The evolution of altruistic workers in termites and their molecular underpinnings

像蜜蜂和蚂蚁这样的群居昆虫是社会进化的教科书范例。它们的特点是由一个或几个繁殖个体进行生殖分工，而其他群体成员执行所有其他任务，如照顾后代和防御。这类似于多细胞生物的劳动分工，细胞专门负责生殖（种系）和躯体组织执行所有其他任务。因此，群居昆虫被称为“超级有机体”，群居性的进化被归类为一个主要的进化转变。白蚁是社会性昆虫的第二大分支，对它的研究较少。它们都是群居昆虫因为有蜂后、蜂王和不育的士兵。然而，工人利他主义的程度在不同的血统之间差别很大。它的范围从(i)在生殖中发育的全能性“假工人”和（ii）生殖选择减少的非无菌“真工人”到（iii）无菌“真工人”。只有第三种类型有资格通过主要的进化转变。这些工蜂类型的出现与该物种的社会复杂性和生态一致。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种同样简单的假设的模糊信号。此外，其他特征，如发育，也不能给出明确的答案。因此，围绕这些假说，关于白蚁社会性进化史的争论持续了近40年。我们的目标是利用基因组学和转录组学方法揭示工人发展的分子基础。通过研究不同程度工蚁利他主义在白蚁系统发育中的关键物种，我们将确定同源基因调控网络。它们将使我们能够推断出工人利他主义的进化史，检验两种可供选择的假设，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个主要进化转变的历史。最后，它将使未来的研究能够将生态特征映射到转变中，并推断出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.