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.

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.