Maintenance costs of male dominance and sexually antagonistic selection in the wild

1. Variation in dominance status determines male mating and reproductive success, but natural selection for male dominance can be detrimental or antagonistic for female performance, and ultimately their fitness. Attaining and maintaining a high dominance status in a population of competing individuals is physiologically costly for males. But how male dominance status is mediated by maintenance energetics is currently not well understood, nor are the correlational effects of male energetics on his sisters recognized. 2. We conducted laboratory and field experiments on rodent populations to test whether selective breeding for male dominance status (dominant vs. subordinate breeding lines) antagonistically affected basal metabolic rate (BMR) and fitness of females in the wild conditions. 3. Our results showed elevated BMR in females, but not in males, from the dominant breeding line. However, phenotypically dominant males from the subordinate breeding line had the highest BMR. 4. Males from the dominant line with low BMR sired the most litters and offspring in the field. Similarly, females from the dominant selection line tended to have more offspring if they had lower BMR, while the opposite trend was found in females from the subordinate selection line. The highest probability to reproduce had females of both high and low BMR, as indicated by significant quadratic selection gradient. 5. The increased female BMR resulting from selection for male dominance suggests genetic incompatibility between sexes in metabolism inheritance. Elevated BMR in behaviourally dominant males, but not in males from the dominant breeding line, suggests physiological costs in males not genetically suited for dominance. 6. Fitness costs of elevated maintenance costs (measured as BMR) shown here support the energetic compensation hypothesis where high BMR is selected against as it would trade-off energy required for other important life functions.

1. 雄性的优势地位差异决定其交配与繁殖成功率，但针对雄性优势地位的自然选择，可能对雌性的生存表现乃至整体适合度产生有害或拮抗效应。在竞争种群中，获得并维持较高的优势地位对雄性而言存在显著生理代价。然而目前学界对雄性优势地位如何受维持能量代谢（maintenance energetics）调控尚不清楚，同时也未充分认识到雄性能量代谢对其雌性同胞的关联效应。
2. 我们以啮齿动物种群为对象开展实验室与野外实验，旨在验证针对雄性优势地位的选择育种（selective breeding，分为优势繁殖系与从属繁殖系）是否会在野外条件下对雌性的基础代谢率（basal metabolic rate, BMR）与适合度产生拮抗效应。
3. 我们的研究结果显示，来自优势繁殖系的雌性个体基础代谢率显著升高，而雄性个体未出现该现象；但来自从属繁殖系的表型优势雄性，其基础代谢率最高。
4. 来自优势繁殖系且基础代谢率较低的雄性个体，在野外环境中能产下最多胎次与后代。类似地，来自优势选择系的雌性个体，若其基础代谢率较低，后代数量往往更多；而来自从属选择系的雌性个体则呈现相反趋势。显著的二次选择梯度（quadratic selection gradient）表明，基础代谢率极高与极低的雌性个体，其繁殖概率最高。
5. 雄性优势选择育种导致雌性基础代谢率升高，这提示代谢遗传层面存在两性遗传不相容性。行为优势雄性的基础代谢率升高，但优势繁殖系的雄性未出现该现象，这表明非遗传适配优势地位的雄性需承担额外生理代价。
6. 本研究揭示的维持成本（以基础代谢率衡量）升高带来的适合度代价，支持能量补偿假说：即基础代谢率过高会与其他重要生命功能所需的能量产生权衡，因此会遭到自然选择的抑制。