The metabolic cost of meiotic drive

Selfish genetic elements, such as meiotic drive genes, disrupt Mendel's law of equal segregation by biasing their own transmission, often at a detriment to the rest of the genome. The Malaysian stalk-eyed fly (Teleopsis dalmanni) sex-ratio (SR) meiotic drive system is located within a series of large inversions on the X chromosome subject to low recombination and is associated with deleterious effects on fitness. Here we examine the metabolic effects of meiotic drive across male and female stalk-eyed flies. High-resolution O2k respirometry coupled with whole-organism respirometry were used to obtain mitochondrial function and metabolic rates. Complimentary assays on food consumption established downstream effects of metabolism on nutrient acquisition. The experiments demonstrate that individuals with SR meiotic drive elements have impaired mitochondrial function and reduced capacity for ATP synthesis, as shown by a lower respiratory control ratio and weaker contribution of Complex I to respiration. Drive individuals also exhibited an increased basal metabolic rate and consumed a greater amount of food than wild-type individuals. These findings show that the drive genotype imposes metabolic costs in both male and female hosts. The disruption in mitochondrial function likely leads to compensation via an increase in both basal metabolic rate and nutrient acquisition. A potential cause lies in the accumulation of deleterious mutations in the inversions on the X chromosome that house the meiotic drive, which are subject to weak natural selection. In females, the drive chromosome has a dominant effect, with a single copy causing substantial metabolic compromise. There was little evidence of male-specific metabolic costs, nor evidence of an accumulation of sexually antagonistic effects of drive chromosomes on female metabolism. These results suggest that direct metabolic costs from meiotic drive on spermatogenesis and from sexually antagonistic selection are relatively weak. This research provides new insight into the interplay between meiotic drive and metabolism, drawing attention to the broader physiological repercussions selfish genetic elements may have on their hosts.

自私遗传因子，如减数分裂驱动基因，通过偏袒自身的传递，破坏了孟德尔等位基因分离定律，通常对整个基因组造成损害。马来西亚长眼飞蝇（Teleopsis dalmanni）的性别比例（SR）减数分裂驱动系统位于X染色体上的一系列大型倒位之中，这些倒位具有低重组率，并与适应性有害效应相关。本研究旨在探讨减数分裂驱动对雄性和雌性长眼飞蝇的代谢效应。通过高分辨率O2k呼吸代谢率和整个有机体呼吸代谢率相结合的方法，获得了线粒体功能和代谢速率。对食物消耗的互补实验建立了代谢对营养获取的下游效应。实验表明，具有SR减数分裂驱动基因的个体表现出受损的线粒体功能和减少的ATP合成能力，这体现在较低的呼吸控制比和Complex I对呼吸的较弱贡献。驱动个体还表现出较高的基础代谢率和比野生型个体消耗更多的食物。这些发现表明，驱动基因型对雌性和雄性宿主都造成了代谢成本。线粒体功能的破坏可能导致通过增加基础代谢率和营养获取来进行补偿。潜在的原因在于携带减数分裂驱动的X染色体倒位中累积了有害突变，这些突变受到较弱的自然选择。在雌性中，驱动染色体具有显性效应，单拷贝即可导致显著的代谢损害。在雄性中，几乎没有发现特定的代谢成本，也没有发现驱动染色体对雌性代谢的性对抗效应积累。这些结果提示，来自减数分裂驱动对精子发生和性对抗选择的直接代谢成本相对较弱。这项研究为减数分裂驱动与代谢之间的相互作用提供了新的见解，引起了人们对自私遗传因子对其宿主可能产生的更广泛生理影响的关注。