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Journal of Biosciences

, Volume 36, Issue 5, pp 845–850 | Cite as

Wolbachia endosymbiont infection in two Indian butterflies and female-biased sex ratio in the Red Pierrot, Talicada nyseus

  • Kunal Ankola
  • Dorothea Brueckner
  • H P Puttaraju
Article

Abstract

The maternally inherited obligate bacteria Wolbachia is known to infect various lepidopteran insects. However, so far only a few butterfly species harbouring this bacterium have been thoroughly studied. The current study aims to identify the infection status of these bacteria in some of the commonly found butterfly species in India. A total of nine butterfly species belonging to four different families were screened using PCR with Wolbachia-specific wsp and ftsZ primers. The presence of the Wolbachia super group ‘B’ in the butterflies Red Pierrot, Talicada nyseus (Guerin) (Lepidoptera: Lycaenidae) and Blue Mormon, Papilio polymnestor Cramer (Papilionidae), is documented for the first time in India. The study also gives an account on the lifetime fecundity and female-biased sex ratio in T. nyseus, suggesting a putative role for Wolbachia in the observed female-biased sex ratio distortion.

Keywords

Papilio polymnestor PCR sex ratio Talicada nyseus Wolbachia 

Notes

Acknowledgements

The authors thank Mr Millo Tago IFS, Curator, Bannerghatta Biological Park, Mr Venkatachalapati, MSc, Scientist, Butterfly Park, Bannerghatta Biological Park, Bangalore, and Prof Atef Sayed Abdel-Razek, Department of Pest and Plant Protection, National Research Centre, Cairo, for their useful suggestions and constant support during the study. The authors are also thankful to the Department of Science and Technology, India, for financial assistant and Bangalore University for providing necessary infrastructure and facilities.

