Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-20T01:17:59.271Z Has data issue: false hasContentIssue false

A new male-killing parasitism: Spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae)

Published online by Cambridge University Press:  03 February 2006

M. C. TINSLEY
Affiliation:
Department of Genetics, University of Cambridge, Downing Street, Cambridge CB2 3EH, UK
M. E. N. MAJERUS
Affiliation:
Department of Genetics, University of Cambridge, Downing Street, Cambridge CB2 3EH, UK

Abstract

Whilst most animals invest equally in males and females when they reproduce, a variety of vertically transmitted parasites has evolved the ability to distort the offspring sex ratios of their hosts. One such group of parasites are male-killing bacteria. Here we report the discovery of females of the ladybird Anisosticta novemdecimpunctata that produced highly female-biased offspring sex ratios associated with a 50% reduction in egg hatch rate. This trait was maternally transmitted with high efficiency, was antibiotic sensitive and was infectious following experimental haemolymph injection. We identified the cause as a male-killing Spiroplasma bacterium and phylogenetic analysis of rDNA revealed that it belongs to the Spiroplasma ixodetis clade in which other sex ratio distorters lie. We tested the potential for interspecific horizontal transfer by injection from an infected A. novemdecimpunctata line into uninfected individuals of the two-spot ladybird Adalia bipunctata. In this novel host, the bacterium was able to establish infection, transmit vertically and kill male embryos.

