92: 521-528.
26. Pijls, J.W.A.M., van Steenbergen, H.J. & van Alphen, J.J.M. 1996. Asexuality cured: the relations and differences between sexual and asexual Apoanagyrus diversicornis. Heredity 76: 506-513.
27. Provencher, L.M., Morse, G.E., Weeks, A.R. & Normark, B.B. 2005. Parthenogenesis in the Aspidiotus nerii complex (Hemiptera: Diaspididae): a single origin of a worldwide polyphagous lineage associated with Cardinium bacteria. Ann. Entomol. Soc. Am. 98: 629-635.
28. Russell, J.A. & Moran, N.A. 2006. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc. R. Soc. Lond. B Biol. Sci. 273: 603-610.
29. Stouthamer, R. & Kazmer, D.J. 1994. Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 73: 317-327.
30. Stouthamer, R. & Mak, F. 2002. Influence of antibiotics on the offspring production of the Wolbachia-infected parthenogenetic parasitoid Encarsia formosa. J. Invertebr. Pathol. 80: 41-45.
31. Stouthamer, R., Luck, R.F. & Hamilton, W.D. 1990. Antibiotics cause parthenogenetic Trichogramma (Hymenoptera: Trichogrammatidae) to revert to sex. Proc. Natl Acad. Sci. USA 87: 2424-2427.
32. Stouthamer, R., Breeuwer, J.A.J. & Hurst, G.D.D. 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53: 71-102.
33. Varaldi, J., Boulétreau, M. & Fleury, F. 2005. Cost induced by viral particles manipulating superparasitism behaviour in the parasitoid Leptopilina boulardi. Parasitology 131: 161-168.
34. Walter, G.H. 1983. Differences in host relationships between male and female heteronomous parasitoids (Aphelinidae: Chalcidoidea): a review of host location, oviposition and pre-imaginal physiology and morphology. J. Entomol. Soc. S. Af. 46: 261-282.
35. Weeks, A.R. & Breeuwer, J.A.J. 2003. A new bacterium from the Cytophaga-Flavobacterium-Bacteroides phylum that causes sex-ratio distortion. In: Insect Symbiosis (K. Bourtzis & T.A. Miller, eds), pp. 165-176. CRC Press, New York.
36. Weeks, A.R. & Stouthamer, R. 2003. Increased fecundity associated with infection by a Cytophaga-like intracellular bacterium in the predatory mite, Metaseiulus occidentalis. Proc. R. Soc. Lond. B. (Suppl.)271: S193-S195.
37. Weeks, A.R., Marec, F. & Breeuwer, J.A.J. 2001. A mite species that consists entirely of haploid females. Science 292: 2479-2482.
38. Weeks, A.R., Velten, R. & Stouthamer, R. 2003. Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc. R. Soc. Lond. B Biol. Sci. 270: 1857-1865.
39. Werren, J.H. 1997. Biology of Wolbachia. Annu. Rev. Entomol. 42: 587-609.
40. Werren, J.H., Windsor, D. & Guo, L.R. 1995. Distribution of Wolbachia among Neotropical Arthropods. Proc. R. Soc. Lond. B Biol. Sci. 262: 197-204.
41. Zchori-Fein, E. & Perlman, S.J. 2004. Distribution of the bacterial symbiont Cardinium in arthropods. Mol. Ecol. 13: 2009-2016.
42. Zchori-Fein, E., Roush, R.T. & Hunter, M.S. 1992. Male production induced by antibiotic treatment in Encarsia formosa (Hymenoptera: Aphelinidae) and asexual species. Experientia 48: 102-105.
43. Zchori-Fein, E., Faktor, O., Zeidan, M., Gottlieb, Y., Czosnek, H. & Rosen, D. 1995. Parthenogenesis-inducing microorganisms in Aphitis (Hymenoptera: Aphelinidae). Insect Mol. Biol. 4: 173-178.
44. Zchori-Fein, E., Gottlieb, Y., Kelly, S.E., Brown, J.K., Wilson, J.M., Karr, T.L. & Hunter, M.S. 2001. A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proc. Natl Acad. Sci. U S A 98: 12555-12560.
45. Zchori-Fein, E., Perlman, S.J., Kelly, S.E., Katzir, N. & Hunter, M.S. 2004. Characterization of a 'Bacteroidetes' symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of 'Candidatus Cardinium hertigii'. Int. J. Syst. Evol. Microbiol. 54: 961-968.