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. Overall design: Cross-fostering newly-hatched larvae of lineages B and M into social environments of lineages B or M

基因不仅调控其载体生物的性状（即直接遗传效应（Direct Genetic Effects, DGEs）），还会塑造载体的物理环境以及其社会伙伴的表型（即间接遗传效应（Indirect Genetic Effects, IGEs））。理论研究表明，基因对社会伙伴施加的效应可产生深远影响，甚至可能改变性状的遗传力及其演化方向。相关配套实证研究证实，在多种场景下（尤其是畜牧养殖业中），间接遗传效应可解释特定性状的大量变异。然而，目前学界对间接遗传效应的普遍发生程度仍知之甚少。本研究针对克隆掠夺蚁（Ooceraea biroi）的两个遗传谱系开展了双向交叉抚育实验，以量化直接遗传效应与间接遗传效应对脑基因表达变异（该变异是行为变异的分子基础）的相对贡献。研究结果显示，数千个基因的表达受直接遗传效应调控，但未发现任何一个基因的表达受间接遗传效应调控。鉴于蚁群高度社会化的生存环境，以及克隆掠夺蚁的个体行为会随社会环境的基因型组成发生改变，这一结果颇为出人意料。总体而言，本研究结果表明，我们仍需深入探究间接遗传效应的强度在不同物种与实验场景下的变化规律。实验整体设计：将谱系B与谱系M的初孵幼虫交叉抚育至谱系B或谱系M的社会环境中。