Gene expression is more strongly associated with behavioural specialisation than with age or fertility in ant workers

The ecological success of social insects is based on division of labour, not only between queens and workers, but also among workers. Whether a worker tends the brood or forages is influenced by age, fertility and nutritional status, with brood carers being younger, more fecund and more corpulent. Here, we experimentally disentangle behavioural specialisation from age and fertility in Temnothorax longispinosus ant workers and analyse how these parameters are linked to whole-body gene expression. A total of 3644 genes were associated with behavioural specialisation which is ten times more than associated with age and 50 times more than associated with fertility. Brood carers were characterized by an upregulation of three Vitellogenin (Vg) genes, one of which, Vg-like A, was the most differentially expressed gene that was recently shown experimentally to control the switch from brood- to worker-care. The expression of Conventional Vg was unlinked to behavioural specialisation, age or fertility, which contrasts to studies on bees and some ants. Diversity in Vg/Vg-like copy number and expression bias across ants supports subfunctionalisation of vitellogenin genes and indicates that some regulatory mechanisms of division of labour diverged in different ant lineages. Simulations revealed that our experimental dissociation of co-varying factors reduced transcriptomic noise, suggesting that confounding factors could potentially explain inconsistencies across transcriptomic studies of behavioural specialisation in ants. Thus, our study reveals that worker gene expression is mainly linked to the worker’s function for the colony and provides novel insights into the evolution of sociality in ants.

社会性昆虫的生态成功基于劳动分工，这种分工不仅存在于蚁后与工蚁之间，更存在于工蚁群体内部。工蚁选择育幼还是觅食，受年龄、生育力与营养状态的调控：育幼工蚁通常更为年轻、繁殖潜力更强且体型更为饱满。本研究针对长刺细胸蚁（Temnothorax longispinosus）工蚁展开实验，将行为特化与年龄、生育力两个变量实验性分离，并分析这些参数与全身基因表达的关联。最终共鉴定出3644个与行为特化相关的基因，其数量是与年龄相关基因的10倍，与生育力相关基因的50倍。育幼工蚁的特征为三个卵黄原蛋白（Vitellogenin, Vg）基因的表达上调，其中Vg-like A基因是差异表达最显著的基因，此前已有实验证实该基因可调控育幼行为向觅食行为的转换。常规卵黄原蛋白（Conventional Vg）的表达与行为特化、年龄或生育力均无关联，这一结果与蜜蜂及部分蚂蚁的相关研究结论相悖。不同蚂蚁类群中卵黄原蛋白/类卵黄原蛋白基因的拷贝数与表达偏好多样性，支持了卵黄原蛋白基因的亚功能化现象，同时表明劳动分工的部分调控机制在不同蚂蚁演化支系中发生了分化。模拟分析显示，本研究对共变因素的实验性分离降低了转录组数据的噪声，这提示混淆变量或许可以解释此前蚂蚁行为特化转录组学研究中出现的诸多不一致结果。综上，本研究揭示工蚁的基因表达主要与其在蚁群中的功能角色相关，同时为蚂蚁社会性的演化提供了全新的认知视角。