Data from: Complex mitonuclear interactions and metabolic costs of mating in male seed beetles

The lack of evolutionary response to selection on mitochondrial genes through males predicts the evolution of nuclear genetic influence on male-specific mitochondrial function, for example by gene duplication and evolution of sex-specific expression of paralogs involved in metabolic pathways. Intergenomic epistasis may therefore be a prevalent feature of the genetic architecture of male-specific organismal function. Here, we assess the role of mitonuclear genetic variation for male metabolic phenotypes [metabolic rate and respiratory quotient (RQ)] associated with ejaculate renewal, in the seed beetle Callosobruchus maculatus, by assaying lines with crossed combinations of distinct mitochondrial haplotypes and nuclear lineages. We found a significant increase in metabolic rate following mating relative to virgin males. Moreover, processes associated with ejaculate renewal showed variation in metabolic rate that was affected by mitonuclear interactions. Mitochondrial haplotype influenced mating-related changes in RQ, but this pattern varied over time. Mitonuclear genotype and the energy spent during ejaculate production affected the weight of the ejaculate, but the strength of this effect varied across mitochondrial haplotypes showing that the genetic architecture of male-specific reproductive function is complex. Our findings unveil hitherto underappreciated metabolic costs of mating and ejaculate renewal, and provide the first empirical demonstration of mitonuclear epistasis on male reproductive metabolic processes.

雄性介导的线粒体基因选择缺乏进化响应，这一现象可预测核遗传对雄性特异性线粒体功能的演化调控模式，例如通过基因重复以及参与代谢通路的旁系同源基因的性别特异性表达演化而来。因此，基因组间上位性（intergenomic epistasis）或许是雄性特异性机体功能遗传结构的普遍特征。本研究以绿豆象（Callosobruchus maculatus）为实验材料，通过构建具有不同线粒体单倍型与核谱系杂交组合的实验品系，探究线粒体核遗传变异（mitonuclear genetic variation）在与精液更新相关的雄性代谢表型[代谢率及呼吸商（respiratory quotient, RQ）]中的调控作用。我们发现，与处女雄虫相比，交配后的雄虫代谢率显著升高。此外，与精液更新相关的生理过程表现出代谢率变异，且该变异受线粒体核互作（mitonuclear interactions）调控。线粒体单倍型会影响交配相关的呼吸商变化，但这一模式随时间进程发生改变。线粒体核基因型（mitonuclear genotype）以及精液产生过程中消耗的能量均会影响射精产物重量，但该效应的强度因线粒体单倍型而异，这表明雄性特异性生殖功能的遗传结构较为复杂。本研究揭示了此前未被充分重视的交配与精液更新的代谢成本，并首次通过实验证实了线粒体核上位性（mitonuclear epistasis）对雄性生殖代谢过程的调控作用。