Schmid College of Science and Technology, Chapman University, Orange, CA, USA.
Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zürich, Switzerland.
BMC Genomics. 2020 Jul 22;21(1):506. doi: 10.1186/s12864-020-06911-5.
Appropriate social interactions influence animal fitness by impacting several processes, such as mating, territory defense, and offspring care. Many studies shedding light on the neurobiological underpinnings of social behavior have focused on nonapeptides (vasopressin, oxytocin, and homologues) and on sexual or parent-offspring interactions. Furthermore, animals have been studied under artificial laboratory conditions, where the consequences of behavioral responses may not be as critical as when expressed under natural environments, therefore obscuring certain physiological responses. We used automated recording of social interactions of wild house mice outside of the breeding season to detect individuals at both tails of a distribution of egocentric network sizes (characterized by number of different partners encountered per day). We then used RNA-seq to perform an unbiased assessment of neural differences in gene expression in the prefrontal cortex, the hippocampus and the hypothalamus between these mice with naturally occurring extreme differences in social network size.
We found that the neurogenomic pathways associated with having extreme social network sizes differed between the sexes. In females, hundreds of genes were differentially expressed between animals with small and large social network sizes, whereas in males very few were. In males, X-chromosome inactivation pathways in the prefrontal cortex were the ones that better differentiated animals with small from those with large social network sizes animals. In females, animals with small network size showed up-regulation of dopaminergic production and transport pathways in the hypothalamus. Additionally, in females, extracellular matrix deposition on hippocampal neurons was higher in individuals with small relative to large social network size.
Studying neural substrates of natural variation in social behavior in traditional model organisms in their habitat can open new targets of research for understanding variation in social behavior in other taxa.
适当的社交互动通过影响交配、领地防御和后代照顾等多个过程来影响动物的适应度。许多研究揭示了社会行为的神经生物学基础，这些研究集中在神经肽（加压素、催产素和同源物）以及性或亲代-后代相互作用上。此外，动物在人工实验室条件下进行了研究，在这些条件下，行为反应的后果可能不如在自然环境下表达时那么关键，从而掩盖了某些生理反应。我们利用非繁殖季节野生家鼠的社交互动自动记录，来检测具有自我中心网络大小分布两端的个体（以每天遇到的不同伙伴数量为特征）。然后，我们使用 RNA-seq 技术，在prefrontal cortex、hippocampus 和 hypothalamus 中，对具有自然发生的极端社交网络大小差异的这些小鼠进行了基因表达的神经差异的无偏评估。
我们发现，与具有极端社交网络大小相关的神经基因组途径在性别之间存在差异。在雌性中，具有小和大社交网络大小的动物之间有数百个基因表达差异，而在雄性中则很少。在雄性中，prefrontal cortex 中的 X 染色体失活途径更好地将具有小社交网络大小的动物与具有大社交网络大小的动物区分开来。在雌性中，具有小网络大小的动物表现出下丘脑多巴胺生成和转运途径的上调。此外，在雌性中，具有小社交网络大小的个体的海马神经元细胞外基质沉积较高。
在传统模式生物的栖息地中研究自然变化的社交行为的神经基础，可以为理解其他分类群的社交行为变化开辟新的研究目标。
