The evolution of altruistic workers in termites and their molecular underpinnings

群居昆虫，如蜜蜂和蚂蚁，是社会进化的教科书。它们的特点是与一个或几个繁殖个体进行生殖分工，而其他群体成员则执行所有其他任务，如育苗和防御。这类似于多细胞生物体的分工，由专门负责生殖的细胞(生殖系)和体细胞组织执行所有其他任务。因此，群居昆虫被称为超级生物，优势性的进化被归类为一次重大的进化转变。白蚁是群居昆虫的第二大谱系，对其研究较少。它们都是社会昆虫，因为有女王、国王和不育的士兵的存在。然而，工人的利他主义程度在不同的世系之间存在着巨大的差异。它的范围从(I)繁衍后代的全能“假工种”和(Ii)生殖选择减少的非不育“真工种”，到(Iii)不育的“真工种”。只有第三种类型才有资格通过一个重大的进化转变。这些工蚁类型的出现与该物种的社会复杂性和生态环境相一致。然而，工人利他主义的进化史尚不清楚。系统发育重建提供了两个可供选择的、同样简约的假设的模糊信号。此外，其他特征，如发展，也不会产生明确的答案。因此，围绕这些假说，白蚁社会性的进化史有近40年的争论。我们的目标是利用基因组和转录组方法揭示工蚁发育的分子基础。通过研究白蚁系统发育过程中不同程度的工蚁利他主义的关键物种，我们将识别出同源的基因调控网络。它们将使我们能够推断工人利他主义的进化史，检验两种可供选择的假说，从而解决一个长期存在的争议。我们的研究也提供了一个难得的机会来追踪一次重大进化转变的历史。最后，它将使未来的研究能够将生态特征映射到转变，并推断社会进化的潜在驱动力。

Eusocial insects, like honeybees and ants, are textbook examples of social evolution. They are characterized by reproductive division of labour with a one or a few reproducing individuals, while the other colony members perform all other tasks such as brood care and defence. This resembles division of labour in multicellular organisms with cells specialized in reproduction (germline) and somatic tissues performing all other tasks. Accordingly, social insects have been called ‘superorganisms’ and the evolution of eusociality has be classified as a major evolutionary transition.Termites, the second major lineage of social insects, are less studied. They are all eusocial insects because of the presence of queens and kings and sterile soldiers. Yet, the degree of worker altruism varies profoundly between lineages. It ranges from (i) totipotent ‘false workers’ which develop in reproductives and (ii) non-sterile ‘true workers’ with reduced reproductive options, to (iii) sterile ‘true workers’. Only the third type qualifies as having passed a major evolutionary transition. The occurrence of these worker types aligns with the social complexity and ecology of the species. Yet the evolutionary history of worker altruism is unclear. Phylogenetic reconstructions provide an ambiguous signal of two alternative, equally parsimonious hypotheses. Also other traits, like development, do not yield clear answers. Thus, there is a nearly 40 years’ debate on the evolutionary history of termite sociality centring on these hypotheses.We aim to uncover the molecular underpinnings of worker development using genomic and transcriptomic approaches. By studying crucial species of different degrees of worker altruism across the termites’ phylogeny, we will identify homologous gene regulatory networks. They will allow us to deduce the evolutionary history of worker altruism, test the two alternative hypotheses, and thus solve a long-standing controversy. Our study also offers a rare opportunity to track the history of a major evolutionary transition. Finally, it will allow future studies to map ecological traits to transitions and infer potential driving forces of social evolution.