Skip to main content
Genetics logoLink to Genetics
. 2002 Mar;160(3):1075–1086. doi: 10.1093/genetics/160.3.1075

History of infection with different male-killing bacteria in the two-spot ladybird beetle Adalia bipunctata revealed through mitochondrial DNA sequence analysis.

J Hinrich G v d Schulenburg 1, Gregory D D Hurst 1, Dagmar Tetzlaff 1, Gwendolen E Booth 1, Ilia A Zakharov 1, Michael E N Majerus 1
PMCID: PMC1462029  PMID: 11901123

Abstract

The two-spot ladybird beetle Adalia bipunctata (Coleoptera: Coccinellidae) is host to four different intracellular maternally inherited bacteria that kill male hosts during embryogenesis: one each of the genus Rickettsia (alpha-Proteobacteria) and Spiroplasma (Mollicutes) and two distinct strains of Wolbachia (alpha-Proteobacteria). The history of infection with these male-killers was explored using host mitochondrial DNA, which is linked with the bacteria due to joint maternal inheritance. Two variable regions, 610 bp of cytochrome oxidase subunit I and 563 bp of NADH dehydrogenase subunit 5, were isolated from 52 A. bipunctata with known infection status and different geographic origin from across Eurasia. Two outgroup taxa were also considered. DNA sequence analysis revealed that the distribution of mitochondrial haplotypes is not associated with geography. Rather, it correlates with infection status, confirming linkage disequilibrium between mitochondria and bacteria. The data strongly suggest that the Rickettsia male-killer invaded the host earlier than the other taxa. Further, the male-killing Spiroplasma is indicated to have undergone a recent and extensive spread through host populations. In general, male-killing in A. bipunctata seems to represent a highly dynamic system, which should prove useful in future studies on the evolutionary dynamics of this peculiar type of symbiont-host association.

