A complete absence of indirect genetic effects on brain gene expression in a highly social context

Genes not only control traits of their carrier organism (known as Direct Genetic Effects or DGEs) but also shape their carrier's physical environment and the phenotypes of their carrier's social partners (known as Indirect Genetic Effects or IGEs). Theoretical research has shown that the effects that genes exert on social partners can have profound consequences, potentially altering heritability and the direction of trait evolution. Complementary empirical research has shown that in various contexts (particularly in animal agriculture) IGEs can explain a large proportion of variation in specific traits. However, little is known about the general prevalence of IGEs. We conducted a reciprocal cross-fostering experiment with two genetic lineages of the clonal raider ant Ooceraea biroi to quantify the relative contribution of DGEs and IGEs to variation in brain gene expression (which underlies behavioral variation). We find that thousands of genes are differentially expressed by DGEs but not a single gene is differentially expressed by IGEs. This is surprising given the highly social context of ant colonies and given that individual behavior varies according to the genotypic composition of the social environment in O. biroi. Overall, these findings indicate that we have a lot to learn about how the magnitude of IGEs varies across species and contexts

Social isolation shortens lifespan through oxidative stress in ants

Abstract Social isolation negatively affects health, induces detrimental behaviors, and shortens lifespan in social species. Little is known about the mechanisms underpinning these effects because model species are typically short-lived and non-social. Using colonies of the carpenter ant Camponotus fellah, we show that social isolation induces hyperactivity, alters space-use, and reduces lifespan via changes in the expression of genes with key roles in oxidation-reduction and an associated accumulation of reactive oxygen species. These physiological effects are localized to the fat body and oenocytes, which perform liver-like functions in insects. We use pharmacological manipulations to demonstrate that the oxidation-reduction pathway causally underpins the detrimental effects of social isolation on behavior and lifespan. These findings have important implications for our understanding of how social isolation affects behavior and lifespan in general

Social network position is a major predictor of ant behavior, microbiota composition, and brain gene expression

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.La physiologie et le comportement des organismes sociaux sont liés à leurs environnements sociaux. Cependant, les environnements sociaux sont généralement confondus par l'âge et les environnements physiques (c'est-à-dire, la localisation spatiale et les facteurs abiotiques associés), rendant ces corrélations souvent difficiles à interpréter. Par exemple, les associations entre l'environnement social d'un individu et ses patrons d'expression génique peuvent résulter à la fois de l'âge ou du comportement. La mesure simultanée des variables pertinentes et la quantification des corrélations entre ces variables peuvent indiquer si les relations sont directes (et potentiellement causales) ou indirectes. Ici, nous combinons le suivi démographique et comportemental automatisé avec une approche multiomique pour disséquer la structure de corrélation parmi l'environnement social et physique, l'âge, le comportement, l'expression génique cérébrale et la composition de la microbiote chez la fourmi charpentière Camponotus fellah. Les variations dans la physiologie et le comportement étaient les plus fortement corrélées avec l'environnement social. De plus, des corrélations apparemment fortes entre l'expression génique cérébrale et la composition de la microbiote, l'environnement physique, l'âge et le comportement sont devenues faibles lorsque l'on contrôlait pour l'environnement social. En accord avec cela, une analyse d'apprentissage automatique a révélé que, à partir des données d'expression génique cérébrale, l'environnement social d'un individu peut être prédit de manière plus précise que toute autre mesure comportementale. Ces résultats indiquent que l'environnement social est un régulateur clé du comportement et de la physiologie