The strong coevolutionary arms race between social parasites and their hosts has dramatically shaped the life-history traits of both parties. One of the main strategies exhibited by hosts in response to parasitism is reproduction by host workers. We lack a mechanistic understanding of how these defence strategies unfold and, specifically, whether hosts exhibit more subtle strategies to reduce the costs of parasitism from the outset. Here we test the hypothesis that there are both behavioural and neurogenomic signatures of worker responses to parasitism, prior to overt expression in the form of egg-laying; we test this using the social parasite—social host system of the paper wasps Polistes sulcifer-Polistes dominula. We characterized individual workers’ position within the social interaction network of queenright and host colonies immediately after parasite usurpation, weeks before the workers’ reproductive rebellion is evident. Parasitism influenced network centrality measures, with workers in parasitized colonies showing increased connectedness and centrality compared to those in unparasitized ones. Next, we quantified brain gene expression levels for five genes related to physiological and behavioural phenotypes in Polistes wasps. The gene Imaginal disc growth factor ( Idgf4 ), thought to be responsive to changes in the social environment, was significantly down-regulated in workers from parasitized colonies; this may be an indication that parasitized workers are anticipating a shift toward a less worker-like phenotype in preparation for their reproductive rebellion. Our results provide the first evidence of early behavioural and neurogenomic responses of host workers toward the presence of an inquiline social parasite in a social insect.

中文翻译：

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寄主工人对社会性昆虫社会寄生虫入侵的行为和神经基因组反应

社会寄生虫与其宿主之间强烈的共同进化军备竞赛极大地塑造了双方的生活史特征。宿主应对寄生的主要策略之一是宿主工人的繁殖。我们缺乏对这些防御策略如何展开的机械理解，特别是宿主是否从一开始就表现出更微妙的策略来降低寄生成本。在这里，我们测试了以下假设，即在以产卵形式公开表达之前，工人对寄生的反应存在行为和神经基因组特征；我们使用社会寄生虫——纸黄蜂 Polistes sulcifer-Polistes dominula 的社会宿主系统来测试这一点。我们在寄生虫篡夺后立即描述了个体工人在皇后权和宿主菌落的社会互动网络中的位置，也就是工人的生殖叛逆明显之前的几周。寄生影响了网络中心性措施，与未寄生群体中的工人相比，寄生群体中的工人表现出更高的连通性和中心性。接下来，我们量化了与 Polistes 黄蜂生理和行为表型相关的五个基因的大脑基因表达水平。被认为对社会环境变化有反应的基因成虫盘生长因子（Idgf4）在来自寄生菌落的工人中显着下调；这可能表明被寄生的工人正在期待向不太像工人的表型转变，为他们的生殖叛逆做准备。我们的研究结果提供了宿主工人对社会昆虫中存在的无角社会寄生虫的早期行为和神经基因组反应的第一个证据。