Vitellogenin-like A–associated shifts in social cue responsiveness regulate behavioral task specialization in an ant

Division of labor and task specialization explain the success of human and insect societies. Social insect colonies are characterized by division of labor with workers specializing on brood care early and foraging later in life. Theory posits that this task switching requires shifts in responsiveness to task-related cues, yet experimental evidence is weak. Here we show that a Vitellogenin (Vg) ortholog identified in a RNAseq study on the ant Temnothorax longispinosus is involved in this process: Using phylogenetic analyses of Vg and Vg-like genes, we firstly show that this candidate gene does not cluster with the intensively studied honey bee Vg, but falls into a separate Vg-like A cluster. Secondly, an experimental knockdown of Vg-like A in the fat body caused a reduction in brood care and an increase in nestmate care in young ant workers. Nestmate care is normally exhibited by older workers. We demonstrate experimentally that this task switch is at least partly based on Vg-like-A-associated shifts in responsiveness from brood to worker cues. We thus reveal a novel mechanism leading to early behavioral maturation via changes in social cue responsiveness mediated by Vg-like A and associated pathways, which proximately play a role in regulating division of labor.

劳动分工与任务特化是人类社会与昆虫社会得以成功的核心动因。社会昆虫群落以劳动分工为典型特征：工蚁在生命早期特化承担育幼任务，后期则转向觅食行为。现有理论推测，此类任务转换需要工蚁调整对任务相关线索的响应性，但相关实验证据仍较为匮乏。本研究证实，在长刺瘤颚蚁（Temnothorax longispinosus）的RNA测序（RNA-seq）研究中鉴定得到的卵黄蛋白原（Vitellogenin, Vg）同源基因参与了这一过程：通过对Vg及类Vg基因开展系统发育分析，我们首先发现该候选基因并未与被广泛深入研究的蜜蜂Vg聚类为一支，而是独立归入类Vg A（Vg-like A）簇。其次，对年轻工蚁脂肪体内的Vg-like A基因进行实验性敲低后，其育幼行为显著减少，而同巢同伴照料行为则有所提升——这类行为通常仅见于年长工蚁。我们通过实验证明，该任务转换至少部分源于Vg-like A介导的、从育幼线索到同巢同伴线索的响应性偏移。综上，本研究揭示了一种全新的行为早熟机制：通过Vg-like A及其相关通路介导社会线索响应性的改变，该机制在调控劳动分工的近因层面发挥关键作用。