Molecular adjustment to a social niche: Brain transcriptomes reveal divergent influence of social environment on the two queen morphs of the ant Temnothorax rugatulus

In this study, we experimentally disentangled the effect of queen morph and social organization by using a full-factorial design. We expected macrogynes to be well adapted to the situation of being the only queen in a colony, whereas for microgynes, this could be an unusual and potentially stressful social environment. Conversely, we predicted that macrogynes might respond to the lower level of care potentially provided in polygynous societies compared to microgynes, for whom polygyny is the typical social organization (Negroni et al., 2021). We focus here on the transcriptional activity in the brain, as the central nervous system is where information about the social environment is perceived, processed, and can lead to physiological or behavioral responses (Manfredini et al., 2022; Jernigan & Uy 2023). There is evidence that behavioral dynamics between workers and queens depend on queen morph, as trophallactic interactions with microgynes are much more frequent (Negroni et al., 2021). In addition to changes in the expression of behavioral genes, we were interested in whether the queens responded to their social environment by altering the expression of genes associated with stress, fertility, or lifespan functions. We also investigated the influence of queen form and behavioral task on brain transcriptome of workers to determine whether T. rugatulus workers from macrogynous colonies differ in brain activity and potentially behavior from those raised and living in microgynous societies.

在本项研究中，我们通过全因子设计实验性地解析了蜂后形态与社会组织效果之间的关系。我们预期，大雌蜂能够很好地适应作为群落中唯一蜂后的境遇，而对于小雌蜂而言，这可能是一种罕见且可能充满压力的社会环境。反之，我们推测，大雌蜂可能会对多配偶社会中可能提供的较低水平关怀作出反应，相比之下，多配偶制对于小雌蜂来说是典型的社会组织形式（Negroni 等人，2021年）。在此，我们聚焦于大脑中的转录活动，因为中枢神经系统是感知、处理社会环境信息并可能导致生理或行为反应的核心区域（Manfredini 等人，2022年；Jernigan 与 Uy，2023年）。有证据表明，工蜂与蜂后之间的行为动态取决于蜂后形态，因为与微雌蜂的共食互动更为频繁（Negroni 等人，2021年）。除了行为基因表达的变化之外，我们还关注蜂后对其社会环境的响应，即通过改变与压力、生育或寿命功能相关的基因表达来调整。此外，我们还研究了蜂后形态和行为任务对工蜂大脑转录组的影响，以确定来自多雌蜂群的大雌蜂工蜂在脑活动及潜在行为上是否与在多雌蜂社会中成长和生活的工蜂存在差异。