While systemic steroid hormones are known to regulate reproductive behaviour, the actual mechanisms of steroidal regulation remain largely unknown. Steroidogenic enzyme activity can rapidly modulate social behaviour by influencing neurosteroid production. In fish, the enzyme 11b-hydroxysteroid dehydrogenase (11b-HSD) synthesizes 11-ketotestosterone (KT, a potent teleost androgen) and deactivates cortisol (the primary teleost glucocorticoid), and both of these steroid hormones can regulate behaviour. Here, we investigated the role of neurosteroidogenesis in regulating parenting in a haremic bidirectionally hermaphroditic fish, Lythrypnus dalli, where males provide all requisite parental care. Using an in vitro assay, we found that an 11b-HSD inhibitor, carbenoxolone (CBX), reduced brain and testicular KT synthesis by 90% or more. We modulated neurosteroid levels in parenting males via intracerebroventricular injection of CBX. Within only 20 min, CBX transiently eliminated parenting behaviour, but not other social behaviour, suggesting an enzymatic mechanism for rapid neurosteroidal regulation of parenting. Consistent with our proposed mechanism, elevating KT levels rescued parenting when paired with CBX, while cortisol alone did not affect parenting. Females paired with the experimental males opportunistically consumed unattended eggs, which reduced male reproductive success by 15%, but some females also exhibited parenting behaviour and these females had elevated brain KT. Brain KT levels appear to regulate the expression of parenting behaviour as a result of changes in neural 11b-HSD activity.

In many social species, there are important connections between social behaviour and reproduction that provide critical insights into the evolution of sociality. In this study, we describe associations between agonistic behaviour and male reproductive success in stable social groups of bluebanded gobies (Lythrypnus dalli). This highly social, sex-changing species forms linear hierarchies of a dominant male and multiple subordinate females. Males reproduce with each female in the harem and care for the eggs. Since aggression tends to be associated with reduced reproduction in social hierarchies, we hypothesized that males in groups with high rates of aggression would fertilise fewer eggs. We also hypothesized that a male’s agonistic behaviour would be associated with his reproductive success. Dominants often exert substantial control over their harem, including control over subordinate reproduction. To address these hypotheses, we quantified egg laying/fertilisation over 13 days and observed agonistic behaviour. We show that there was a significant, negative association between male reproductive success and the total rate agonistic interactions by a group. While no male behaviours were associated with the quantity of eggs fertilised, female agonistic behaviour may be central to male reproductive success. We identified a set of models approximating male reproductive success that included three female behaviours: aggression by the highest-ranking female and approaches by the lowest-ranking female were negatively associated with the quantity of eggs fertilised by males in their groups, but the efficiency with which the middle-ranking female displaced others was positively associated with this measure. These data provide a first step in elucidating the behavioural mechanisms that are associated with L. dalli reproductive success.

While individual variation in social behaviour is ubiquitous and causes social groups to differ in structure, how these structural differences affect fitness remains largely unknown. We used social network analysis of replicate bluebanded goby (Lythrypnus dalli) harems to identify the reproductive correlates of social network structure. In stable groups, we quantified agonistic behaviour, reproduction and steroid hormones, which can both affect and respond to social/reproductive cues. We identified distinct, optimal social structures associated with different reproductive measures. Male hatching success (HS) was negatively associated with agonistic reciprocity, a network structure that describes whether subordinates 'reciprocated' agonism received from dominants. Egg laying was associated with the individual network positions of the male and dominant female. Thus, males face a trade-off between promoting structures that facilitate egg laying versus HS. Whether this reproductive conflict is avoidable remains to be determined. We also identified different social and/or reproductive roles for 11-ketotestosterone, 17β-oestradiol and cortisol, suggesting that specific neuroendocrine mechanisms may underlie connections between network structure and fitness. This is one of the first investigations of the reproductive and neuroendocrine correlates of social behaviour and network structure in replicate, naturalistic social groups and supports network structure as an important target for natural selection.

While males typically compete for females, species with female biased sex ratios and/or large male investment in offspring care often exhibit reversed sex roles. Here we investigated, in a haremic fish species, the bluebanded goby,Lythrypnus dalli, the impact of male and female courtship behaviour on male reproductive success, measured as the total number of eggs in the nest and total number of developed eggs. Reproductive success was not associated with rates of male behaviour, such as parenting, approaching and courtship, but was associated with rates of female courtship. Consistent with predictions for a role-reversed reproductive strategy, only males demonstrated nest care and females exhibited high rates of courtship and intrasexual competition, such that alpha females interrupted courtship solicitations by beta females. Overall, these data are consistent with sex role reversal inL. dalliand show that the expression of male courtship behaviour does not interfere with paternal care.