Skip to main content
SpringerLink
Log in

Effect of Wolbachia infection and temperature variations on the fecundity of the Uzifly Exorista sorbillans (Diptera: Tachinidae)

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Wolbachia are cytoplasmically inherited endosymbionts known to cause several reproductive alterations in insects which allow their spread in host populations. In the Uzifly Exorista sorbillans, endoparasites of silkworms, the prevalence of Wolbachia is high in the field. In the present study, we investigated Wolbachia’s effects on the Uzifly fitness traits by measuring fecundity and hatching rate in crosses involving infected and cured individuals. We found evidence for positive fitness effects associated with Wolbachia infection in females which could help promote the spread of Wolbachia in E. sorbillans populations. We tested two types of treatments for removing Wolbachia, antibiotic therapy and high temperature treatment and found an influence on the reproduction: females treated by antibiotics have a lower fecundity than females cured by high temperature which could indicate a negative effect of the antibiotherapy on females’ fitness. Furthermore, the monitoring of the Uzifly populations during 2 years revealed seasonal variations of the offspring production which may be linked to temperature.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Braig HR, Zhou W, Dobson SL, O’Neill SL (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol 180:2373–2378

    PubMed  CAS  Google Scholar 

  • Breeuwer JAJ, Werren JH (1993) Effect of genotype on cytoplasmic incompatibility between two species of Nasonia. Heredity 70:428–436

    Article  Google Scholar 

  • Brownlie JC, Cass BN, Riegler M, Witsenburg JJ, Iturbe-Ormaetxe I, McGraw EA, O’Neill SL (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLOS Pathogens 5:e1000368

    Article  PubMed  Google Scholar 

  • Chatterjee SN, Mohandas TP, Taraphdar T (2003) Molecular characterization of the gene pool of Exorista sorbillans (Diptera: Tachnindae), a parasitoid of silkworm Bombyx mori, in India. Eur J Entomol 100:195–200

    CAS  Google Scholar 

  • Chen DQ, Montllor CB, Purcell AH (2000) Fitness effects of two facultative endosymbiotic bacteria on the pea aphid Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomol Exp Appl 95:315–323

    Article  Google Scholar 

  • Cossins AR, Bowler K (1987) Temperature biology of animals. Chapman & Hall, New York

    Book  Google Scholar 

  • David JR, Allemand R, Van Heerewege J, Cohet Y (1983) The genetics and biology of Drosophila. In: Ashburner M, Carson HL, Thompson JN (eds) Ecophysiology: abiotic factors. Academic, London, pp 106–170

    Google Scholar 

  • Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 98:6247–6252

    Article  PubMed  CAS  Google Scholar 

  • Dobson SL, Marsland EJ, Rattanadechakul W (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160:1087–1094

    PubMed  Google Scholar 

  • Douglas AE (1994) Symbiotic interactions. Oxford University Press, Oxford

    Google Scholar 

  • Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747–754

    Article  PubMed  CAS  Google Scholar 

  • Ferrari J, Godfray HCJ (2003) Resistance to a fungal pathogen and host plant specialization in the pea aphid. Ecol Lett 6:111–118

    Article  Google Scholar 

  • Fry AJ, Rand DM (2002) Wolbachia interactions that determine Drosophila melanogaster survival. Evolution 56:1976–1981

    PubMed  Google Scholar 

  • Fry AJ, Palmer MR, Rand DM (2004) Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity 93:379–389

    Article  PubMed  CAS  Google Scholar 

  • Guruprasad NM, Mouton L, Sumithra, Putturaju HP (2011) Phylogeny of Wolbachia and its phage WO in the Uzifly Exorista sorbillans (Diptera: Tachinidae). Curr Microbiol 63:267–272

    Article  PubMed  CAS  Google Scholar 

  • Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702

    Article  PubMed  CAS  Google Scholar 

  • Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia?- a statistical analysis of current data. FEMS Microbiol Lett 281:215–220

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hosokawa T, Koga R, Kikuchi Y, Meng X-Y, Fukatsu T (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci USA 107:769–774

    Article  PubMed  CAS  Google Scholar 

  • Huey RB, Berrigan D (2001) Temperature, demography, and ectotherm fitness. Am Nat 158:204–210

    Article  PubMed  CAS  Google Scholar 

  • Hurst GDD, Jiggins FM, Schulenburg JHGVD, Bertand D, West SA, Goriacheva II, Zakharov IA, Werren JH, Stouthamer R, Majerus MEN (1999) Male-killing Wolbachia in two species of insect. Proc Roy Soc Lond B Biol Sci 266:735–740

    Article  Google Scholar 

  • Jeyaprakash A, Hoy MA (2000) Long PCR improves Wolbachia DNA amplification: WSP sequence found in 76% of sixty-three arthropod species. Insect Mol Biol 9:393–405

    Article  PubMed  CAS  Google Scholar 

  • Johanowicz DL, Hoy MA (1998) Experimental induction and termination of non-reciprocal reproductive incompatibilities in a parahaploid mite. Entomol Exp Appl 87:51–58

    Article  Google Scholar 

  • Krebs RA, Loeschcke V (1994) Costs and benefits of activation of the heat-shock response in Drosophila melanogaster. Funct Ecol 8:730–737

    Article  Google Scholar 

  • Krishnaswamy S (1978) New technology of Silkworm rearing. Bulletin-2. CSR and TI, Mysore