References

  1. Arakaki N, Miyoshi T and Noda H 2001 Wolbachia-mediated parthenogenesis in the predatory thrips Franklinothrips vespiformis (Thysanoptera: Insecta). Proc. R. Soc. London B. 268 1011–1016CrossRefGoogle Scholar
  2. Breeuwer JAJ and Werren JH 1990 Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature (London) 346 558–560CrossRefGoogle Scholar
  3. Breeuwer JAJ, Stouthamer R, Barns SM, Pelletier DA, Weisburg WG and Werren JH 1992 Phylogeny of Cytoplasmic Incompatability microorganisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16S ribosomal DNA sequences. Insect Mol. Biol. 1 25–36PubMedCrossRefGoogle Scholar
  4. Charlat S, Hornett EA, Dyson EA, Patrick PYH, Thiloc N, Schilthuizen M, Davies N, Roderick GK and Hurst GDD 2005 Prevalence and Penetrance variation of male-killing Wolbachia across Indo-Pacific Populations of the Butterfly Hypolimnas bolina. Mol. Ecol. 14 3525–3530PubMedCrossRefGoogle Scholar
  5. Dyson EA, Kamath MK and Hurst GDD 2002 Wolbachia infection associated with all female broods in Hypolimnas bolina (Lepidoptera: Nymphalidae): evidence for horizontal transmission of a butterfly male killer. Heredity 88 166–171PubMedCrossRefGoogle Scholar
  6. Fialho RF and Stevens L 1997 Molecular evidence for single Wolbachia infections among geographic strains of the flour beetle Tribolium confusum. Proc. R. Soc. London B. 264 1065–1068CrossRefGoogle Scholar
  7. Fialho RF and Stevens L 2000 Male-killing Wolbachia in a flour beetle. Proc. R. Soc. London B. 267 1469–1474CrossRefGoogle Scholar
  8. Hiroki M, Kato Y, Kamito T and Miura K 2002 Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae). Naturwissenschaften 89 167–170PubMedCrossRefGoogle Scholar
  9. Hiroki M, Yohsuke Tagami Y, Miura K and Kato Y 2004 Multiple infections with Wolbachia inducing different reproductive manipulations in the butterfly Eurema hecabe. Proc. R. Soc. London B. 271 1751–1755CrossRefGoogle Scholar
  10. Hurst GDD and Jiggins FM 2000 Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerging Infect. Dis. 6 329–336PubMedCrossRefGoogle Scholar
  11. Hurst GDD, Jiggins FM, Von der Schulenburg JHG, Bertrand D, West SA, Goriacheva II, Zakhrov IA, Werren JH, Stouthamer R and Majerus MEN 1999 Male-killing Wolbachia in two species of insect. Proc. R. Soc. London B. 266 735–740CrossRefGoogle Scholar
  12. Hurst GDD, Johnson AP, Von der Schulenburg JHG and Fuyama Y 2000 Male-killing Wolbachia. Drosophila: a temperature sensitive trait with a threshold bacteria density. Genetics 156 699–709PubMedGoogle Scholar
  13. Jeyaprakash A and Hoy MA 2000 Long PCR improves Wolachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol. Biol. 9 393–405PubMedCrossRefGoogle Scholar
  14. Jiggins FM, Hurst GDD and Majerus MEN 1998 Sex ratio distortion in Acraea encedon (Lapidoptera: Nymphalidae) is caused by a male killing bacterium. Heredity 81 87–91CrossRefGoogle Scholar
  15. Jiggins FM, Hurst GDD and Majerus MEN 1999 Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc. R. Soc. London B. 267 69–73CrossRefGoogle Scholar
  16. Jiggins FM, Hurst GDD, Jiggins CD, Schulenburg JHGVD and Majerus MEN 2000 The butterfly Danaus chrysippus is infected by male-killing Spiroplasma bacterium. Parasitology 120 439–446PubMedCrossRefGoogle Scholar
  17. Jiggins FM, Hurst GD, Schulenburg JH and Majerus ME 2001 Two male-killing Wolbachia strains coexist within a population of the butterfly Acraea encedon. Heredity 86 161–166PubMedCrossRefGoogle Scholar
  18. Karunaratne V, Bombuwela K, Kathirgamanathar S, Kumar V, Nedra Karunaratne D, Ranawana KB, Wijesundara DSA, Weerasooriya A and De Silva ED 2002 An association between the butterfly Talicada nyseus and the lichen Leproloma sipmanianum as evidenced from chemical studies. Curr. Sci. 83 741–745Google Scholar
  19. Laven H 1967 Speciation and evolution in Culex pipiens; in Genetics of insect vectors of disease (eds) J Wright and R Pal (Amsterdam: Elsevier) pp 251–275Google Scholar
  20. Narita S, Kageyama D, Nomura M and Fukatsu T 2007 Unexpected mechanism of symbiont-induced reversal of insect sex: Feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development. Appl. Environ. Microbiol. 73 4332–4341PubMedCrossRefGoogle Scholar
  21. O’Neill SL, Giordano R, Colbert AME, Karr TL and Robertson HM 1992 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Nat. Acad. Sci. USA 89 2699–2702PubMedCrossRefGoogle Scholar
  22. O’Neill SL, Hoffmann AA and Werren JH 1997 Influential passengers: inherited microorganisms and arthropod reproduction (New York: Oxford University Press)Google Scholar
  23. Prakash BM and Puttaraju HP 2007 Frequency of infection with A and B super group Wolbachia in insects and pests associated with mulberry and silkworm. J. Biosci. 32 671–676PubMedCrossRefGoogle Scholar
  24. Puttaraju HP and Madhu M 2002 Presence of Wolbachia endosymbionts in different silkworm species and races and in their uzifly parasites. J. Invertebrate Pathol. 79 120–122CrossRefGoogle Scholar
  25. Puttaraju HP and Prakash BM 2005a Wolbachia and reproductive conflict in Exorista sorbillans (Diptera: Tachinidae). Arch. Insect Biochem. Physiol. 60 230–235CrossRefGoogle Scholar
  26. Puttaraju HP and Prakash BM 2005b Effects of Wolbachia in the Uzifly, Exorista sorbillans, a parasitoid of the silkworm, Bombyx mori. J. Insect Sci. 5 30Google Scholar
  27. Rousset F, Bouchon D, Pintureau B, Juchault P and Solignac M 1992 Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc. R. Soc. London B. 250 91– 98CrossRefGoogle Scholar
  28. Sambrook J, Fritshi EF and Miniatis T 1989 Molecular cloning: A laboratory manual 2nd edition (NewYork: Cold Spring Harbor Laboratory Press) p 999Google Scholar
  29. Singh AP 2005 Initial colonization of Red Pierrot butterfly, Talicada nyseus Guerin (Lycaenidae) in the lower western Himalayas: An indicator of the changing environment. Curr. Sci. 89 41–42Google Scholar
  30. Stouthamer R, Luck RF and Hamilton WD 1990 Antibiotics cause parthenogenetic Trichogramma to revert to sex. Proc. Nat. Acad. Sci. USA 87 2424–2427PubMedCrossRefGoogle Scholar
  31. Stouthamer R, Breeuwer JAJ, Luck RF and Werren JH 1993 Molecular identification of microorganisms associated with parthenogenesis. Nature (London) 361 66–68CrossRefGoogle Scholar
  32. Tabata J, Hattori Y, Sakamoto H, Yukuhiro F, Fujii T, Kugimiya S, Mochizuki A, Ishikawa Y and Kageyama D 2011 Male killing and incomplete inheritance of a novel Spiroplasma in the moth Ostrinia zaguliaevi. Microb. Ecol. 61 254–263.PubMedCrossRefGoogle Scholar
  33. Werren JH, Zhang W and Guo LR 1995 Evolution and phylogeny of Wolbachia: reproductive parasite of arthropod. Proc. R. Soc. London B. 161 55–63CrossRefGoogle Scholar
  34. Werren JH and Windsor DW 2000 Wolbachia infection frequencies in insects: evidence of a global equilibrium. Proc. R. Soc. London B. 267 1277–1285CrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2011

Authors and Affiliations

  • Kunal Ankola
    • 1
  • Dorothea Brueckner
    • 2
  • H P Puttaraju
    • 1
  1. 1.Division of Biological Sciences, School of Natural SciencesBangalore UniversityBangaloreIndia
  2. 2.Department of BiologyUniversity of BremenBremenGermany

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