Isotocin increases female avoidance of males in a coercive mating system: Assessing the social salience hypothesis of oxytocin in a fish species

Abstract

The nonapeptide oxytocin (and its fish homolog isotocin (IT)) is an evolutionarily-conserved hormone associated with social behaviors across most vertebrate taxa. Oxytocin has traditionally been regarded as a prosocial hormone, but studies on social cognition in mammalian models suggest it may play a more nuanced role in modulating social discrimination based on social salience and stimulus valence. Here we test IT and its role in regulating female social decision-making and anxiety behaviors in a live-bearing fish with a male coercive mating system. Gambusia affinis males engage in a forced mating strategy, with frequent harassment and attempted copulatory thrusts directed towards unwilling females. Exogenous IT produced anxiolytic responses in female G. affinis that altered exploration (time in center of tank) but not time in dark vs. light regions of the tank. Exogenous IT also produced context-specific changes in social tendency: IT-treated G. affinis females spent less time associating with males while association time with conspecific females was not altered. Further, while overall activity levels were not changed by IT treatment, the amount of social behaviors IT-treated females directed towards males, but not females, was reduced. Our results support the social salience hypothesis of oxytocin action in a teleost and suggest that oxytocin's critical input into social cognitive processing is conserved across vertebrate taxa.

Keywords: Anxiety; Exploration; Isotocin; Oxytocin; Poeciliid; Sexual conflict; Social cognition; Social decision-making; Social discrimination; Social salience.