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Due to the difficulty of simultaneously assessing variation in individual physiology, behaviour and fitness, we often know little about the mechanistic basis of life-history trade-offs and fitness variation. It is similarly challenging to examine how physiological variation in one individual has cascading fitness consequences for others in the social environment. Using a wild-living fish (ocellated wrasse, Symphodus ocellatus), we manipulated a neuropeptide pathway associated with courtship, aggression and parental care in vertebrates (arginine vasotocin, AVT) and directly examined the behavioural and fitness consequences. Nesting males injected with the AVT antagonist increased their paternal care, resulting in increased hatching of offspring and increased reproductive success of all individuals that mated at his nest. By directly examining physiology, behaviour and reproductive success, we revealed how a small change in individual physiology has clear and direct fitness consequences for multiple individuals. © 2019 The Association for the Study of Animal Behaviour
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While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. “Nesting males” provide parental care, defend territories and form cooperative associations with unrelated “satellites,” who cheat by sneaking fertilizations but help by reducing sperm competition from “sneakers” who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used “phenotypic engineering” that involved administering an androgen receptor antagonist (flutamide) to wild, free-living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down-regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite-directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms. © 2018 John Wiley & Sons Ltd