Eur. J. Entomol. 110 (1): 103-107, 2013 | 10.14411/eje.2013.014

Occurrence of arrhenotoky and thelytoky in a parasitic wasp Venturia canescens (Hymenoptera: Ichneumonidae): Effect of endosymbionts or existence of two distinct reproductive modes?

Vincent FORAY1,2, Hélène HENRI1, Sonia MARTINEZ1, Patricia GIBERT1, Emmanuel DESOUHANT1
1 Université Lyon 1, Laboratoire de Biométrie et Biologie Evolutive, F-69000 Lyon & CNRS, UMR5558, F-69622 Villeurbanne, France
2 Earth and Life Institute, Biodiversity Research Centre, Catholic University of Louvain, Croix du Sud 4-5, B-1348 Louvain-la-Neuve, Belgium; e-mail: vincent.foray@uclouvain.be

Endosymbiotic organisms are known to manipulate the reproductive biology of their hosts. Incomplete prevalence of endosymbiont inducing thelytokous parthenogenesis results in the coexistence of sexual and asexual individuals, and could account for the maintenance of sexual reproduction in certain populations or species. In the parasitoid Venturia canescens, arrhenotokous ("sexual") and thelytokous ("asexual") individuals occur sympatrically. We aimed to determine whether endosymbionts are implicated in the thelytoky of V. canescens. After screening females of the two reproductive modes for several reproductive parasites: bacteria (Wolbachia, Rickettsia, Bacteroidetes, Spiroplasma, Arsenophonus) and Microsporidia, we concluded that thelytoky in V. canescens is not induced by any of these parasites and confirmed its suitability as a biological model for solving the evolutionary enigma of the maintenance of sexual reproduction.

Keywords: Hymenoptera, Ichneumonidae, Venturia canescens, reproductive parasite, thelytokous parthenogenesis, sex evolution

Received: September 14, 2011; Accepted: June 28, 2012; Published: January 2, 2013

