Social dominance and reproduction result in increased integration of oxidative state in males of an African cichlid fish

Abstract

Oxidative stress is a potential cost of social dominance and reproduction, which could mediate life history trade-offs between current and future reproductive fitness. However, the evidence for an oxidative cost of social dominance and reproduction is mixed, in part because organisms have efficient protective mechanisms that can counteract oxidative insults. Further, previous studies have shown that different aspects of oxidative balance, including oxidative damage and antioxidant function, varies dramatically between tissue types, yet few studies have investigated oxidative cost in terms of interconnectedness and coordination within the system. Here, we tested whether dominant and subordinate males of the cichlid Astatotilapa burtoni differ in integration of different components of oxidative stress. We assessed 7 markers of oxidative stress, which included both oxidative damage and antioxidant function in various tissue types (total of 14 measurements). Across all oxidative stress measurements, we found more co-regulated clusters in dominant males, suggesting that components of oxidative state are more functionally integrated in dominant males than they are in subordinate males. We discuss how a high degree of functional integration reflects increased robustness or efficiency of the system (e.g. increased effectiveness of antioxidant machinery in reducing oxidative damage), but we also highlight potential costs (e.g. activation of cytoprotective mechanisms may have unwanted pleiotropic effects). Overall, our results suggest that quantifying the extent of functional integration across different components of oxidative stress could reveal insights into the oxidative cost of important life history events.

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

“…Following a two-week stabilization period, we filmed each group three times a week for four weeks and recorded social behaviours of focal males (the dominant male and one randomly selected subordinate male in each tank) as previously described (Border et al, 2019; Fialkowski et al, 2021). Dominant males were brightly coloured, aggressive, defended a territory and actively courted females, whereas subordinates were visually drab, performed little-to-no aggression, did not court females, and spent large amounts of time shoaling (see Fialkowski et al, 2022). A single observer recorded the number of chases, lateral displays, border displays, courtship displays, and flees that each focal male performed, as well how much time each fish spent shoaling, during a five-minute period.…”

“…We measured a combination of these measures in the blood (DNA), plasma (ROMs, TAC, OXY, BAP), liver (DNA, NOX, TAC, SOD), and gonads (DNA, NOX, TAC, SOD) of all individuals. For a detailed description of the protocols used to measure these markers, see Fialkowski et al (2022).…”

“…The costs of being unable to acquire a territory appear high for subordinates because they usually have higher levels of the glucocorticoid hormone cortisol (Border et al 2019; Carpenter et al 2014; Fox et al 1997; Korzan et al 2014; but see Huffman et al 2015; Maruska et al 2013). However, dominant males have greater overall oxidative damage (Border et al, 2019; Fialkowski et al, 2021, 2022)—although this effect is highly tissue-specific—which likely reflects the high metabolic demands associated with reproduction and/or territory defense, as has been suggested in other vertebrates (Beaulieu et al, 2014; Cram et al, 2015; Dowling and Simmons, 2009; Georgiev et al, 2015b). Given these differences in hormone levels and the contrasting physiological demands associated with social rank in A. burtoni , we decided to probe whether the relationship between hormone levels and oxidative stress varies across social ranks.…”

“…While socially dominant individuals use aggression to acquire and maintain priority access to key limited resources—including food, shelter, and access to mates— subordinates may experience social suppression and limited access to these same resources (Clutton-Brock and Huchard, 2013; Milinski and Parker, 1991; Stockley and Bro-Jørgensen, 2011). Consequently, individuals of different social ranks tend to experience different levels of oxidative stress—the relative balance between the production of free radicals ( e.g ., reactive oxygen species (ROS)) and the neutralization of free radicals by antioxidant defenses (Monaghan et al, 2009; Pamplona and Costantini, 2011; Sies et al, 2017)—based on their social rank (Cram et al, 2015; Fialkowski et al, 2022; Losdat et al, 2019; Mendonça et al, 2020; Silva et al, 2018). Dominants tend to experience greater oxidative stress, especially when metabolic demands associated with reproduction and/or territory defense are high (Beaulieu et al, 2014; Cram et al, 2015; Dowling and Simmons, 2009; Georgiev et al, 2015b).…”

“…These lekking fish live in aggregations where males compete for spawning territories that are used to attract and mate with females (Fernald, 1977). Dominant males that monopolize these territories invest heavily in their reproductive system, having higher levels of androgens (e.g., testosterone) and larger gonads (Fialkowski et al, 2022; Maruska, 2014; Maruska and Fernald, 2011). Conversely, subordinate males that are unable to defend a territory maintain lower testosterone levels, have smaller gonads, and spend most of their time shoaling with females.…”