Skip to main content

The butterfly Danaus chrysippus (Lepidoptera: Nymphalidae) in Kenya is variably infected with respect to genotype and body size by a maternally transmitted male-killing endosymbiont (Spiroplasma)

  • Jeremy K. Herren (a1), Ian Gordon (a2), Peter W. H. Holland (a1) and David Smith (a3)

Female-biased sex ratios in Danaus chrysippus (Linnaeus) (family Nymphalidae, subfamily Danainae, tribe Danaini) populations are attributed to the action of an endosymbiotic ‘male-killer’ bacterium of the genus Spiroplasma. In stark contrast to the extensive geographic range of their host, the Spiroplasma appears to be restricted to East Africa, where four African D. chrysippus subspecies exist sympatrically and form a hybrid zone. In this study, specimens collected at three sample sites within the hybrid zone were screened for Spiroplasma infection. The findings demonstrate that, within the hybrid zone, the frequency of Spiroplasma infection varies both spatially and temporally. Host genotype at three biallelic wing pattern loci, representative of subspecific genetic divergence, is correlated to Spiroplasma infection. Linkage between the frequency of the recessive a allele and Spiroplasma is established, suggesting the presence of a linked allele controlling infection susceptibility. In addition, a negative correlation between D. chrysippus forewing length and Spiroplasma infection is identified, suggesting that infection has a deleterious effect on body size.

Corresponding author
Hide All
Bonduriansky R. (2001) The evolution of male mate choice in insects: A synthesis of ideas and evidence. Biological Reviews of the Cambridge Philosophical Society 72, 283327.
Clarke C. A., Sheppard P. M. and Smith A. G. (1973) The genetics of fore and hindwing colour in crosses between Danaus chrysippus from Australia and from Sierra Leone (Danaidae). Journal of the Lepidopterists' Society 27, 7377.
Edmunds M. E. (1976) Larval mortality and population regulation in the butterfly Danaus chrysippus in Ghana. Zoological Journal of the Linnean Society 58, 129145.
Fisher R. A. (1930) The Genetical Theory of Natural Selection. Oxford University Press, Oxford.
Gordon I. J. (1984) Polymorphism of the tropical butterfly Danaus chrysippus L. in Africa. Heredity 53, 583593.
Hornett A. E., Charlat S., Duplouy A. M. R., Davies N., Roderick G. K., Wedell N. and Hurst G. D. D. (2006) Evolution of male-killer suppression in a natural population. PLOS Biology 4 (9), e283.
Hurst G. D. D. and Jiggins F. M. (2000) Male-killing bacteria in insects: Mechanisms, incidence, and implications. Emerging Infectious Diseases 6, 329336.
Hurst G. D. D. and Werren J. H. (2001) The role of selfish genetic elements in eukaryotic evolution. Nature Reviews 2, 597606.
Hurst G. D., Graf von der Schulenburg J. H., Majerus T. M., Bertrand D., Zakharov I. A., Baungaard J. et al. . (1999) Invasion of one insect species, Adalia punctata, by two different male-killing bacteria. Insect Molecular Biology 8, 133–139.
Jiggins F. M., Hurst G. D. D., Jiggins C. D., Schulenburg J. H. G. V. D. and Majerus M. E. N. (2000) The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasitology 120, 439446.
Jiggins F. M., Randerson J. P., Hurst G. D. D. and Majerus M. E. N. (2002) How can sex ratio disorders reach extreme prevalences? Male-killing Wolbachia are not suppressed and have near-perfect vertical transmission efficiency in Acraea encedon. Evolution; International Journal of Organic Evolution 56, 2290–2295.
Lushai G., Allen J. A., Goulson D., Maclean N. and Smith D. A. S. (2005) The butterfly Danaus chrysippus (L.) in East Africa comprises polyphyletic, sympatric lineages that are, despite behavioural isolation, driven to hybridization by female-biased sex ratios. Biological Journal of the Linnean Society 86, 117–131.
Lushai G., Smith D. A. S., Gordon I. J., Goulson D., Allen J. A. and Maclean N. (2003) Incomplete sexual isolation in sympatry between subspecies of the butterfly Danaus chrysippus (L.) and the creation of a hybrid zone. Heredity 90, 236246.
Owen D. F. and Chanter D. O. (1968) Population biology of tropical African butterflies. 2. Sex ratio and polymorphism in Danaus chrysippus L. Revues Zoologiques et Botaniques Africaines 78, 81–97.
Smith D. A. S. (1975a) Genetics of some polymorphic forms of the African butterfly Danaus chrysippus L. (Lepidoptera: Danaidae). Entomologica Scandinavica 6, 134144.
Smith D. A. S. (1975b) All-female broods in Danaus chrysippus L. and their ecological significance. Heredity 34, 363371.
Smith D. A. S. (1980) Heterosis, epistasis and linkage disequilibrium in a wild population of the polymorphic butterfly Danaus chrysippus (L.). Zoological Journal of the Linnean Society 69, 87–109.
Smith D. A. S. (1998) Non-Mendelian segregation and variable penetrance of colour genes in the polymorphic butterfly Danaus chrysippus (L.). Heredity 80, 474480.
Smith D. A. S., Gordon I. J., Depew L. A. and Owen D. F. (1998) Genetics of the butterfly Danaus chrysippus (L.) in a broad hybrid zone, with special reference to sex ratio, polymorphism and intragenomic conflict. Biological Journal of the Linnean Society 65, 140.
Smith D. A. S., Lushai G. and Allen J. A. (2005) A classification of Danaus butterflies (Lepidoptera: Nymphalidae) based upon data from morphology and DNA. Zoological Journal of the Linnean Society 144, 191–212.
Smith D. A. S., Owen D. F., Gordon I. J. and Lowis N. K. (1997) The butterfly Danaus chrysippus (L.) in East Africa: Polymorphism and morph-ratio clines within a complex, extensive and dynamic hybrid zone. Zoological Journal of the Linnean Society 120, 51–78.
Stouthamer R. J., Breeuwer A. J. and Hurst G. D. D. (1999) Wolbachia pipientis: Microbial manipulator of arthropod reproduction. Annual Review of Microbiology 53, 71–102.
Talbot G. (1943) Revisional notes on the genus Danaus Kluk (Lep. Rhop. Danaidae). Transactions of the Royal Entomological Society 93, 115148.
Veneti Z., Toda M. J. and Hurst G. D. D. (2004) Host resistance does not explain variation in incidence of male-killing bacteria in Drosophila bifasciata. BMC Evolutionary Biology 4, 52.
Wada H., Komatsu M. and Satoh N. (1996) Mitochondrial rDNA phylogeny of the asteroidea suggests the primitiveness of the paxillosida. Molecular Phylogenetics and Evolution 6, 97106.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

International Journal of Tropical Insect Science
  • ISSN: 1742-7584
  • EISSN: 1742-7592
  • URL: /core/journals/international-journal-of-tropical-insect-science
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 1
Total number of PDF views: 17 *
Loading metrics...

Abstract views

Total abstract views: 72 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 22nd January 2018. This data will be updated every 24 hours.