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

ABSTRACT: 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.

ORGANISM(S): Ooceraea biroi

PROVIDER: GSE210246 | GEO | 2022/08/29

REPOSITORIES: GEO

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Project description:Rearing conditions may elicit noticeable plastic responses in life-history traits of living organisms. For instance, diet composition has proven to influence prominent traits such as body size, fecundity, and lifespan. In contrast, the social environment may influence the survival rate at immature stages, food consumption, and fat storage. Nevertheless, the physiological mechanisms underlying such responses are largely unknown. In this study, we investigated changes in the proteome of the house cricket Acheta domesticus subjected to diets of different nutritional composition (i.e., protein to carbohydrates ratio) and two distinct social environments (i.e., solitary or in groups). We measured the relative abundances of 685 proteins identified in whole-body cricket samples using high-performance liquid chromatography coupled to tandem mass spectrometry. Differential expression of proteins induced by diet composition and social environment in female and male A. domesticus was assessed in a data-independent proteomics approach. Additionally, we performed a functional analysis of the differentially expressed proteins using comprehensive databases (KEGG and GO). We found that sex alone explained a significant portion (40.87%) of the relative protein abundance variation. Males had a higher representation of proteins involved in metabolic pathways and locomotion. In contrast, females exhibited a higher abundance of proteins related to genetic processes regulation and nutrient catabolism. Moreover, diet composition and social environment induced sex-specific changes in a smaller set of proteins with particular roles. Females had their protein profile affected by diet composition and social environment. The involved proteins were mainly related to several protein synthesis stages, carbohydrate metabolism, and muscle development. In contrast, males were only affected by diet composition, overexpressing proteins related to hormone production, carbohydrate metabolism, and apparently depositing excess protein in the cuticle when fed with a protein-rich diet. It was evident that diet had a more substantial influence on the proteome of the cricket A. domesticus than the social environment, showing that diet composition may exert profound physiological changes in insects in a sex-specific manner.

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

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