The spread of fear in an empathetic fish.

An evolutionarily ancient signaling pathway mediates emotional contagion.

Social network dynamics predict hormone levels and behavior in a highly social cichlid fish.

Group living confers many benefits while simultaneously exposing group members to intense competition. An individual's rise to prominence within a group may conflict with the overall functioning of the group. There is therefore a complex and dynamic relationship between the behavioral displays that directly benefit an individual, the consequences of these actions for the community, and how they feed back on individual-level fitness. We used a network analysis approach to study the link between behavior, social stability, and steroid hormone levels in replicate communities of the cichlid fish, Astatotilapia burtoni, which live in social groups with a dominance hierarchy. We demonstrate that individual behavior can have direct and indirect effects on the behavior of others while also affecting group characteristics. Our results show that A. burtoni males form stable social networks, where dominant individuals act as hubs for social interactions. However, there was variation in the temporal stability in these networks, and this variation in stability impacted hormone levels. Dominant males had higher testosterone levels, however, the differences in testosterone levels between dominant and subordinate males were greatest in stable communities. In sum, our analyses provide novel insights into the processes by which individual and community properties interact.

Neural and molecular mechanisms underlying female mate choice decisions in vertebrates.

Female mate choice is a dynamic process that allows individuals to selectively mate with those of the opposite sex that display a preferred set of traits. Because in many species males compete with each other for fertilization opportunities, female mate choice can be a powerful agent of sexual selection, often resulting in highly conspicuous traits in males. Although the evolutionary causes and consequences of the ornamentation and behaviors displayed by males to attract mates have been well studied, embarrassingly little is known about the proximate neural mechanisms through which female choice occurs. In vertebrates, female mate choice is inherently a social behavior, and although much remains to be discovered about this process, recent evidence suggests the neural substrates and circuits underlying other fundamental social behaviors (such as pair bonding, aggression and parental care) are likely similarly recruited during mate choice. Notably, female mate choice is not static, as social and ecological environments can shape the brain and, consequently, behavior in specific ways. In this Review, we discuss how social and/or ecological influences mediate female choice and how this occurs within the brain. We then discuss our current understanding of the neural substrates underlying female mate choice, with a specific focus on those that also play a role in regulating other social behaviors. Finally, we propose several promising avenues for future research by highlighting novel model systems and new methodological approaches, which together will transform our understanding of the causes and consequences of female mate choice.

Spontaneous alloparental care of unrelated offspring by non-breeding Amphiprion ocellaris in absence of the biological parents.

Many species display alloparental care, where individuals care for offspring that are not their own, but usually the behavior is contingent on the individual receiving some direct or indirect benefit. In anemonefish, after removing the breeding male, non-breeders have been observed providing care for eggs they did not sire and which are not kin. Previously this behavior was interpreted as coerced by the female. The purpose of this study was to test the alternative hypothesis that the alloparental care occurs spontaneously without prodding by the female. Groups of Amphiprion ocellaris (male, female and non-breeder) were maintained in the laboratory and behavior monitored after removing the male and both the male and female. Non-breeders began to care for eggs after male removal and further increased parental care after male and female removal. Level of care was not as high as experienced males, but additional experiments showed performance increases with experience. In a separate experiment, non-breeders were placed alone in a novel aquarium and eggs from an established spawning pair were introduced. Approximately 30% of the fish displayed extensive fathering behavior within 90 min. Taken together, our results demonstrate that fathering behavior in A. ocellaris occurs spontaneously, independent of paternity or kinship.

Nonapeptides mediate trade-offs in parental care strategy.

Parental care represents a suite of distinct behaviors performed by parents to maximize fitness. Dynamic shifts in parental care behaviors, such as between nest defense and direct provisioning of the offspring, are required in response to environmental variation. However, the neural mechanisms which mediate such behavioral shifts remain a mystery. The anemonefish, Amphiprion ocellaris, represents an experimentally valuable model in social neuroscience which is conducive to manipulating the environment while simultaneously measuring parental care. The goal of this study was to determine the extent to which arginine vasotocin (AVT) and isotocin (IT) signaling are necessary for males to shift between direct egg care and aggressive nest defense in the presence of intruders, Domino damselfish (Dascyllus trimaculatus). The IT receptor antagonist desGly-NH2-d(CH2)5[D-Tyr2,Thr4]OVT, significantly reduced direct egg care, while at the same time increased levels of aggressive nest defense relative to vehicle. Conversely, blockade of AVT using the antagonist d(CH2)5[Tyr(Me)2]AVP, reduced aggression and tended to increase egg care. Results demonstrate that male anemonefish alter their parental strategy in response to allospecific intruders, and that IT and AVT signaling oppositely regulate parental care displays of aggression versus egg care.

Active feminization of the preoptic area occurs independently of the gonads in Amphiprion ocellaris.

Sex differences in the anatomy and physiology of the vertebrate preoptic area (POA) arise during development, and influence sex-specific reproductive functions later in life. Relative to masculinization, mechanisms for feminization of the POA are not well understood. The purpose of this study was to induce sex change from male to female in the anemonefish Amphiprion ocellaris, and track the timing of changes in POA cytoarchitecture, composition of the gonads and circulating sex steroid levels. Reproductive males were paired together and then sampled after 3 weeks, 6 months, 1 year and 3 years. Results show that as males change sex into females, number of medium cells in the anterior POA (parvocellular region) approximately double to female levels over the course of several months to 1 year. Feminization of gonads, and plasma sex steroids occur independently, on a variable timescale, up to years after POA sex change has completed. Findings suggest the process of POA feminization is orchestrated by factors originating from within the brain as opposed to being cued from the gonads, consistent with the dominant hypothesis in mammals. Anemonefish provide an opportunity to explore active mechanisms responsible for female brain development in an individual with male gonads and circulating sex steroid levels.

