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.

自私遗传元件（Selfish genetic elements），如减数分裂驱动基因（meiotic drive genes），可通过偏向自身传递的方式扰乱孟德尔均等分离定律，且通常会对基因组其余部分造成损害。马来西亚柄眼蝇（Teleopsis dalmanni）的性比（SR）减数分裂驱动系统定位于X染色体上的一系列大型倒位区域内，该区域重组率较低，且与适合度的有害效应相关。本研究探究了减数分裂驱动对雌雄柄眼蝇代谢的影响。我们采用高分辨率O2k呼吸测定法结合整体生物呼吸测定法，获取线粒体功能与代谢速率相关数据。通过针对食物摄取的互补测定实验，明确了代谢对营养获取的下游效应。实验结果显示，携带SR减数分裂驱动元件的个体，其线粒体功能受损、ATP合成能力下降，具体表现为更低的呼吸控制比以及复合物I（Complex I）对呼吸作用的贡献减弱。驱动型个体的基础代谢率更高，且食物摄取量多于野生型（wild-type）个体。上述研究结果表明，驱动基因型在雌雄宿主中均会带来代谢成本。线粒体功能的紊乱可能通过提升基础代谢率与营养获取能力进行补偿。其潜在原因可能是承载减数分裂驱动元件的X染色体倒位区域积累了有害突变，而该区域受自然选择的作用较弱。在雌性个体中，驱动染色体呈现显性效应，单拷贝的驱动染色体即可造成显著的代谢损伤。未观察到雄性特有的代谢成本，也未发现驱动染色体对雌性代谢产生性拮抗效应（sexually antagonistic selection）的相关证据。上述结果提示，减数分裂驱动对精子发生（spermatogenesis）带来的直接代谢成本以及性拮抗选择的作用均相对较弱。本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，同时也提请关注自私遗传元件可能对宿主产生的更广泛生理效应。