• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. May 2003; 164(1): 5–12.
PMCID: PMC1462540

Male-killing Wolbachia and mitochondrial DNA: selective sweeps, hybrid introgression and parasite population dynamics.


Mitochondrial DNA (mtDNA) sequences are widely used as neutral genetic markers in insects. However, patterns of mtDNA variability are confounded by the spread of maternally transmitted parasites, which are genetically linked to the mitochondria. We have investigated these effects in the butterflies Acraea encedon (which is host to two strains of male-killing Wolbachia bacteria) and A. encedana (which is host to one strain). Within a population, the mitochondria are in linkage disequilibrium with the different male-killers. Furthermore, there has been a recent selective sweep of the mtDNA, which has led to the loss of mitochondrial variation within populations and erased any geographical structure. We also found that one of the male-killers, together with the associated mtDNA, has introgressed from A. encedana into A. encedon within the last 16,000 years. Interestingly, because butterflies are female heterogametic, this will presumably have also led to the introgression of genes on the W sex chromosome. Finally, in A. encedon the mitochondria in uninfected females are unaltered by the spread of the male-killer and have diverse, geographically structured mtDNA. This means we can reject the hypothesis that the male-killer is at a stable equilibrium maintained by imperfect transmission of the bacterium. Instead, some other form of balancing selection may be maintaining uninfected females in the population and preventing the species from going extinct due to a shortage of males.

Full Text

The Full Text of this article is available as a PDF (106K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Jiggins Francis M, Randerson James P, Hurst Gregory D D, Majerus Michael E N. How can sex ratio distorters reach extreme prevalences? Male-killing Wolbachia are not suppressed and have near-perfect vertical transmission efficiency in Acraea encedon. Evolution. 2002 Nov;56(11):2290–2295. [PubMed]
  • McCauley DE, Taylor DR. Local population structure and sex ratio: evolution in gynodioecious plants. Am Nat. 1997 Sep;150(3):406–419. [PubMed]
  • Ballard JW. When one is not enough: introgression of mitochondrial DNA in Drosophila. Mol Biol Evol. 2000 Jul;17(7):1126–1130. [PubMed]
  • Montchamp-Moreau C, Ferveur JF, Jacques M. Geographic distribution and inheritance of three cytoplasmic incompatibility types in Drosophila simulans. Genetics. 1991 Oct;129(2):399–407. [PMC free article] [PubMed]
  • Ballard JW, Hatzidakis J, Karr TL, Kreitman M. Reduced variation in Drosophila simulans mitochondrial DNA. Genetics. 1996 Dec;144(4):1519–1528. [PMC free article] [PubMed]
  • Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. [PMC free article] [PubMed]
  • Fouts D, Ganguly R, Gutierrez AG, Lucchesi JC, Manning JE. Nucleotide sequence of the Drosophila glucose-6-phosphate dehydrogenase gene and comparison with the homologous human gene. Gene. 1988 Mar 31;63(2):261–275. [PubMed]
  • Randerson JP, Jiggins FM, Hurst LD. Male killing can select for male mate choice: a novel solution to the paradox of the lek. Proc Biol Sci. 2000 May 7;267(1446):867–874. [PMC free article] [PubMed]
  • Randerson JP, Smith NG, Hurst LD. The evolutionary dynamics of male-killers and their hosts. Heredity (Edinb) 2000 Feb;84(Pt 2):152–160. [PubMed]
  • Goldman N, Anderson JP, Rodrigo AG. Likelihood-based tests of topologies in phylogenetics. Syst Biol. 2000 Dec;49(4):652–670. [PubMed]
  • Rich SM, Licht MC, Hudson RR, Ayala FJ. Malaria's Eve: evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4425–4430. [PMC free article] [PubMed]
  • Hasegawa M, Kishino H, Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985;22(2):160–174. [PubMed]
  • Rousset F, Solignac M. Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6389–6393. [PMC free article] [PubMed]
  • Hillis DM, Dixon MT. Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol. 1991 Dec;66(4):411–453. [PubMed]
  • Hudson RR, Kreitman M, Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. [PMC free article] [PubMed]
  • Hurst GDD, Jiggins FM, Schulenburg J H G von der, Bertrand D, West SA, Goriacheva II, Zakharov IA, Werren JH, Stouthamer R, Majerus MEN. Male-killing Wolbachia in two species of insect. Proc Biol Sci. 1999 Apr 7;266(1420):735–735. [PMC free article]
  • Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. [PMC free article] [PubMed]
  • Tamura K. The rate and pattern of nucleotide substitution in Drosophila mitochondrial DNA. Mol Biol Evol. 1992 Sep;9(5):814–825. [PubMed]
  • Turelli M, Hoffmann AA. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics. 1995 Aug;140(4):1319–1338. [PMC free article] [PubMed]
  • Turelli M, Hoffmann AA, McKechnie SW. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics. 1992 Nov;132(3):713–723. [PMC free article] [PubMed]
  • Jiggins FM, Hurst GD, Majerus ME. Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc Biol Sci. 2000 Jan 7;267(1438):69–73. [PMC free article] [PubMed]
  • v d Schulenburg J Hinrich G, Hurst Gregory D D, Tetzlaff Dagmar, Booth Gwendolen E, Zakharov Ilia A, Majerus Michael E N. History of infection with different male-killing bacteria in the two-spot ladybird beetle Adalia bipunctata revealed through mitochondrial DNA sequence analysis. Genetics. 2002 Mar;160(3):1075–1086. [PMC free article] [PubMed]
  • Jiggins FM, Bentley JK, Majerus ME, Hurst GD. How many species are infected with Wolbachia? Cryptic sex ratio distorters revealed to be common by intensive sampling. Proc Biol Sci. 2001 Jun 7;268(1472):1123–1126. [PMC free article] [PubMed]
  • Zylstra P, Rothenfluh HS, Weiller GF, Blanden RV, Steele EJ. PCR amplification of murine immunoglobulin germline V genes: strategies for minimization of recombination artefacts. Immunol Cell Biol. 1998 Oct;76(5):395–405. [PubMed]
  • Jiggins Francis M, Bentley Joanna K, Majerus Michael E N, Hurst Gregory D D. Recent changes in phenotype and patterns of host specialization in Wolbachia bacteria. Mol Ecol. 2002 Aug;11(8):1275–1283. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...