Behavior plays a fundamental role in shaping the origin and fate of species. Mating decisions can act to promote or restrict gene flow, as can personality traits that influence dispersal and niche use. Mate choice and personality are often both learned and therefore influenced by an individual's social environment throughout development. Likewise, the molecular pathways that shape these behaviors may also be co-expressed. In this study on swordtail fish (Xiphophorus birchmanni), we show that female mating preferences for species-typical pheromone cues are entirely dependent on social experience with adult males. Experience with adults also shapes development along the shy-bold personality axis, with shy behaviors arising from exposure to risk-averse heterospecifics as a potential stress-coping strategy. In maturing females, conspecific exposure results in a strong upregulation of olfaction and vision genes compared with heterospecific exposure, as well as immune response genes previously linked to anxiety, learning and memory. Conversely, heterospecific exposure involves an increased expression of genes important for neurogenesis, synaptic plasticity and social decision-making. We identify subsets of genes within the social decision-making network and with known stress-coping roles that may be directly coupled to the olfactory processes females rely on for social communication. Based on these results, we conclude that the social environment affects the neurogenomic trajectory through which socially sensitive behaviors are learned, resulting in adult phenotypes adapted for specific social groupings.

Behavioral phenotypes play an active role in maximizing fitness and shaping the evolutionary trajectory of species by offsetting the ecological and social environmental factors individuals experience. How these phenotypes evolve and how they are expressed is still a major question in ethology today. In recent years, an increased focus on the mechanisms that regulate the interactions between an individual and its environment has offered novel insights into the expression of alternative phenotypes. In this review, we explore the proximate mechanisms driving the expression of alternative reproductive phenotypes in the male prairie vole (Microtus ochrogaster) as one example of how the interaction of an individual’s social context and internal milieu has the potential to alter behavior, cognition, and reproductive decision-making. Ultimately, integrating the physiological and psychological mechanisms of behavior advances understanding into how variation in behavior arises. We take a “levels of biological organization” approach, with prime focus placed on the level of the organism to discuss how cognitive processes emerge as traits, and how they can be studied as important mechanisms driving the expression of behavior.

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