Full Text

The Full Text of this article is available as a PDF (110.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ballard J. W. Comparative genomics of mitochondrial DNA in Drosophila simulans. J Mol Evol. 2000 Jul;51(1):64–75. doi: 10.1007/s002390010067. [DOI] [PubMed] [Google Scholar]
  2. Ballard J. W., Hatzidakis J., Karr T. L., Kreitman M. Reduced variation in Drosophila simulans mitochondrial DNA. Genetics. 1996 Dec;144(4):1519–1528. doi: 10.1093/genetics/144.4.1519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beard C. B., Hamm D. M., Collins F. H. The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Mol Biol. 1993;2(2):103–124. doi: 10.1111/j.1365-2583.1993.tb00131.x. [DOI] [PubMed] [Google Scholar]
  4. Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. doi: 10.1007/BF02099755. [DOI] [PubMed] [Google Scholar]
  5. Cockerham C. C. Analyses of gene frequencies. Genetics. 1973 Aug;74(4):679–700. doi: 10.1093/genetics/74.4.679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crozier R. H., Crozier Y. C. The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics. 1993 Jan;133(1):97–117. doi: 10.1093/genetics/133.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Excoffier L., Smouse P. E., Quattro J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992 Jun;131(2):479–491. doi: 10.1093/genetics/131.2.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Flook P. K., Rowell C. H., Gellissen G. The sequence, organization, and evolution of the Locusta migratoria mitochondrial genome. J Mol Evol. 1995 Dec;41(6):928–941. doi: 10.1007/BF00173173. [DOI] [PubMed] [Google Scholar]
  9. Guillemaud T., Pasteur N., Rousset F. Contrasting levels of variability between cytoplasmic genomes and incompatibility types in the mosquito Culex pipiens. Proc Biol Sci. 1997 Feb 22;264(1379):245–251. doi: 10.1098/rspb.1997.0035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hurst G. D., Graf von der Schulenburg J. H., Majerus T. M., Bertrand D., Zakharov I. A., Baungaard J., Völkl W., Stouthamer R., Majerus M. E. Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Mol Biol. 1999 Feb;8(1):133–139. doi: 10.1046/j.1365-2583.1999.810133.x. [DOI] [PubMed] [Google Scholar]
  11. Hurst G. D., Jiggins F. M. Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Dis. 2000 Jul-Aug;6(4):329–336. doi: 10.3201/eid0604.000402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. James A. C., Ballard J. W. Expression of cytoplasmic incompatibility in Drosophila simulans and its impact on infection frequencies and distribution of Wolbachia pipientis. Evolution. 2000 Oct;54(5):1661–1672. doi: 10.1111/j.0014-3820.2000.tb00710.x. [DOI] [PubMed] [Google Scholar]
  13. Lewis D. L., Farr C. L., Kaguni L. S. Drosophila melanogaster mitochondrial DNA: completion of the nucleotide sequence and evolutionary comparisons. Insect Mol Biol. 1995 Nov;4(4):263–278. doi: 10.1111/j.1365-2583.1995.tb00032.x. [DOI] [PubMed] [Google Scholar]
  14. Lunt D. H., Zhang D. X., Szymura J. M., Hewitt G. M. The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Mol Biol. 1996 Aug;5(3):153–165. doi: 10.1111/j.1365-2583.1996.tb00049.x. [DOI] [PubMed] [Google Scholar]
  15. Majerus M. E., Hinrich J., Schulenburg G. V., Zakharov I. A. Multiple causes of male-killing in a single sample of the two-spot ladybird, Adalia bipunctata (Coleoptera: coccinellidae) from Moscow. Heredity (Edinb) 2000 May;84(Pt 5):605–609. doi: 10.1046/j.1365-2540.2000.00710.x. [DOI] [PubMed] [Google Scholar]
  16. Nigro L., Prout T. Is there selection on RFLP differences in mitochondrial DNA? Genetics. 1990 Jul;125(3):551–555. doi: 10.1093/genetics/125.3.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. doi: 10.1098/rspb.1999.0698. [DOI] [PMC free article] [Google Scholar]
  18. Posada D., Crandall K. A. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817–818. doi: 10.1093/bioinformatics/14.9.817. [DOI] [PubMed] [Google Scholar]
  19. Randerson J. P., Smith N. G., Hurst L. D. The evolutionary dynamics of male-killers and their hosts. Heredity (Edinb) 2000 Feb;84(Pt 2):152–160. doi: 10.1046/j.1365-2540.2000.00645.x. [DOI] [PubMed] [Google Scholar]
  20. Rigaud T., Bouchon D., Souty-Grosset C., Raimond R. Mitochondrial DNA polymorphism, sex ratio distorters and population genetics in the isopod Armadillidium vulgare. Genetics. 1999 Aug;152(4):1669–1677. doi: 10.1093/genetics/152.4.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rokas A., Atkinson R. J., Brown G. S., West S. A., Stone G. N. Understanding patterns of genetic diversity in the oak gallwasp Biorhiza pallida: demographic history or a Wolbachia selective sweep? Heredity (Edinb) 2001 Sep;87(Pt 3):294–304. doi: 10.1046/j.1365-2540.2001.00872.x. [DOI] [PubMed] [Google Scholar]
  22. Schulenburg J. H., Hurst G. D., Huigens T. M., van Meer M. M., Jiggins F. M., Majerus M. E. Molecular evolution and phylogenetic utility of Wolbachia ftsZ and wsp gene sequences with special reference to the origin of male-killing. Mol Biol Evol. 2000 Apr;17(4):584–600. doi: 10.1093/oxfordjournals.molbev.a026338. [DOI] [PubMed] [Google Scholar]
  23. Shoemaker D. D., Ross K. G., Keller L., Vargo E. L., Werren J. H. Wolbachia infections in native and introduced populations of fire ants (Solenopsis spp.). Insect Mol Biol. 2000 Dec;9(6):661–673. doi: 10.1046/j.1365-2583.2000.00233.x. [DOI] [PubMed] [Google Scholar]
  24. Von Der Schulenburg Hinrich Graf, Majerus Tamsin M. O., Dorzhu Chorduraa M., Zakharov Ilia A., Hurst Gregory D. D., Majerus Michael E. N. Evolution of male-killing Spiroplasma (Procaryotae: Mollicutes) inferred from ribosomal spacer sequences. J Gen Appl Microbiol. 2000 Apr;46(2):95–98. doi: 10.2323/jgam.46.95. [DOI] [PubMed] [Google Scholar]
  25. Werren J. H., Hurst G. D., Zhang W., Breeuwer J. A., Stouthamer R., Majerus M. E. Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). J Bacteriol. 1994 Jan;176(2):388–394. doi: 10.1128/jb.176.2.388-394.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yang Z., Goldman N., Friday A. Comparison of models for nucleotide substitution used in maximum-likelihood phylogenetic estimation. Mol Biol Evol. 1994 Mar;11(2):316–324. doi: 10.1093/oxfordjournals.molbev.a040112. [DOI] [PubMed] [Google Scholar]
  27. von der Schulenburg J. H., Habig M., Sloggett J. J., Webberley K. M., Bertrand D., Hurst G. D., Majerus M. E. Incidence of male-killing Rickettsia spp. (alpha-proteobacteria) in the ten-spot ladybird beetle Adalia decempunctata L. (Coleoptera: Coccinellidae). Appl Environ Microbiol. 2001 Jan;67(1):270–277. doi: 10.1128/AEM.67.1.270-277.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. von der Schulenburg J. H., Hancock J. M., Pagnamenta A., Sloggett J. J., Majerus M. E., Hurst G. D. Extreme length and length variation in the first ribosomal internal transcribed spacer of ladybird beetles (Coleoptera: Coccinellidae). Mol Biol Evol. 2001 Apr;18(4):648–660. doi: 10.1093/oxfordjournals.molbev.a003845. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES