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Darwin, L. J.

Publications and source records attributed to Darwin, L. J..

3 recordsLinked to original sources

Do divergent mitochondrial backgrounds alter the fate of nuclear alleles during hybridization and admixture?

Hybridization brings together genetic variation from different populations or species into admixed genomes. As selection sorts this variation, the fate of each allele is determined by its fitness effect in the new hybrid genomic background. Because mitochondrial genes coevolve with the nuclear genome, they may be especially sensitive to foreign nuclear backgrounds, making them potential "hot-spots" for hybrid incompatibilities. Here, we test whether selection against mitonuclear incompatibilities drives repeatable hybridization outcomes. Specifically, we experimentally evolved three sets of five populations of hybrid Drosophila melanogaster, each carrying the same nuclear chromosomes but paired with one of three increasingly divergent mitochondrial DNA backgrounds. We hypothesized that accumulated incompatibilities would result in different patterns of nuclear admixture among mitochondrial backgrounds. To test this, we tracked nuclear allele frequencies in all 15 populations by whole-genome sequencing at intermediate time points. After 25 generations, we observed that rapid genomic evolution produced a strikingly parallel mosaic of both nuclear ancestries, independent of mitochondrial background. Contrary to our hypothesis, we found no evidence that mitochondrial background1 shaped nuclear admixture, even for interspecific combinations. These results suggest that in species with large effective population sizes, efficient purifying selection limits the accumulation of mitonuclear incompatibilities, allowing selection on nuclear alleles to promote repeatable ancestry sorting immediately following hybridization.

evolutionary biology↗

Absence of Mothers Curse for performance traits among divergent mtDNAs in heterozygous nuclear backgrounds in Drosophila

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 phenotypic variation should be more common among males than among females, a pattern referred to as Mothers Curse (MC). Most studies of MC place alternative mtDNAs on common homozygous nuclear chromosomal backgrounds, a condition not common in nature. Moreover, it is not known whether MC effects accumulate as mtDNAs acquire nucleotide substitutions between populations or species. We tested the MC hypothesis using mtDNAs from Drosophila melanogaster (OreR, Zimbabwe or w1118), D. simulans (siI and siII) and D. yakuba each placed on several D. melanogaster nuclear backgrounds heterozygous for different chromosomal deficiencies paired with a common w1118 chromosome set. Females and males were tested for starvation resistance, climbing speed, and flight performance. In the majority of chromosomal backgrounds the variance among mtDNA genotypes was greater in females than in males, opposite from the central prediction of Mothers Curse. This suggests that additive and dominance variation across the nuclear genome may provide nuclear blessings that can counter the curse of maternally inherited mtDNA. Teaser textMothers Curse (MC) posits that selection on mtDNA should be stronger in females than in males due to maternal inheritance of mtDNA. This predicts that phenotypic variation among mtDNA genotypes should be lower for females and higher for males. There is conflicting experimental evidence for MC. Most studies of MC have used a common, homozygous nuclear background and have not explored the influence of divergent mtDNAs as strong predictors of MC effects. We address both issues by assaying performance traits among mtDNAs of varying levels of divergence on heterozygous backgrounds. The data fail to support the MC hypothesis and even reveal the opposite effect that females have greater phenotypic variation across mtDNAs. MC may operate in some contexts, but it is not a consistent force in evolutionary genetics.

evolutionary biology↗

Genetic and environmental interactions outweigh mitonuclear coevolution for complex traits in Drosophila

The interdependent relationship between mitochondrial and nuclear genomes is a powerful model for understanding how epistasis shapes the architecture and evolution of complex traits. Once considered a neutral marker, mitochondrial DNA variation is now recognized as critical to phenotypic evolution because of its epistatic interactions and history of coevolution with the nuclear genome. A central challenge in evolutionary genetics is to quantify the relative importance of stabilizing and directional selection shaping complex trait distributions within and among species. Both can act on interacting and/or co-evolving genes contributing to quantitative traits, but resolving their relative roles is complicated by the complex architecture of most traits. Here, we use a panel of 90 Drosophila mitonuclear genotypes to quantify the relative contributions of mitochondrial, nuclear, and environmental variation and their interactions to four metabolically demanding complex traits. We sample both within-species and between-species mitochondrial variation and observe stronger interaction effects attributable to within-species variation, consistent with stabilizing selection maintaining mitonuclear function. Additionally, culturing the flies on a mitochondrial Complex I inhibitor, rotenone, reveals significant genotype x environment (GxE and GxGxE) interaction effects, providing insight into how genetic variation can be maintained across changing environments. Our results have broader implications in medicine, where mitochondrial DNA donors with longer purifying selection histories may be safer for mitochondrial replacement therapies.

evolutionary biology↗