Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.
Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland.
PLoS Biol. 2023 Jul 24;21(7):e3002203. doi: 10.1371/journal.pbio.3002203. eCollection 2023 Jul.
The physiology and behavior of social organisms correlate with their social environments. However, because social environments are typically confounded by age and physical environments (i.e., spatial location and associated abiotic factors), these correlations are usually difficult to interpret. For example, associations between an individual's social environment and its gene expression patterns may result from both factors being driven by age or behavior. Simultaneous measurement of pertinent variables and quantification of the correlations between these variables can indicate whether relationships are direct (and possibly causal) or indirect. Here, we combine demographic and automated behavioral tracking with a multiomic approach to dissect the correlation structure among the social and physical environment, age, behavior, brain gene expression, and microbiota composition in the carpenter ant Camponotus fellah. Variations in physiology and behavior were most strongly correlated with the social environment. Moreover, seemingly strong correlations between brain gene expression and microbiota composition, physical environment, age, and behavior became weak when controlling for the social environment. Consistent with this, a machine learning analysis revealed that from brain gene expression data, an individual's social environment can be more accurately predicted than any other behavioral metric. These results indicate that social environment is a key regulator of behavior and physiology.
社会生物的生理和行为与其社会环境密切相关。然而,由于社会环境通常与年龄和物理环境(即空间位置和相关的非生物因素)混淆,这些相关性通常难以解释。例如,个体的社会环境与其基因表达模式之间的关联可能是由年龄或行为这两个因素共同驱动的。同时测量相关变量并量化这些变量之间的相关性,可以表明关系是直接(可能是因果关系)的还是间接的。在这里,我们将人口统计学和自动化行为跟踪与多组学方法相结合,以剖析木匠蚁 Camponotus fellah 中社会和物理环境、年龄、行为、大脑基因表达和微生物群落组成之间的相关结构。生理和行为的变化与社会环境的相关性最强。此外,当控制社会环境时,大脑基因表达与微生物群落组成、物理环境、年龄和行为之间看似强烈的相关性变得较弱。与此一致的是,机器学习分析表明,从大脑基因表达数据中,可以更准确地预测个体的社会环境,而不是任何其他行为指标。这些结果表明,社会环境是行为和生理的关键调节因素。