Radical change: temporal patterns of oxidative stress during social ascent in a dominance hierarchy

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.