Social odors conveying dominance and reproductive information induce rapid physiological and neuromolecular changes in a cichlid fish.. Oreochromis mossambicus

Social plasticity is a pervasive feature of animal behavior. Animals adjust the expression of their social behavior to the daily changes in social life and to transitions between life-history stages, and the ability to change in these ways impacts their Darwinian fitness. This behavioral plasticity may be achieved either by rewiring or by biochemically switching nodes of the neural network underlying the social behavior in response to perceived social information. Independent of the proximate mechanisms, at the neuromolecular level social plasticity relies on the regulation of gene expression, such that different neurogenomic states emerge in response to different social stimuli and the switches between states are orchestrated by signaling pathways that interface the social environment and the genotype. Here, we test this hypothesis by characterizing the changes in the brain profile of gene expression in response to social odors in the Mozambique Tilapia, Oreochromis mossambicus. This species has a rich repertoire of social behaviors during which both visual and chemical information are conveyed to conspecifics. Specifically, dominant males increase their urination frequency during agonist encounters and during courtship to convey chemical information reflecting their dominance status. We recorded electro-olfactograms to test the extent to which the olfactory epithelium can discriminate between olfactory information from dominant and subordinate males as well as from pre- and post-spawning females. We then performed a genome-scale gene expression analysis of the olfactory bulb and the olfactory cortex homolog in order to identify the neuromolecular systems involved in processing these social stimuli. Our results show that different olfactory stimuli from conspecifics’ have a major impact in the brain transcriptome, with different chemical social cues eliciting specific patterns of gene expression in the brain. These results confirm the role of rapid changes in gene expression in the brain as a genomic mechanism underlying behavioural plasticity and reinforce the idea of an extensive transcriptional plasticity of cichlid genomes, especially in response to rapid changes in their social environment. Overall design: Brain samples from 40 African cichlid males, Oreochromis mossambicus were collected after stimulation with different social olfactory stimuli. Samples were collected from 2 brain areas: BO and Dp after males were exposed to dominant (DOM) and subordinate (SUB) male urine and pre- (PRE) and post-ovulatory (POST) female scent. In OB 5 replicates were collected from males exposed to DOM and 6 to the other stimuli. For Dp 5 replicates were collected from males exposed to DOM and POST, 4 to SUB and 6 to PRE.

社会可塑性是动物行为的普遍特征。动物会依据社会生活的日常波动以及生命史阶段间的转变，调整自身社会行为的表达模式，而这类行为调整能力会对其达尔文适合度（Darwinian fitness）产生影响。这类行为可塑性可通过两种途径实现：一是针对感知到的社会信息，对支撑社会行为的神经网络节点进行重新连接；二是通过生化方式切换这些节点。撇开近因机制不谈，在神经分子层面，社会可塑性依赖于基因表达的调控，即不同的社会刺激会诱导产生不同的神经基因组状态，而状态间的切换由衔接社会环境与基因型的信号通路所调控。

本研究以莫桑比克罗非鱼（Oreochromis mossambicus）为对象，通过解析其脑部基因表达谱响应社会嗅觉刺激的变化，对该假说进行验证。该物种拥有丰富的社会行为谱，在这类行为中，视觉与化学信息均可被传递给同种个体。具体而言，优势雄性在与竞争者对峙以及求偶过程中会提升排尿频率，以此传递反映其优势地位的化学信息。我们通过记录嗅觉电图（electro-olfactograms），探究嗅觉上皮（olfactory epithelium）对优势雄性、从属雄性以及产卵前、产卵后雌性的嗅觉信息的分辨能力。随后，我们对嗅球（olfactory bulb）与嗅皮层同源区（olfactory cortex homolog）开展全基因组尺度的基因表达分析，以鉴定参与处理这类社会刺激的神经分子系统。

我们的研究结果显示，来自同种个体的不同嗅觉刺激对脑部转录组（transcriptome）具有显著影响，不同的化学社会线索会诱导脑部产生特异性的基因表达模式。上述结果证实，脑部基因表达的快速变化作为行为可塑性的基因组机制发挥作用，并进一步支持了慈鲷（cichlid）基因组存在广泛转录可塑性的观点，尤其是在响应社会环境快速变化的情境下。

实验设计概述：本研究选取40尾雄性莫桑比克罗非鱼（Oreochromis mossambicus），向其施加不同的社会嗅觉刺激后采集脑部样本。采集样本的脑区包括两个：嗅球（OB）与嗅皮层同源区（Dp），刺激物分别为优势雄性（DOM）与从属雄性（SUB）的尿液，以及产卵前（PRE）与排卵后（POST）雌性的气味。在嗅球样本中，接受优势雄性刺激的雄性个体设置5个生物学重复，其余刺激组设置6个生物学重复；在嗅皮层同源区样本中，接受优势雄性与排卵后雌性刺激的个体各设置5个重复，接受从属雄性刺激的设置4个重复，接受产卵前雌性刺激的设置6个重复。