    Google Scholar 

  • Kyei-Poku GK, Floate KD, Benkel B, Goettel MS (2003) Elimination of Wolbachia from Urolepis rufipes (Ashmead) (Hymenoptera: Pteromalidae) with heat and antibiotic treatments: implications for host reproduction. Biocontrol Sci Technol 13:341–354

    Article  Google Scholar 

  • Manjunatha HB (1993) Morphological and Cytological investigations on the uzifly, Exorista sorbillans. Ph. D. Thesis, Bangalore University, Bangalore, India

  • Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195

    Article  Google Scholar 

  • Mouton L, Dedeine F, Henri H, Boulétreau M, Profizi N, Vavre F (2004) Virulence, multiple infections and regulation of symbiotic population in the Wolbachia-Asobara tabida symbiosis. Genetics 168:181–189

    Article  PubMed  Google Scholar 

  • Mouton L, Henri H, Bouletreau M, Vavre F (2006) Effect of temperature on Wolbachia density and impact on cytoplasmic incompatibility. Parasitology 132:49–56

    Article  PubMed  CAS  Google Scholar 

  • O’Neill SL, Karr TL (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348:178–180

    Article  PubMed  Google Scholar 

  • Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacteria in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100:1803–1807

    Article  CAS  Google Scholar 

  • Olsen K, Reynolds KT, Hoffmann AA (2001) A field cage test of the effects of the endosymbiont Wolbachia on Drosophila melanogaster. Heredity 86:731–737

    Article  PubMed  CAS  Google Scholar 

  • Perrot-Minnot MJ, Guo LR, Werren JH (1996) Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis: effects on compatibility. Genetics 143:961–972

    PubMed  CAS  Google Scholar 

  • Poinsot D, Merçot H (1997) Wolbachia infection in Drosophila simulans: does the female host bear a physiological cost? Evolution 51:180–186

    Article  Google Scholar 

  • Puttaraju HP, Prakash BM (2005) Effects of Wolbachia in the uzifly, Exorista sorbillans, a parasitoid of silkworm, Bombyx mori. J Insect Sci 5(30)

  • Rigaud T, Juchault P, Mocquard JP (1991a) Experimental study of temperature effects on the sex ratio of broods in terrestrial crustacea Armadillidium vulgare Latr. Possible implications in natural populations. J Evol Biol 4:603–617

    Article  Google Scholar 

  • Rigaud T, Souty-Grosset C, Raimond R, Mocquard J, Juchault P (1991b) Feminizing endocytobiosis in the terrestrial crustacean Armadillidium vulgare LATR. (Isopoda): recent acquisitions. Endocytobiosis Cell Res 7:259–273

    Google Scholar 

  • Ris N, Allemand R, Fouillet P, Fleury F (2004) The joint effect of temperature and host species induces complex genotype-by-environment interactions in the larval parasitoid of Drosophila, Leptopilina heterotoma (Hymenoptera: Figitidae). Oikos 106:451–456

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Miniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Silbermann R, Tatar M (2000) Reproductive costs of heat shock protein in transgenic Drosophila melanogaster. Evolution 54:2038–2045

    PubMed  CAS  Google Scholar 

  • Stevens L (1989) Environmental factors affecting reproductive incompatibility in flour beetles, genus Tribolium. J Invertebr Pathol 53:78–84

    Article  PubMed  CAS  Google Scholar 

  • Stouthamer R, Luck RF, Hamilton WD (1990) Antibiotics cause parthenogenetic Trichogramma to revert to sex. Proc Natl Acad Sci USA 87:2424–2427

    Article  PubMed  CAS  Google Scholar 

  • Stouthamer R, Breeuwer JAJ, Hurst GDD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102

    Article  PubMed  CAS  Google Scholar 

  • Taylor MJ, Bandi C, Hoerauf A (2005) Wolbachia bacterial endosymbiont of filarial nematodes. Adv Parasitol 60:245–284

    Article  PubMed  Google Scholar 

  • Team RDC (2006) R: a language and environment for statistical computing. R foundation for Statistical Computing, Vienna, Austria, URL http://www.R-project.org

  • Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989

    Article  PubMed  CAS  Google Scholar 

  • Van Opijnen T, Breeuwer JA (1999) High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Exp Appl Acarol 23:871–881

    Article  PubMed  Google Scholar 

  • Werren JH, Zhang W, Guo LR (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc Roy Soc Lond B Biol Sci 261:55–63

    Article  CAS  Google Scholar 

  • Zhou W, Rousset F, O’Neill SL (1998) Phylogeny and PCR-based classification of Wolbachia strain using wsp gene sequences. Proc Roy Soc Lond B Biol Sci 265:509–515

    Article  CAS  Google Scholar 

Download references

Acknowledgement

Funding for this study was provided by grants from DST, Government of India to H.P. Puttaraju (SR/SO/AS-77/2008).

Author information

Authors and Affiliations

  1. Biotechnology Research Lab, Department of Sericulture & Biological Sciences, Bangalore University, Bangalore, 560056, India

    N. M. Guruprasad & H. P. Puttaraju

  2. Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, UMR CNRS 5558, 43 Bd du 11 Novembre 1918, 69622, Villeurbanne Cedex, France

    L. Mouton

Authors
  1. N. M. Guruprasad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. Mouton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. P. Puttaraju
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. P. Puttaraju.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guruprasad, N.M., Mouton, L. & Puttaraju, H.P. Effect of Wolbachia infection and temperature variations on the fecundity of the Uzifly Exorista sorbillans (Diptera: Tachinidae). Symbiosis 54, 151–158 (2011). https://doi.org/10.1007/s13199-011-0138-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-011-0138-y

Keywords

Search

Navigation