Glucocorticoids do not promote prosociality in a wild group-living fish

Highlights

• We investigated whether glucocorticoids promote prosociality in a group-living fish.

• We assessed how injection of saline or cortisol influenced prosocial behaviours.

• Cortisol treatment reduced affiliative behaviours in subordinate females.

• Cortisol treatment did not affect submissive or helping behaviours.

• Glucocorticoids may not directly promote prosociality in group-living fishes.

Abstract

Individuals often respond to social disturbances by increasing prosociality, which can strengthen social bonds, buffer against stress, and promote overall group cohesion. Given their importance in mediating stress responses, glucocorticoids have received considerable attention as potential proximate regulators of prosocial behaviour during disturbances. However, previous investigations have largely focused on mammals and our understanding of the potential prosocial effects of glucocorticoids across vertebrates more broadly is still lacking. Here, we assessed whether experimentally elevated glucocorticoid levels (simulating endogenous cortisol responses mounted following disturbances) promote prosocial behaviours in wild groups of the cichlid fish, Neolamprologus pulcher. Using SCUBA in Lake Tanganyika, we observed how subordinate group members adjusted affiliation, helping, and submission (all forms of prosocial behaviour) following underwater injections of either cortisol or saline. Cortisol treatment reduced affiliative behaviours—but only in females—suggesting that glucocorticoids may reduce overall prosociality. Fish with elevated glucocorticoid levels did not increase performance of submission or helping behaviours. Taken together, our results do not support a role for glucocorticoids in promoting prosocial behaviour in this species and emphasize the complexity of the proximate mechanisms that underlie prosociality.

Introduction

Maintaining stability in social groups is a key way to increase the benefits associated with group-living, such as workload sharing (Clutton-Brock et al., 2002; Ulrich et al., 2018), improved foraging (Evans et al., 2016; Ward and Zahavi, 1973), and increased vigilance (Evans et al., 2016; Roberts, 1996). While group stability is often maintained via the formation of social hierarchies, instability within groups can arise from changes in group composition or as a result of fluctuations in resource availability (Creel et al., 2013; Culbert et al., 2018). Following such disturbances, group members will often increase their performance of prosocial behaviours that promote stability within the group. Specifically, the performance of affiliative behaviours—a type of prosocial behaviour that reinforces social bonds—often increases following a disturbance (Anderson et al., 2020; Buchanan and Preston, 2014; Fraser et al., 2008; Radford, 2008). Such responses are thought to play an important role in the persistence and stability of social groups, yet the proximate mechanisms regulating these responses are not well understood. Because glucocorticoids help to coordinate behavioural and physiological responses during periods of stress (Creel et al., 2013; Raulo and Dantzer, 2018; Tort and Teles, 2011), these hormones have been hypothesized to be involved in the regulation of prosocial behaviours during periods of instability.

Glucocorticoid synthesis increases when individuals encounter physical or psychological challenges in their surrounding environment (i.e. a stressor) and elevated glucocorticoid levels help individuals overcome challenges primarily through their effects on metabolism, osmoregulation, and immune function (Mommsen et al., 1999; Sapolsky et al., 2000; Tort and Teles, 2011). Production of glucocorticoids is regulated by the hypothalamic-pituitary-adrenal (HPA) axis in mammals and birds, or by the hypothalamic-pituitary-interrenal (HPI) axis in other vertebrates (Dallman et al., 1994; José et al., 2011; Wendelaar Bonga, 1997). Following the perception of a stressor, hypothalamic neurons release corticotropin-releasing factor causing corticotropes located in the anterior pituitary to release adrenocorticotropic hormone into circulation (Aguilera, 1998; Bernier et al., 2009). Adrenocorticotropic hormone then binds melanocortin receptor 2 located on the adrenals or interrenal tissue and stimulates glucocorticoid synthesis from precursory cholesterol (Fridmanis et al., 2017; Payne and Hales, 2004; Tokarz et al., 2015). Glucocorticoid levels can be affected by an individual's social environment (Creel et al., 2013; Gilmour et al., 2005), and the presence of an individual's social partners can even reduce glucocorticoid production following a stressor (Culbert et al., 2019; Smith and Wang, 2014). This ‘social buffering’ of glucocorticoid synthesis is often associated with increased prosocial behaviours (Kiyokawa and Hennessy, 2018); however, whether glucocorticoids themselves regulate the performance of prosocial behaviours is less clear (Raulo and Dantzer, 2018). While there is evidence that glucocorticoids can promote prosociality in mammals (Dantzer et al., 2017; Santema et al., 2013; Voellmy et al., 2014) and in birds (Thierry et al., 2014), there have been few investigations of the potential prosocial role of glucocorticoids in other vertebrate groups. Thus, to determine whether the prosocial effects of glucocorticoids are broadly evolutionarily conserved across vertebrates, studies in other animals—such as fishes—are critical.

To test the hypothesis that glucocorticoids promote prosocial behaviours in fishes, we assessed how the behaviour of subordinate group members of the cooperatively breeding cichlid—Neolamprologus pulcher—changed following treatment with either saline or cortisol (to simulate endogenous cortisol responses mounted following disturbances). These fish live in social groups containing a dominant breeding pair and up to 20 subordinates that help the dominant pair by performing brood care and territory defense (Taborsky and Limberger, 1981; Wong and Balshine, 2011). Previous studies conducted on laboratory populations of N. pulcher suggest that glucocorticoids are involved with the development of social competency (Nyman et al., 2018; Reyes-Contreras et al., 2019; Taborsky et al., 2013), and circulating glucocorticoid levels often vary between dominants and subordinates (Culbert et al., 2018; Mileva et al., 2009). However, no study has assessed the potential role of glucocorticoids in regulating social behaviour of N. pulcher under ecologically relevant conditions encountered in the field. Therefore, we performed our experiments using wild N. pulcher located on the southern tip of Lake Tanganyika in Africa. These fish perform a suite of prosocial behaviours, including affiliation, helping, and submission; however, whether cortisol directly regulates these behaviours has not been examined. Helping and submissive behaviours have been proposed as a means of appeasing dominants, decreasing aggression, and maintaining group stability (Bergmüller et al., 2005b; Bergmüller and Taborsky, 2005; Reddon et al., 2019). Additionally, N. pulcher regularly perform affiliative behaviours towards their groupmates which reinforce social relationships and promote cooperation (Anderson et al., 2020; Bruintjes et al., 2016). As such, we predicted that individuals that were treated with cortisol would perform more affiliative, helping, and submissive acts compared to individuals treated with saline.