Abstract

Dominant individuals have priority access to mates and resources. However, high rank can be costly too, especially when it is maintained by intense agonistic behavior. Oxidative stress has been proposed as a potential cost of social dominance. However, social dominance hierarchies can be dynamic, and few studies have examined the cost of social dominance when males are changing status. We studied temporal changes in markers of oxidative stress during social ascent in the East African cichlid fish Astatotilapia burtoni. After removing the dominant male, males ascended from subordinate to dominant status. On the first day of social ascent, immediately after the dominant male removal, the newly dominant male showed lower levels of plasma total antioxidant capacity (TAC). However, we found that liver TAC and liver superoxide dismutase (SOD), an enzymatic antioxidant, were significantly upregulated on day 1 and 2 of social ascent, respectively. No temporal variation in nicotinamide adenine dinucleotide phosphate-oxidase (NADPH-oxidase) activity, blood DNA damage, and liver DNA damage was observed. By day 14, all markers of oxidative stress were similar to those observed in stable dominant males, which had higher levels of reactive oxygen metabolites (ROM) compared to subordinate males. We conclude that markers of oxidative stress vary dramatically during social ascent in a time- and tissue-dependent manner. Our study provides a more nuanced look at the oxidative cost of social dominance and highlights the importance of considering temporal changes in markers of oxidative stress during important life-history events.

Significance statement

High social status gives priority access to resources but also entails costs. Since dominant individuals tend to have higher metabolic rates, oxidative stress could be a potential cost of high social status. Oxidative stress can occur when reactive oxygen species, produced during metabolic activities, cannot be effectively neutralized by antioxidants, leading to oxidative cellular damage. Social hierarchies can be dynamic, yet how the cost of rank varies when males are changing social status is unknown. We allowed subordinate males to ascend to dominant status in the cichlid fish Astatotilapia burtoni. At the beginning of social ascent when males suddenly increase aggressive behavior, the total antioxidant defense was lower in blood plasma, as expected, when males suddenly increase their metabolism during aggressive interactions. However, antioxidant defense was increased in the liver suggesting that males can compensate for the potential cost of becoming dominant. Circulating reactive oxygen metabolites gradually increased over time reaching levels similar to stable dominant males, possibly due to males upregulating their reproductive axis. Our results highlight that markers of oxidative stress can vary dramatically over time during important events in life.

中文翻译：

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根本性变化：主导阶层中社会提升期间氧化应激的时间模式

摘要

占主导地位的个人具有优先选择伙伴和资源的权限。但是，高等级也很昂贵，尤其是当激烈的激动行为维持高等级时。已经提出氧化应激是社会支配的潜在成本。但是，社会支配等级可以是动态的，很少有研究检查男性改变身份时社会支配的成本。我们在东非的社会上升过程中研究了氧化应激标志物随时间的变化丽鱼伯氏妊丽鱼。除去优势男性后，男性从从属地位升为优势地位。在社交活动的第一天，雄性雄性被移除后，刚出现显性雄性的男性血浆总抗氧化能力（TAC）降低。但是，我们发现在社交活动的第1天和第2天，肝脏TAC和肝脏超氧化物歧化酶（SOD）（一种酶促抗氧化剂）分别显着上调。没有观察到烟酰胺腺嘌呤二核苷酸磷酸氧化酶（NADPH-氧化酶）活性，血液DNA损伤和肝DNA损伤的时间变化。到第14天，所有氧化应激指标都与稳定的显性雄性中观察到的相似，与下级雄性相比，其具有更高的活性氧代谢产物（ROM）水平。我们得出结论，在社会上升期间，氧化应激的标志物以时间和组织依赖性的方式发生显着变化。我们的研究对社会支配性的氧化成本提供了更为细致入微的观察，并强调了在重要的生命历史事件中考虑氧化应激标志物随时间变化的重要性。

重要性声明

较高的社会地位使人们可以优先获得资源，但也要付出成本。由于显性个体倾向于具有较高的新陈代谢率，因此氧化应激可能是较高社会地位的潜在代价。当在代谢活动中产生的活性氧不能被抗氧化剂有效中和时，就会发生氧化应激，从而导致氧化性细胞损伤。社会等级制度可以是动态的，但是当男性改变社会地位时，等级成本如何变化尚不得而知。我们允许下属雄性在丽鱼科鱼淡色无刺鱼中上升为优势地位。在社交活动开始时，当雄性突然增加攻击行为时，血浆中的总抗氧化防御能力就降低了，这是预期的，当雄性在交互作用过程中突然增加新陈代谢时。但是，肝脏中抗氧化剂的防御能力增强，这表明雄性可以弥补成为优势的潜在成本。循环中的活性氧代谢产物随时间逐渐增加，达到与稳定雄性雄性相似的水平，这可能是由于雄性上调了其生殖轴而引起的。我们的结果表明，在生活中的重要事件中，氧化应激的标志物会随着时间而发生巨大变化。