Type
Research Article
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bandi, C., Dunn, A. M., Hurst, G. D. D. and Rigaud, T. ( 2001). Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends in Parasitology 17, 8894.CrossRefGoogle Scholar
Dyer, K. A., Minhas, M. S. and Jaenike, J. ( 2005). Expression and modulation of embryonic male-killing in Drosophila innubila: opportunities for multilevel selection. Evolution 59, 838848.CrossRefGoogle Scholar
Gasparich, G. E., Whitcomb, R. F., Dodge, D., French, F. E., Glass, J. and Williamson, D. L. ( 2004). The genus Spiroplasma and its non-helical descendants: phylogenetic classification, correlation with phenotype and roots of the Mycoplasma mycoides clade. International Journal of Systematic and Evolutionary Microbiology 54, 893918.CrossRefGoogle Scholar
Hasegawa, M., Kishino, H. and Yano, T. ( 1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 21, 160174.CrossRefGoogle Scholar
Hoffmann, A. A., Turelli, M. and Harshman, L. G. ( 1990). Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126, 933948.Google Scholar
Hunter, M. S., Perlman, S. J. and Kelly, S. E. ( 2003). A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proceedings of the Royal Society of London, B 270, 21852190.CrossRefGoogle Scholar
Hurst, G. D. D., Bandi, C., Sacchi, L., Cochrane, A., Bertrand, D., Karaca, I. and Majerus, M. E. N. ( 1999 b). Adonia variegata (Coleoptera: Coccinellidae) bears maternally inherited Flavobacteria that kill males only. Parasitology 118, 125134.Google Scholar
Hurst, G. D. D., Hammarton, T. M., Bandi, C., Majerus, T. M. O., Bertrand, D. and Majerus, M. E. N. ( 1997). The diversity of inherited parasites of insects: the male killing agent of the ladybird beetle Coleomegilla maculata is a member of the Flavobacteria. Genetical Research 70, 16.CrossRefGoogle Scholar
Hurst, G. D. D. and Jiggins, F. M. ( 2000). Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerging Infectious Diseases 6, 329336.CrossRefGoogle Scholar
Hurst, G. D. D., Jiggins, F. M. and Majerus, M. E. N. ( 2003). Inherited microorganisms that selectively kill male hosts: the hidden players of insect evolution? In Insect Symbiosis ( ed. Bourtzis, K. and Miller, T. A.). CRC Press, Boca Raton, FL, USA.CrossRef
Hurst, G. D. D. and Majerus, M. E. N. ( 1993). Why do maternally inherited microorganisms kill males? Heredity 71, 8195.Google Scholar
Hurst, G. D. D., Majerus, M. E. N. and Walker, L. E. ( 1992). Cytoplasmic male killing elements in Adalia bipunctata (Linnaeus) (Coleoptera: Coccinellidae). Heredity 69, 8491.CrossRefGoogle Scholar
Hurst, G. D. D., Schulenburg, J. H. G., Majerus, T. M. O., Bertrand, D., Zakharov, I. A., Baungaard, J., Volkl, W., Stouthamer, R. and Majerus, M. E. N. ( 1999 a). Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Molecular Biology 8, 133139.Google Scholar
Hurst, L. D. ( 1991). The incidences and evolution of cytoplasmic male killers. Proceedings of the Royal Society of London, B 244, 9199.CrossRefGoogle Scholar
Jiggins, F. M., Hurst, G. D. D., Jiggins, C. D., Schulenburg, J. H. G. and Majerus, M. E. N. ( 2000). The butterfly Danaus chrysippus is host to a male-killing Spiroplasma bacterium. Parasitology 120, 439446.CrossRefGoogle Scholar
Kumar, S., Tamura, K. and Nei, M. ( 2004). MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150163.CrossRefGoogle Scholar
Majerus, M. E. N. ( 1991). Habitat and host plant preferences of British ladybirds. Entomologists Monthly Magazine 127, 167175.Google Scholar
Majerus, M. E. N. and Hurst, G. D. D. ( 1997). Ladybirds as a model system for the study of male-killing symbionts. Entomophaga 42, 1320.CrossRefGoogle Scholar
Majerus, M. E. N., Kearns, P. W. E., Ireland, H. and Forge, H. ( 1989). Ladybirds as teaching aids: 1 Collecting and culturing. Journal of Biological Education 23, 8595.CrossRefGoogle Scholar
Majerus, T. M. O., Majerus, M. E. N., Knowles, B., Wheeler, J., Bertrand, D., Kuznetzov, V. N., Ueno, H. and Hurst, G. D. D. ( 1998). Extreme variation in the prevalence of inherited male-killing microorganisms between three populations of Harmonia axyridis (Coleoptera: Coccinellidae). Heredity 81, 683691.CrossRefGoogle Scholar
Majerus, T. M. O., Majerus, M. E. N., Schulenburg, J. H. G. and Hurst, G. D. D. ( 1999). Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinelidae). Insect Molecular Biology 8, 551555.CrossRefGoogle Scholar
Randall, K., Majerus, M. E. N. and Forge, H. ( 1992). Characteristics for sex determination in British ladybirds (Coleoptera: Coccinellidae). Entomologist 111, 109122.Google Scholar
Schulenburg, J. H. G., Habig, M., Sloggett, J. J., Webberley, K. M., Bertrand, D., Hurst, G. D. D. and Majerus, M. E. N. ( 2001). Incidence of male-killing Rickettsia spp. (α-proteobacteria) in the ten-spot ladybird beetle Adalia decempunctata L. (Coleoptera: Coccinellidae). Applied and Environmental Microbiology 67, 270277.Google Scholar
Schulenburg, J. H. G., Hurst, G. D. D., Tetzlaff, D., Booth, G. E., Zakharov, I. A. and Majerus, M. E. N. ( 2002). History of infection with different male-killing bacteria in the two-spot ladybird beetle Adalia bipunctata revealed through mitochondrial DNA analysis. Genetics 160, 10751086.Google Scholar
Sloggett, J. J. and Majerus, M. E. N. ( 2000). Habitat preferences and diet in the predatory Coccinellidae (Coleoptera): an evolutionary perspective. Biological Journal of The Linnean Society 70, 6388.CrossRefGoogle Scholar
Stevens, L. ( 1989). Environmental factors affecting reproductive incompatibility in flour beetles, genus Tribolium. Journal of Invertebrate Pathology 53, 7884.CrossRefGoogle Scholar
Swofford, D. L. ( 1998). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates. Sunderland, Massachusetts.
van Kuppeveld, F. J. M., van der Logt, H. T. M., van Zoest, M. J., Quint, W. G. V., Niesters, H. G. M., Galama, J. M. D. and Melchers, W. J. G. ( 1992). Genus- and species-specific identification of the mycoplasmas by 16s rDNA amplification. Applied and Environmental Microbiology 58, 26062615.Google Scholar
Veneti, Z., Bentley, J. K., Koana, T., Braig, H. R. and Hurst, G. D. D. ( 2005). A functional dosage compensation complex required for male killing in Drosophila. Science 307, 14611463.CrossRefGoogle Scholar
Weeks, A. R., Marec, F. and Breeuwer, J. A. J. ( 2001). A mite species that consists entirely of haploid females. Science 292, 24792482.CrossRefGoogle Scholar
Werren, J. H. and Windsor, D. M. ( 2000). Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proceedings of the Royal Society of London, B 267, 12771285.Google Scholar
Werren, J. H., Windsor, D. and Guo, L. R. ( 1995). Distribution of Wolbachia among neotropical arthropods. Proceedings of the Royal Society of London, B 262, 197204.CrossRefGoogle Scholar
Zchori-Fein, E. and Perlman, S. J. ( 2004). Distribution of the bacterial symbiont Cardinium in arthropods. Molecular Ecology 13, 20092016.CrossRefGoogle Scholar
Zchori-Fein, E., Gottlieb, Y., Kelly, S. E., Brown, J. K., Wilson, J. M., Karr, T. L. and Hunter, M. S. ( 2001). A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proceedings of the National Academy of Sciences, USA 98, 1255512560.CrossRefGoogle Scholar
Zhou, W. F., Rousset, F. and O'Neill, S. ( 1998). Phylogeny and PCR based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society of London, B 265, 509515.CrossRefGoogle Scholar