School of Biological Sciences, Monash University, Clayton, VIC, Australia.
Faculty of Biology, Applied Zoology, TU Dresden, Dresden, Germany.
J Evol Biol. 2020 May;33(5):694-713. doi: 10.1111/jeb.13605. Epub 2020 Mar 2.
Genetic variation outside of the cell nucleus can affect the phenotype. The cytoplasm is home to the mitochondria, and in arthropods often hosts intracellular bacteria such as Wolbachia. Although numerous studies have implicated epistatic interactions between cytoplasmic and nuclear genetic variation as mediators of phenotypic expression, two questions remain. Firstly, it remains unclear whether outcomes of cyto-nuclear interactions will manifest differently across the sexes, as might be predicted given that cytoplasmic genomes are screened by natural selection only through females as a consequence of their maternal inheritance. Secondly, the relative contribution of mitochondrial genetic variation to other cytoplasmic sources of variation, such as Wolbachia infection, in shaping phenotypic outcomes of cyto-nuclear interactions remains unknown. Here, we address these questions, creating a fully crossed set of replicated cyto-nuclear populations derived from three geographically distinct populations of Drosophila melanogaster, measuring the lifespan of males and females from each population. We observed that cyto-nuclear interactions shape lifespan and that the outcomes of these interactions differ across the sexes. Yet, we found no evidence that placing the cytoplasms from one population alongside the nuclear background of others (generating putative cyto-nuclear mismatches) leads to decreased lifespan in either sex. Although it was difficult to partition mitochondrial from Wolbachia effects, our results suggest at least some of the cytoplasmic genotypic contribution to lifespan was directly mediated by an effect of sequence variation in the mtDNA. Future work should explore the degree to which cyto-nuclear interactions result in sex differences in the expression of other components of organismal life history.
细胞核外的遗传变异会影响表型。细胞质中含有线粒体，节肢动物的细胞质中通常还含有沃尔巴克氏体等胞内细菌。尽管许多研究表明细胞质和核遗传变异之间的上位性相互作用是表型表达的中介，但仍存在两个问题。首先，细胞质基因组仅通过雌性进行自然选择筛选，因为它们是母系遗传的，因此细胞质和核相互作用的结果是否会在两性之间表现出不同，这一点尚不清楚。其次，线粒体遗传变异对其他细胞质来源（如沃尔巴克氏体感染）的变异对塑造细胞质和核相互作用的表型结果的相对贡献仍不清楚。在这里，我们通过从三个不同地理种群的黑腹果蝇中创建完全交叉的复制细胞质核种群来解决这些问题，测量每个种群中雄性和雌性的寿命。我们观察到细胞质和核相互作用会影响寿命，并且这些相互作用的结果在两性之间存在差异。然而，我们没有发现将一个种群的细胞质与其他种群的核背景（产生潜在的细胞质核不匹配）放在一起会导致两性寿命缩短的证据。尽管很难将线粒体和沃尔巴克氏体的作用分开，但我们的结果表明，至少部分细胞质基因型对寿命的影响是由 mtDNA 序列变异直接介导的。未来的工作应该探索细胞质和核相互作用在多大程度上导致生物体生活史的其他组成部分在两性之间表达的差异。
