Abstract
BackgroundA number of recent studies have shown that the pattern of mitochondrial DNA variation and evolution is at odds with a neutral equilibrium model. Theory has suggested that selection on mitonuclear genotypes can act to maintain stable mitonuclear polymorphism within populations. However, this effect largely relies upon selection being either sex-specific or frequency dependent. Here, we use mitonuclear introgression lines to assess differences in a series of key life-history traits (egg-to-adult developmental time, viability, offspring sex-ratio, adult longevity and resistance to desiccation) in Drosophila subobscura fruit flies carrying one of three different sympatric mtDNA haplotypes.ResultsWe found functional differences between these sympatric mtDNA haplotypes, but these effects were contingent upon the nuclear genome with which they were co-expressed. Further, we demonstrate a significant mitonuclear genetic effect on adult sex ratio, as well as a sex × mtDNA × nuDNA interaction for adult longevity.ConclusionsThe observed effects suggest that sex specific mitonuclear selection contributes to the maintenance of mtDNA polymorphism and to mitonuclear linkage disequilibrium in this model system.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0421-2) contains supplementary material, which is available to authorized users.
Highlights
A number of recent studies have shown that the pattern of mitochondrial DNA variation and evolution is at odds with a neutral equilibrium model
We found no significant effects of mitochondrial DNA (mtDNA), Nuclear genetic background (nuDNA) or their interaction on overall egg-to-adult developmental time or egg-to-adult viability per replicate vial, in any of the three modules (Table 1)
The authors of a study that assessed metabolic rate suggested that negative frequency dependent selection may contribute to the maintenance of haplotype I and II [27]. This suggestion was based on (i) roughly equal frequencies of haplotypes I and II over the entire species range, (ii) the dynamics of haplotype change in laboratory populations [54] and (iii) recent evidence for negative frequency dependent selection on mtDNA in another insects species [34, 55]. While this may be true, the result of our study suggests an additional mechanism; sex-specific viability selection on mitonuclear genotypes may contribute both to the maintenance of mtDNA polymorphism and to mitonuclear linkage disequilibrium [24, 25]
Summary
A number of recent studies have shown that the pattern of mitochondrial DNA variation and evolution is at odds with a neutral equilibrium model. Theory has suggested that selection on mitonuclear genotypes can act to maintain stable mitonuclear polymorphism within populations. This effect largely relies upon selection being either sex-specific or frequency dependent. Genetic sequence variation within the mitochondrial genome (mtDNA) has by tradition been considered to represent accumulation under the neutral equilibrium model [1, 2] This view relied largely on the genetics of mtDNA: it is haploid, maternally transmitted and nonrecombining. A number of studies have shown that the pattern of mitochondrial DNA variation and evolution is often at odds with a neutral model. Recent experimental studies that use crossing designs to isolate effects
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