A mitonuclear reality check on the evolutionary significance of Mother’s Curse in Drosophila.
Authors: David Rand; Faye Lemieux; Kenneth Bradley; Lindsay Marmor
Affiliation: Brown University
Keywords: Experimental evolution
Maternal inheritance allows selection to act on mtDNA-encoded effects in females, but prevents direct selection on mtDNA in males. Mutations that are deleterious in males but neutral or beneficial in females can persist in populations. This predicts that mtDNA-based disease or phenotypic variation should be more common in males, while haploid selection in females will purge mtDNA-based variation (Frank and Hurst (1996); repackaged as the ‘Mother’s Curse’ by Gemmell et al. (2004)). There is conflicting evidence for this pattern in the literature. A key assumption in Mother’s Curse is that mtDNA phenotypes must be sex limited with different effects, even different signs, in males and females. Extreme Mother’s Curse scenarios invoke mtDNA mutations that are beneficial in females and deleterious in males and sweep through populations leading to extinction from male unfitness. Comparisons of sex-specific mtDNA phenotypic effects from different populations and species are needed to evaluate the evolutionary significance of Mother’s Curse.
Most Mother’s Curse analyses use alternative mtDNAs placed on one or more homozygous nuclear chromosomal backgrounds. Since most organisms are heterozygous at many loci, we sought to perform experiments in several different heterozygous backgrounds. MtDNAs from Drosophila melanogaster (OreR and Zimbabwe), D. simulans (siI and siII) and D. yakuba were each placed on a common D. melanogaster w1118 nuclear background. Virgin females from these strains were crossed to males from each of several deficiency stocks carrying a hemizygous segment of chromosome 2L. F1 female and male flies carrying the deficiency chromosome and the w1118 chromosomes were tested for starvation, climbing and flight performance. For all three traits in the majority of chromosomal backgrounds, the variance among mtDNA genotypes was greater in females than in males. This result is the opposite of the Mother’s Curse prediction. Moreover, the impact of the foreign D. yakuba mtDNA was equally neutral or beneficial in both males and females, suggesting some form of phylogenetic heterosis. The mitonuclear epistatic interactions across the different heterozygous backgrounds and the five mtDNA haplotypes are more pronounced in females than males. This suggests that mtDNA interactions with regional hemizygosity or dominance effects are more pronounced in females than males, overshadowing any effect of Mother’s Curse or even hidden Y chromosome variation.