Brain remodeling during queen maturation by a gene-regulation network that was co-opted by ants with reproductive workers

Caste differentiation in ants is decided early in development to produce gynes as future colony germ-lines and workers as present colony soma. However, gynes need to be inseminated to become functional queens, a transition triggered by stored sperm that initiates reproductive role differentiation relative to gynes that remain unmated. Here we analyze the anatomy and transcriptomes of brains during this differentiation process within the reproductive caste of Monomorium pharaonis. Insemination terminated brain growth whereas unmated control gynes continued to increase their brain volume. Transcriptomes revealed that a specific gene regulatory network (GRN) mediates both brain anatomy changes and concomitant behavioral modifications. This reproductive role differentiation GRN hardly overlapped with the gyne-worker caste differentiation GRN, but it appears to have been coopted by distantly related ants where workers became germ-line individuals after the queen caste was secondarily lost, entirely or partially. The genes corazonin and neuroparsin-A in the anterior neurosecretory cells were overexpressed in individuals with less or non-reproductive roles across all four ant species investigated.

蚂蚁的社会型分化在发育早期即已确定，由此产生雌蚁（gyne）作为未来种群的生殖系个体，以及工蚁（worker）作为当前种群的体细胞个体。然而，雌蚁需经受精才能成为具有生殖功能的蚁后，这一转变由储存的精子触发，进而启动与未交配雌蚁相对的生殖角色分化过程。本研究针对法老蚁（Monomorium pharaonis）生殖品级内的这一分化过程，分析其脑部解剖结构与转录组特征。研究发现，受精会终止脑部发育，而未交配的对照雌蚁则会持续增大脑部体积。转录组分析显示，特定的基因调控网络（gene regulatory network, GRN）同时介导脑部解剖结构变化与伴随的行为改变。该生殖角色分化GRN与雌蚁-工蚁社会型分化的GRN几乎无重叠，但它似乎被远缘蚁类所借用以实现功能替代：在这些蚁类中，当蚁后品级次生完全或部分丧失后，工蚁会转变为生殖系个体。前神经分泌细胞中的corazonin与neuroparsin-A基因，在本次研究涉及的4种蚁类中，生殖能力较弱或无生殖能力的个体内均呈过表达状态。