Genome-Wide Expression Patterns and the Genetic Architecture of a Fundamental Social Trait

Explaining how interactions between genes and the environment influence social behavior is a fundamental research goal, yet there is limited relevant information for species exhibiting natural variation in social organization. The fire ant Solenopsis invicta is characterized by a remarkable form of social polymorphism, with the presence of one or several queens per colony and the expression of other phenotypic and behavioral differences being completely associated with allelic variation at a single Mendelian factor marked by the gene Gp-9. Microarray analyses of adult workers revealed that differences in the Gp-9 genotype are associated with the differential expression of an unexpectedly small number of genes, many of which have predicted functions, implying a role in chemical communication relevant to the regulation of colony queen number. Even more surprisingly, worker gene expression profiles are more strongly influenced by indirect effects associated with the Gp-9 genotypic composition within their colony than by the direct effect of their own Gp-9 genotype. This constitutes an unusual example of an “extended phenotype” and suggests a complex genetic architecture with a single Mendelian factor, directly and indirectly influencing the individual behaviors that, in aggregate, produce an emergent colony-level phenotype.

阐明基因与环境间的交互作用如何影响社会行为，是核心研究目标之一，但针对社会组织结构存在自然变异的物种，相关研究资料却极为匮乏。红火蚁（Solenopsis invicta）具备极具特色的社会多态性：其蚁群可由单头或多头蚁后统领，其余所有表型与行为差异，均与以Gp-9基因为标记的单一孟德尔因子上的等位基因变异完全关联。对成年工蚁开展的基因芯片（Microarray）分析结果显示，Gp-9基因型的差异仅与极少数基因的差异表达相关，其中多数基因已被预测具备特定功能，这暗示这些基因在调控蚁群蚁后数量相关的化学通讯中发挥作用。更令人意外的是，工蚁的基因表达谱所受的影响，更多来自其所在蚁群内Gp-9基因型组成带来的间接效应，而非自身Gp-9基因型的直接影响。这一现象构成了‘延伸表型（extended phenotype）’的罕见实例，同时表明存在一种复杂的遗传架构：该单一孟德尔因子可通过直接与间接途径影响个体行为，最终共同催生涌现出的蚁群层级表型。