Social rank influences relationships between hormones and oxidative stress in a cichlid fish

Abstract

An individual's social environment can have widespread effects on their physiology, including effects on oxidative stress and hormone levels. Many studies have posited that variation in oxidative stress experienced by individuals of different social ranks might be due to endocrine differences, however, few studies have evaluated this hypothesis. Here, we assessed whether a suite of markers associated with oxidative stress in different tissues (blood, plasma, liver, or gonads) had social rank-specific relationships with circulating testosterone or cortisol levels in males of a cichlid fish,Astatotilapia burtoni. Across all fish, blood DNA damage (a global marker of oxidative stress) and gonadal synthesis of reactive oxygen species (as indicated by NADPH-oxidase (NOX) activity) were lower when testosterone was high. High DNA damage in both the blood and gonads was associated with high cortisol in subordinates, but low cortisol in dominants. Additionally, high cortisol was associated with greater production of reactive oxygen species (greater NOX activity) in both the gonads (dominants only) and liver (dominants and subordinates). In general, high testosterone was associated with lower oxidative stress across both social ranks, whereas high cortisol was associated with lower oxidative stress in dominants and higher oxidative stress in subordinates. Taken together, our results show that differences in the social environment can lead to contrasting relationships between hormones and oxidative stress.

Teleosts as behaviour test models for social stress

“…Social defeat paradigms are used to study the effects of antagonism by a more dominant conspecific or to observe the differences between dominant-subordinate fish. Various studies simply pair two fish of the same sex together, or form a small mixed sex group of fish, allowing them to interact and develop a social hierarchy (Larson et al, 2006;Filby et al, 2010;Dahlbom et al, 2011;Pavlidis et al, 2011;Tea et al, 2019;Bozi et al, 2021;Culbert et al, 2023). Dominant or subordinate fish are distinguished by their behaviour.…”

“…Dominant or subordinate fish are distinguished by their behaviour. Typically, dominant display far more aggressive behaviour, shown by chasing or biting behaviour towards subordinates, are often bigger in size, and in some species, may have a brighter body colouration, as observed in the Nile tilapia and Astatotilapia burtoni (Lim et al, 2020;Culbert et al, 2023). Dominants are less likely to show anxiety-like behaviour once they have obtained dominancy, and occupies a large territory, often in the middle of the tank.…”

“…Subordinates are more likely to spend time fleeing from dominants and showcase less aggressive behaviours altogether. Many of these studies observed that a social hierarchy is formed early after initial pairing and the hierarchy is preserved for up to 5 days with no changes to social rank (Larson et al, 2006;Filby et al, 2010;Dahlbom et al, 2011;Pavlidis et al, 2011;Bozi et al, 2021;Culbert et al, 2023). This meant that once dominancy or subordinacy is established, is it less likely that the social rank will change after, particularly in experimental settings.…”