Data from: Vitellogenin and vitellogenin receptor gene expression is associated with male and female parenting in a subsocial insect

Complex social behaviour in Hymenoptera has been hypothesized to evolve by co-opting reproductive pathways (the ovarian ground plan hypothesis, OGPH) and gene networks (the reproductive ground plan hypothesis, RGPH). In support of these hypotheses, in eusocial Hymenoptera where there is reproductive division of labour, the yolk precursor protein vitellogenin (Vg) influences the expression of worker social behaviour. We suggest that co-opting genes involved in reproduction may occur more generally than just in the evolution of eusociality; i.e. underlie earlier stages of social evolution such as the evolution of parental care, given that reproduction and parental care rarely overlap. We therefore examined vitellogenin (vg) gene expression associated with parental care in the subsocial beetle Nicrophorus vespilloides. We found a significant reduction in the expression of vg and its receptor, vgr, in head tissue during active parental care, and confirmed that the receptor is expressed in the brains of both sexes. Ours is the first study to show that vgr is expressed in the brain of a non-eusocial insect. Given the association between behaviour and gene expression in both sexes, and the presence of vitellogenin receptors in the brain, we suggest that Vg was co-opted early in the evolution of sociality to have a regulatory function. This extends the association of Vg in parenting to subsocial species and outside of the Hymenoptera, and supports the hypothesis that the OGPH is general and that heterochrony in gene expression is important in the evolution of social behaviour and precedes subsequent evolutionary specialization of social roles.

膜翅目（Hymenoptera）昆虫的复杂社会行为，曾被假设通过共用生殖通路（卵巢地面计划假说，OGPH）与基因网络（生殖地面计划假说，RGPH）演化而来。为支持上述假说，在存在生殖分工的真社会性膜翅目昆虫中，卵黄原蛋白（vitellogenin, Vg）可调控职虫的社会行为表达。我们提出，共用生殖相关基因的演化过程或许比真社会性起源更为普遍；也就是说，该过程可能是社会演化早期阶段（如双亲抚育行为的演化）的基础——鉴于生殖与双亲抚育极少同时发生。为此，我们针对亚社会性甲虫Nicrophorus vespilloides中与双亲抚育相关的卵黄原蛋白（vg）基因表达展开了检测。我们发现，在活跃双亲抚育期间，头部组织中vg及其受体vgr的表达量显著下调，并证实该受体在雌雄两性的大脑中均有表达。本研究为首个证实非真社会性昆虫大脑中存在vgr表达的研究。鉴于雌雄两性均存在行为与基因表达的关联，且大脑中存在卵黄原蛋白受体，我们提出，Vg早在社会性演化早期就被共用以发挥调控功能。这一发现将Vg与双亲抚育的关联拓展至亚社会性类群以及膜翅目之外的类群，并支持了以下假说：OGPH具有普适性，且基因表达的异时性（heterochrony）在社会行为演化中发挥关键作用，同时也是后续社会角色演化特化的前置条件。