Dynamic regulation of brain aromatase and isotocin receptor gene expression depends on parenting status.

Fathering behavior is critical for offspring survival in many species across diverse taxa, but our understanding of the neuroendocrine mechanisms regulating paternal care is limited in part because of the few primarily paternal species among the common animal models. However, many teleosts display primarily paternal care, and among the teleosts, anemonefish species are particularly well suited for isolating molecular mechanisms of fathering as they perform parental care in isolation of many other typically competing behaviors such as territorial defense and nest building. The goal of this study was to determine the extent to which whole brain gene expression levels of isotocin receptors, arginine vasotocin receptors, and aromatase as well as circulating levels of the bioactive sex steroid hormones estradiol (E2) and 11-ketotestosterone (11KT) vary in association with parenting behavior in Amphiprion ocellaris. Brain aromatase and IT receptor gene expression were higher in both males and females that were parenting versus not. IT receptor expression was overall higher in males than females, which we interpret is a reflection of the greater parental effort that males display. Aromatase was overall higher in females than males, which we conclude is related to the higher circulating E2, which crosses into the brain and increases aromatase transcription. Results suggest both aromatase and IT receptors are dynamically upregulated in the brains of A. ocellaris males and females to support high levels of parental effort.

The melanocortin system regulates body pigmentation and social behaviour in a colour polymorphic cichlid fish.

The melanocortin system is a neuroendocrine system that regulates a range of physiological and behavioural processes. We examined the extent to which the melanocortin system simultaneously regulates colour and behaviour in the cichlid fish Astatotilapia burtoni We found that yellow males are more aggressive than blue males, in line with previous studies. We then found that exogenous α-melanocyte-stimulating hormone (α-MSH) increases yellowness of the body and dispersal of xanthophore pigments in both morphs. However, α-MSH had a morph-specific effect on aggression, with only blue males showing an increase in the rate of aggression. Exogenous agouti signalling peptide (ASIP), a melanocortin antagonist, did not affect coloration but reduced the rate of aggression in both colour morphs. Blue males had higher cortisol levels than yellow males. Neural gene expression of melanocortin receptors (mcr) and ligands was not differentially regulated between colour morphs. In the skin, however, mc1r and pro-opiomelanocortin (pomc) ß were upregulated in blue males, while asip 1 was upregulated in yellow males. The effects of α-MSH on behaviour and body coloration, combined with morph-specific regulation of the stress response and the melanocortin system, suggest that the melanocortin system contributes to the polymorphism in behaviour and coloration in A. burtoni.

Opposite effects of nonapeptide antagonists on paternal behavior in the teleost fish Amphiprion ocellaris.

The nonapeptides isotocin (IT) and arginine vasotocin (AVT), along with their mammalian homologs oxytocin and arginine vasopressin, are well known regulators of social behaviors across vertebrate taxa. However, little is known about their involvement in paternal care. Here, we measured the effect of an IT and an AVT V1a receptor antagonist on paternal behaviors in the primarily paternal teleost Amphiprion ocellaris. We also measured the effect of the IT receptor antagonist on aggression in dyadic contests between two non-reproductive fish to assess specificity of the effect on paternal behaviors. Individual differences in levels of paternal behaviors (nips, fanning the eggs, and proportion of the time in the nest) were consistent across spawning cycles when no treatments were administered. The IT receptor antagonist severely reduced paternal behaviors but had no effect on aggression, whereas the AVT V1a receptor antagonist increased paternal behaviors. These results support the idea that IT signaling is crucial for the expression of paternal behavior in A. ocellaris. Based on a previous study showing that the AVT V1a antagonist decreases aggression in dyadic contests, we hypothesize that the antagonist enhances paternal behavior indirectly by reducing vigilance and aggression, thereby alleviating effort directed towards other competing behaviors and allowing for the increased expression of paternal behaviors.

Appetite and weight gain suppression effects of alcohol depend on the route and pattern of administration in Long Evans rats.

Ethanol can be a food source but its effects on energy balance and contribution to obesity remain inconclusive. In this study, we hypothesized that the effects of ethanol on energy intake and body weight would depend on the administration dose, pattern and the blood ethanol concentration (BEC) time-course. Experiment 1 examined changes in food intake, diet preference, and body weight after saline or ethanol (1 and 3g/kg) injection (IP). Experiment 2 compared the effects in rats that received either 3g/kg/day ethanol administered all at once (EtOH_S) or 2 1.5g/kg injections spaced by 3h (EtOH_D). Experiment 3 examined the effects of 7.5h/day, Mon through Fri for 8weeks, voluntary ethanol drinking (5% and 10% ethanol) on food intake and body weight. Results of Experiments 1 and 2 indicate that acute ethanol administrations dose-dependently reduced energy intake, high fat diet preference and weight gain. Acute 3g/kg ethanol injection in the EtOH_S group decreased energy intake, weight gain and visceral fat to a greater extent than in the EtOH_D group. Results of Experiment 3 show that male and female rats voluntarily drank 1.65-2.31g/kg ethanol within 3.5h with reduced chow intake but unchanged total energy intake and weight gain. Furthermore, 3g/kg ethanol injection resulted in BEC that remained at intoxicating levels e.g. >120mg/dL for several hours post-administration and was higher in the EtOH_S than in the EtOH_D group. In contrast, BEC in voluntarily drinking was ~67mg/dL and decreased to below 10mg/dL 5h after termination of ethanol access. Taken together, these data suggest that 3g/kg ethanol injection robustly suppresses appetite and weight gain due to the higher BECs attained. Furthermore, BEC attained and maintained is a determining factor for how ethanol administration affects appetite and long-term energy balance.