Temperature-Specific and Sex-Specific Fitness Effects of Sympatric Mitochondrial and Mito-Nuclear Variation in Drosophila obscura

Abstract

The adaptive significance of sympatric mitochondrial (mtDNA) variation and the role of selective mechanisms that maintain it are debated to this day. Isofemale lines of Drosophila obscura collected from four populations were backcrossed within populations to construct experimental lines, with all combinations of mtDNA Cyt b haplotypes and nuclear genetic backgrounds (nuDNA). Individuals of both sexes from these lines were then subjected to four fitness assays (desiccation resistance, developmental time, egg-to-adult viability and sex ratio) on two experimental temperatures to examine the role of temperature fluctuations and sex-specific selection, as well as the part that interactions between the two genomes play in shaping mtDNA variation. The results varied across populations and fitness components. In the majority of comparisons, they show that sympatric mitochondrial variants affect fitness. However, their effect should be examined in light of interactions with nuDNA, as mito-nuclear genotype was even more influential on fitness across all components. We found both sex-specific and temperature-specific differences in mitochondrial and mito-nuclear genotype ranks in all fitness components. The effect of temperature-specific selection was found to be more prominent, especially in desiccation resistance. From the results of different components tested, we can also infer that temperature-specific mito-nuclear interactions rather than sex-specific selection on mito-nuclear genotypes have a more substantial role in preserving mtDNA variation in this model species.

G × G × E effect on phenotype expression in a non-conventional model organism, the unicellular slime mould Physarum polycephalum

“…Nevertheless, despite the growing body of evidence that shows standing genetic variation in the mitochondrial genome accumulates via natural selection [18,[22][23][24], studies continue to assume strict neutrality of mitochondrial gene sequences. A possible reason for this salient omission could be that the mitonuclear effect on phenotypes is mostly reported in conventional model organisms, like fruit flies and beetles [8,16,17,25]. So the generality of the mitonuclear genetic effects must be tested across different models.…”

Developmental rate displays effects of inheritance but not of sex in inter-population hybrids ofTigriopus californicus

“…Similarly, variation in mitonuclear effects on developmental time between females and males is generally modest or absent in Drosophila sp. (Jelić et al, 2015; Mossman et al, 2016a; Erić et al, 2022) despite sex-specific effects of mitochondrial genotype on many other fitness-related traits when evaluated on common nuclear genetic backgrounds (Camus et al, 2012; Kurbalija Novičić et al, 2015; Nagarajan-Radha et al, 2019, 2020; Carnegie et al, 2021). Taken together, these results and our findings for T. californicus suggest that effects of mitonuclear incompatibilities on developmental rate may often be inconsistent with the expectations of the ‘mother’s curse’ hypothesis.…”

“…The heritability of this trait variation among hybrid individuals is potentially another important factor determining if mitonuclear incompatibilities can create strong barriers for gene flow between populations, and to our knowledge, the transmission of incompatibilities across generations has not been directly assessed. Additionally, it is possible for the effects of mitonuclear incompatibilities to vary between females and males (Jelić et al, 2015, Mossman et al, 2016b; Đorđević et al, 2017; Hoekstra et al, 2018, Carnegie et al, 2021; Erić et al, 2022), which may be the result of genetic interactions involving sex determining loci (e.g., heterologous sex chromosomes; Lopez et al, 2021), or of the predominantly maternal inheritance of mitochondrial DNA in metazoans (e.g., Giles et al, 1980). For example, the ‘mother’s curse’ hypothesis posits that mutations in mitochondrial DNA causing beneficial interactions in females will accumulate, even if they cause negative interactions in males, due to the lack of paternal transmission of mitochondrial DNA (Frank & Hurst, 1996; Gemmell et al, 2004).…”

Mapping mitonuclear epistasis using a novel recombinant yeast population

“…In humans, allelic variation in mitonuclear interactions contributes to human diseases [22][23][24][25][26]. Mitonuclear epistasis occurs within populations [27,28], between populations of the same species [15,[29][30][31][32][33][34][35] and between closely related species [17,36], suggesting that physiologically-relevant mitonuclear epistasis is ubiquitous in natural populations. Mitonuclear loci are clearly influencing phenotypes that shape the structure of natural populations and are important for understanding evolutionary and coevolutionary processes, including speciation.…”