The genetic basis and ground plan of eusocial worker evolution

主要的转变是个性的进化和地球上所有生命的等级结构的基础。在这些活动中，以前独立的个人聚集在一起，形成一个新的、更高级别的合作小组，就其本身而言，类似于个人。典型的例子是多细胞进化和共生进化。社会性社会是指一些成员(工人)对其他成员采取利他主义行为的社会，如蚂蚁、蜜蜂和黄蜂。进化生物学已经成功地解释了转变的最终原因，如多细胞进化和亲缘选择方面的优生性。但参与这些重大转变的实际基因仍然知之甚少。正如研究人员需要知道什么基因导致细胞成为体细胞(利他)或生殖系(生殖)细胞一样，我们也需要知道是什么基因导致社会中的工作者成为非生殖(利他)工作者或生殖工作者。该项目旨在通过使用新技术来确定工蚁利他主义与工蚁繁殖之间的遗传基础，以填补这一关键空白。研究系统将是大黄蜂Bombus terrestris，它的工作人员既可以是非生殖性不育利他主义者(卵巢不活跃)，也可以是生殖性蛋鸡。大黄蜂是两个独立进化的高级共生蜂类群--蜜蜂和无刺蜜蜂--的原始共生祖先，是最相似的生活群体。生殖工作者和非生殖工作者的基因表达以前在蜜蜂中得到了描述，但只有在原始群居昆虫中的研究才能为关键的基因表达差异提供进化的视角。使用B.terrestris，研究将(1a)确定在选定组织(脑、脂肪体和卵巢)中支撑生殖性和非生殖性工作者之间差异的基因表达差异，(1b)使用独立的基因表达分析来验证这些差异中最显著的，(1c)确定关键基因如何随着工蜂生殖表型的出现而随着时间的推移而变化表达(因此在调控途径中分离出上游和下游作用基因)，(2)建立如何通过基因表达变化来跟踪工人生殖表型的逆转，以及(3)检验一个对工人生殖表型进化具有很大影响的假说。这一假设，即生殖基础计划假说，提出工人的劳动分工(例如，任务随年龄的变化)是由遗传路径调节的，这些遗传路径是从调节工人非社会祖先的雌性生殖的路径(‘基础计划’)中增选出来的。这很重要，因为它代表了一个关键的例子，即像工人利他主义这样的进化新颖性可以通过现有基因途径的共同选择而产生。方法将包括实验室和现场实验、下一代测序(RNA-Seq转录组学)、定量聚合酶链式反应(qRT-PCR)和生物信息学。这项研究是基础性的，因为它涉及进化生态学、遗传学和转录组学中具有基本重要性和广泛兴趣的现象。它之所以新颖，是因为尽管越来越多的研究正在阐明社会进化的分子方面，但缺乏关于工人生殖能力丧失的遗传基础的进化论观点，工人生殖表型灵活性与基因表达之间的关系尚不清楚，重要的生殖基础计划假设需要验证。因此，这项工作将极大地促进我们对优生优育的遗传基础和重大转变的深刻理解。

The major transitions are foundational to the evolution of individuality and the hierarchical structure of all life on Earth. In these events, previously independent individuals come together to form a new, higher-level cooperative group resembling an individual in its own right. Classic examples are the evolution of multicellularity and eusociality. Eusocial societies are those in which some members (workers) act altruistically towards their fellow members, as in the ants, bees and wasps. Evolutionary biology has successfully explained the ultimate reasons for transitions like the evolution of multicellularity and eusociality in terms of kin selection. But the actual genes involved in these major transitions remain very poorly known. Just as researchers need to know what genes lead a cell to become a somatic (altruistic) or germline (reproductive) cell, so do we need to know what genes lead workers in eusocial societies to be non-reproductive (altruistic) workers or reproductive workers. This project aims to fill this key gap by using new technologies to determine the genetic basis of worker altruism versus worker reproduction in a eusocial insect. The study system will be the bumble bee, Bombus terrestris, whose workers can either be non-reproductive sterile altruists (with inactive ovaries) or reproductive egg-layers. Bumble bees are the living group most closely resembling the primitively eusocial common ancestor of the two independently-evolved advanced eusocial bee taxa, the honey bees and stingless bees. Gene expression in reproductive and non-reproductive workers has previously been profiled in honey bees, but only studies in primitively eusocial insects can provide an evolutionary perspective on the critical gene expression differences. Hence primitive eusociality in B. terrestris, and the position of B. terrestris in the bee phylogeny, make it an excellent study system for the proposed work.Using B. terrestris, the research will (1a) determine the gene expression differences within selected tissues (brain, fat body and ovary) that underpin the differences between reproductive and non-reproductive workers, (1b) validate the most salient of these differences using independent gene expression assays, (1c) determine how key genes change expression over time as the worker reproductive phenotype arises (so separating out upstream- and downstream-acting genes in the regulatory pathways), (2) establish how reversals in workers' reproductive phenotype are tracked by gene expression changes, and (3) test a highly influential hypothesis for the evolution of the worker reproductive phenotype. This hypothesis, the reproductive ground plan hypothesis, proposes that division of labour (e.g. changes in task with age) in workers is regulated by genetic pathways co-opted from pathways regulating reproduction in females of workers' non-social ancestors (the 'ground plan'). It is important because it represents a key example of the general idea that evolutionary novelties like worker altruism can arise through the co-option of existing gene pathways.Methods will consist of laboratory and field experiments, next-generation sequencing (RNA-Seq transcriptomics), quantitative PCR (qRT-PCR) and bioinformatics. The research is fundamental because it deals with phenomena of basic importance and broad interest in evolutionary ecology, genetics and transcriptomics. It is novel because, although a growing number of studies are elucidating molecular aspects of social evolution, an evolutionary perspective on the genetic basis of workers' loss of reproductive ability is lacking, the relationship between flexibility in the workers' reproductive phenotype and gene expression is not understood and the important reproductive ground plan hypothesis requires testing. The work will therefore substantially advance our deep understanding of the genetic foundations of eusociality and the major transitions.