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References

  1. ADACHI-HAGIMORI T., MIURA K. & STOUTHAMER R. 2008: A new cytogenetic mechanism for bacterial endosymbiont-induced parthenogenesis in Hymenoptera. - Proc. R. Soc. Lond. (B) 275: 2667-2673 Go to original source...
  2. AMAT I., CASTELO M., DESOUHANT E. & BERNSTEIN C. 2006: The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species. - Oecologia 148: 153-161 Go to original source...
  3. AMAT I., DESOUHANT E. & BERNSTEIN C. 2009: Differential use of conspecific-derived information by sexual and asexual parasitic wasps exploiting partially depleted host patches. - Behav. Ecol. Sociobiol. 63: 563-572 Go to original source...
  4. BAKER M.D., VOSSBRINCK C.R., DIDIER E.S., MADDOX J.V. & SHADDUCK J.A. 1995: Small-subunit ribosomal DNA phylogeny of various microsporidia with emphasis on aids-related forms. - J. Eukaryot. Microbiol. 42: 564-570 Go to original source...
  5. BALDO L., DUNNING HOTOPP J.C., JOLLEY K.A., BORDENSTEIN S.R., BIBER S.A, CHOUDHURY R.R., HAYASHI C., MAIDEN M.C.J., TETTELIN H. & WERREN J.H. 2006: Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. - Appl. Environ. Microbiol. 72: 7098-7110 Go to original source...
  6. BEUKEBOOM L.W. 2001: Single-locus complementary sex determination in the ichneumonid Venturia canescens (Gravenhorst) (Hymenoptera). - Neth. J. Zool. 51: 1-15 Go to original source...
  7. BEUKEBOOM L.W. & PIJNACKER L. 2000: Automictic parthenogenesis in the parasitoid Venturia canescens (Hymenoptera: Ichneumonidae) revisited. - Genome 43: 939-944 Go to original source...
  8. BOURTZIS K. & MILLER T.A. 2003: Insect Symbiosis. CRC Press, Boca Raton, FL, 347 pp
  9. BRAIG H.R., ZHOU W., DOBSON S.L. & O'NEILL S. 1998: Cloning and characterization of gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. - J. Bacteriol. 180: 2373-2378
  10. COOK J.M. & BUTCHER R.D.J. 1999: The transmission and effects of Wolbachia bacteria in parasitoids. - Res. Popul. Ecol. 41: 15-28 Go to original source...
  11. DUNN A.M. & SMITH J.E. 2001: Microsporidian life cycles and diversity: the relationship between virulence and transmission. - Microbes Infect. 3: 381-388 Go to original source...
  12. DURON O., BOUCHON D., BOUTIN S., BELLAMY L., ZHOU L., ENGELSTADTER J. & HURST G.D. 2008: The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. - BMC Biology 6: 1-24 Go to original source...
  13. ENGELSTADTER J., SANDROCK C. & VORBURGER C. 2011: Contagious parthenogenesis, automixis, and a sex determination meltdown. - Evolution 65: 501-511 Go to original source...
  14. FLEURY F., VAVRE F., RIS N., FOUILLET P. & BOULETREAU M. 2000: Physiological cost induced by the maternallytransmitted endosymbiont Wolbachia in the Drosophila parasitoid Leptopilina heterotoma. - Parasitology 121: 493-500 Go to original source...
  15. FORAY V., GIBERT P. & DESOUHANT E. 2011: Differential thermal performance curves in response to different habitats in the parasitoid Venturia canescens. - Naturwissenschaften 98: 683-691 Go to original source...
  16. GEIGER A., FARDEAU M.L., GREBAUT P., VATUNGA G., JOSENANDO T., HERDER S., CUNY G., TRUC P. & OLLIVIER B. 2009: First isolation of Enterobacter, Enterococcus, and Acinetobacter spp. As inhabitants of tsetse fly (Glossina palpalis palpalis) midgut. - Infect. Genet. Evol. 9: 1364-1370 Go to original source...
  17. GHERNA R.L., WERREN J.H., WEISBURG W., COTE R., WOESE C.R., MANDELCO L. & BRENNER D.J. 1991: Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. - Int. J. Syst. Bacteriol. 41: 563-565 Go to original source...
  18. GOTOH T., NODA H. & ITO S. 2007: Cardinium symbionts cause cytoplasmic incompatibility in spider mites. - Heredity 98: 13-20 Go to original source...
  19. GOTTLIEB Y., GHANIM M., CHIEL E., GERLING D., PORTNOY V., STEINBERG S., TZURI G., HOROWITZ A.R., BELAUSOV E., MOZESDAUBE N., KONTSEDALOV S., GERSHON M., GAL S., KATZIR N. & ZCHORI-FEIN E. 2006: Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). - Appl. Environ. Microbiol. 72: 3646-3652 Go to original source...
  20. HAGIMORI T., ABE Y., DATE S. & MIURA K. 2006: The first finding of a Rickettsia bacterium associated with parthenogenesis induction among insects. - Curr. Microbiol. 52: 97-101 Go to original source...
  21. HOGG J.C., IRONSIDE J.E., SHARPE R.G., HATCHER M.J., SMITH J.E. & DUNN A.M. 2002: Infection of Gammarus duebeni populations by two vertically transmitted microsporidia; parasite detection and discrimination by PCR-RFLP. - Parasitology 125: 59-63 Go to original source...
  22. HURST G.D.D., SCHULENBURG H.G., MAJERUS T.M.O., BERTRAND D., ZAKHAROV I.A., BAUNGAARD J., VOLKL W., STOUTHAMER R. & MAJERUS M.E. 1999: Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. - Insect Mol. Biol. 8: 133-139 Go to original source...
  23. MATEO LEACH I., HESSELINGT A., HUIBERS W.H.C., WITSENBOER H., BEUKEBOOM L.W. & VAN DE ZANDE L. 2009: Transcriptome and proteome analysis of ovaries of arrhenotokous and thelytokous Venturia canescens. - Insect Mol. Biol. 18: 477-482 Go to original source...
