Testosterone causes pleiotropic effects on cleanerfish behaviour

Abstract

Mathematical modelling regarding evolutionary theory typically assumes that optimal strategies are not constrained through mechanistic processes. In contrast, recent studies on brain anatomy and neurobiology suggest that flexibility in social behaviour is rather constrained by the physiological state of the social decision-making network. Changing its state may yield selective advantages in some social contexts but neutral or even detrimental effects in others. Here we provide field evidence for such physiological trade-offs. We subjected wild female cleaner wrasse to injections of testosterone or of saline solution (control) and then observed both intraspecific interactions and interspecific cleaning behaviour with other reef fish, referred to as clients. Testosterone-treated females intensified intraspecific social interactions, showing more aggression towards smaller females and tendencies of increased aggressive and affiliative contacts with dominant males. Such testosterone-mediated changes fit the hypothesis that an increase in testosterone mediates female’s focus on status in this protogynous hermaphrodite species, where females eventually change sex to become males. Moreover, we also identified other effects on interspecific social interactions: testosterone-treated females interacted less with client reef fishes and hence obtained less food. Most importantly, they selectively reduced service quality for species that were less likely to punish after being cheated. Overall, our findings suggest that testosterone causes pleiotropic effects on intra and interspecific social behaviour by broadly influencing female cleaners’ decision-making.

Effects of local versus global competition on reproductive skew and sex differences in social dominance behaviour

“…They forage by removing ectoparasites from other fish, socalled clients [37], and are organized into dominance hierarchies of females and a top-ranking male that has undergone sex reversal [38]. The study [36] found that testosterone-injected females increased their aggression towards subordinate females and spent less time interacting with clients, which supports our model assumptions. In general, cleaner fish, could be an example where female competition is relatively close to global, because they forage on non-monopolizable resources (clients) and reproduce through pelagic eggs.…”

“…Hormonal manipulation is another way to examine such a trade-off, and this has been performed on cleaner fish in the wild [36]. Cleaner fish ( Labroides dimidiatus ) live on coral reefs.…”

Effects of local versus global competition on reproductive skew and sex differences in social dominance behaviour

“…They forage by removing ectoparasites from other fish, so-called clients [33], and are organised into dominance hierarchies of females and a top-ranking male that has undergone sex reversal [34]. The study [32] found that testosterone-injected females increased their aggression towards subordinate females and spent less time interacting with clients, which supports our model assumptions. In general, cleaner fish, could be an example where female competition is relatively close to global, because they forage on non-monopolisable resources (clients) and reproduce through pelagic eggs.…”

“…Hormonal manipulation is another way to examine such a trade-off, and this has been performed on cleaner fish in the wild [32]. Cleaner fish ( Labroides dimidiatus ) live on coral reefs.…”

The interplay between satiation and temptation drives cleaner fish Labroides dimidiatus foraging behaviour and service quality towards client reef fish

“…In general, increased parasite load should make clients more tolerant, but the exact function may vary between species for various reasons (e.g. differences in manoeuvrability; Roche et al 2021, or punishment being co-opted by intraspecific aggressiveness; Soares et al 2019). As a consequence, the model predicts that satiated cleaner fish may behave more cooperatively towards more 'cautious' client species and more exploitative towards more 'easygoing' client species (Triki et al 2022).…”