Divergent neurogenomic responses shape social learning of both personality and mate preference

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 to 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.

行为在塑造物种的起源与存续命运中扮演着基础性角色。择偶决策与影响扩散及生态位利用的人格特质一样，均可推动或限制基因流。择偶偏好与人格特质通常兼具习得性，因此会在个体整个发育周期内受到其社会环境的调控。同理，调控这两类行为的分子通路或许也存在共表达现象。
本研究以伯奇曼剑尾鱼（Xiphophorus birchmanni）为实验对象，证实雌性对物种典型信息素（pheromone）信号的择偶偏好，完全依赖于其与成年雄性的社会经验。成年个体的暴露经验同样会塑造羞怯-大胆人格轴的发育进程：当幼龄雌性接触避险型异种个体时，会产生羞怯行为，这或为一种潜在的应激应对策略。
在成熟雌性个体中，相较于异种暴露组，同种暴露组的嗅觉与视觉基因，以及此前与焦虑、学习记忆相关的免疫应答基因均呈现显著上调。反之，异种暴露组则会提升与神经发生（neurogenesis）、突触可塑性（synaptic plasticity）及社会决策相关的基因表达水平。
我们在社会决策网络（social decision-making network）中鉴定出了多组基因子集，同时发现部分已知具备应激应对功能的基因，或直接与雌性用于社会交流的嗅觉过程存在关联。基于上述结果，本研究得出结论：社会环境会影响神经基因组轨迹——这一轨迹正是社会性敏感行为的习得路径，最终促使成年个体的表型适配其所处的特定社会群体。