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Mitochondria are often referred to as the powerhouse of the cell. However, research linking intraspecific differences in organismal fitness with genotypic mitochondrial DNA (mtDNA) variation has been hampered by the lack of variation in experimentally tractable species. This study examines whether fly lines harbouring three distinct Drosophila simulans mtDNA types (siI, -II and -III) exhibit differential fitness in laboratory perturbation cages. Comparison of the pre-perturbation and post-perturbation data shows that both the mtDNA and mitonuclear interactions have a significant and repeatable effect on the frequency of flies with specific genotypes in population cages (siII > -III > -I) and that coadapted mitonuclear interactions are greatest in the siI type. The rank order of mtDNA frequency correlates with the observed worldwide distribution of the haplogroups while mitonuclear interactions are most significant in the siI haplogroup that is likely to have been subject to repeated population bottlenecks. One possible explanation for the maintenance of the least fit siI haplogroup on Pacific islands is that it is protected from extinction by Wolbachia infection. [ABSTRACT FROM AUTHOR]