  24. MATEO LEACH I., FERBER S., VAN DE ZANDE L. & BEUKEBOOM L. 2012: Genetic variability of arrhenotokous and thelytokous Venturia canescens (Hymenoptera). - Genetica 140: 53-63 Go to original source...
  25. MAYNARD-SMITH J. 1978: The Evolution of Sex. Cambridge University Press, Cambridge, 236 pp
  26. O'NEILL S.L., GIORDANO R., COLBERT A.M., KARR T.L. & ROBERTSON H.M. 1992: 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. PNAS 89: 2699-2702 Go to original source...
  27. OTTO S.P. 2009: The evolutionary enigma of sex. - Am. Nat. 174: S1-S14 Go to original source...
  28. PELOSSE P., BERNSTEIN C. & DESOUHANT E. 2007: Differential energy allocation as an adaptation to different habitats in the parasitic wasp Venturia canescens. - Evol. Ecol. 21: 669-685 Go to original source...
  29. PELOSSE P., AMAT I., BERNSTEIN C. & DESOUHANT E. 2010: The dynamics of energy allocation in adult arrhenotokous and thelytokous Venturia canescens. - Entomol. Exp. Appl. 135: 68-76 Go to original source...
  30. REYSENBACH A.L., WICKHAM G.S. & PACE N.R. 1994: Phylogenetic analysis of the hyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park. - Appl. Environ. Microbiol. 60: 2113-2119
  31. SANDROCK C. & VORBURGER C. 2011: Single-locus recessive inheritance of asexual reproduction in a parasitoid wasp. - Curr. Biol. 21: 433-437 Go to original source...
  32. SARIDAKI A. & BOURTZIS K. 2010: Wolbachia: more than just a bug in insects genitals. - Curr. Opin. Microbiol. 13: 67-72 Go to original source...
  33. SCHNEIDER M.V., BEUKEBOOM L.W., DRIESSEN G., LAPCHIN L., BERNSTEIN C. & VAN ALPHEN J.J.M. 2002: Geographical distribution and genetic relatedness of sympatrical thelytokous and arrhenotokous populations of the parasitoid Venturia canescens (Hymenoptera). - J. Evol. Biol. 15: 191-200 Go to original source...
  34. SCHNEIDER M.V., DRIESSEN G., BEUKEBOOM L.W., BOLL R., VAN EUNEN K., SELZNER A., TALSMA J. & LAPCHIN L. 2003: Gene flow between arrhenotokous and thelytokous populations of Venturia canescens (Hymenoptera). - Heredity 90: 260-267. Go to original source...
  35. STEARNS S.C. 1990: The evolutionary maintenance of sexual reproduction: the solutions proposed for a longstanding problem. - J. Genet. 69: 1-10 Go to original source...
  36. STOUTHAMER R. & KAZMER D.J. 1994: Cytogenetics of microbeassociated parthenogenesis and its consequences for gene flow in Trichogramma wasps. - Heredity 73: 317-327 Go to original source...
  37. STOUTHAMER R., LUCK R.F. & HAMILTON W.D. 1990: Antibiotics cause parthenogenetic Trichogramma (Hymenoptera: Trichogrammatidae) to revert to sex. - PNAS 87: 2424-2427 Go to original source...
  38. STOUTHAMER R., VAN TILBORG M., DE JONG J.H., NUNNEY L. & LUCK R.F. 2001: Selfish element maintains sex in natural populations of a parasitoid wasp. - Proc. R. Soc. Lond. (B) 268: 617-622 Go to original source...
  39. SUZUKI M.T. & GIOVANNONI S.J. 1996: Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. - Appl. Environ. Microbiol. 62: 625-630
  40. THAO M.L.L. & BAUMANN P. 2004: Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). - Curr. Microbiol. 48: 140-144 Go to original source...
  41. THEOPOLD U., KRAUSE E. & SCHMIDT O. 1994: Cloning of a VLPprotein coding gene from a parasitoid wasp Venturia canescens. - Arch. Insect Biochem. Physiol. 26: 137-145 Go to original source...
  42. THIEL A., DRIESSEN G. & HOFFMEISTER T.S. 2006: Different habitats, different habits? Response to foraging information in the parasitic wasp Venturia canescens. - Behav. Ecol. Sociobiol. 59: 614-623 Go to original source...
  43. TOBLER M. & SCHLUPP I. 2010: Differential susceptibility to food stress in neonates of sexual and asexual mollies (Poecilia, Poeciliidae). - Evol. Ecol. 24: 39-47 Go to original source...
  44. TURELLI M. & HOFFMANN A.A. 1995: Cytoplasmic incompatibility in Drosophila simulans: Dynamics and parameters estimates from natural populations. - Genetics 140: 1319-1338
  45. WEISS L.M. & VOSSBRINCK C.R. 1998: Microsporidiosis: Molecular and diagnostic aspects. - Adv. Parasitol. 40: 351-396 Go to original source...
  46. WEISS L.M., ZHU X., CALI A., TANOWITZ H.B. & WITTNER M. 1994: Utility of microsporidian ribosomal-RNA in diagnosis and phylogeny - A review. - Folia Parasitol. 41: 81-90
  47. WERREN J.H. & WINDSOR D.M. 2000: Wolbachia infection frequencies in insects: Evidence of a global equilibrium? - Proc. R. Soc. Lond. (B) 267: 1277-1285 Go to original source...
  48. WERREN J.H., ZHANG W. & GUO L.R. 1995: Evolution and phylogeny of Wolbachia: Reproductive parasites of arthropods. - Proc. Biol. Sci. 261: 55-63 Go to original source...
  49. WERREN J.H., BALDO L. & CLARK M.E. 2008: Wolbachia: master manipulators of invertebrate biology. - Nat. Rev. Microbiol. 6: 741-751 Go to original source...
  50. ZCHORI-FEIN E. & PERLMAN S.J. 2004: Distribution of the bacterial symbiont Cardinium in arthropods. - Mol. Ecol. 13: 2009-2016 Go to original source...
  51. ZCHORI-FEIN E., GOTTLIEB Y., KELLY S.E., BRTOWN 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. USA 98: 12555-12560 Go to original source...