The genetic basis and ground plan of eusocial worker evolution

主要的转变是地球上所有生命的个体进化和等级结构的基础。在这些事件中，以前独立的个体走到一起，形成一个新的，更高层次的合作团体，类似于一个独立的个体。经典的例子是多细胞性和真社会性的进化。真正的社会是那些其中一些成员（工人）对他们的同伴利他主义行为，如在蚂蚁，蜜蜂和黄蜂。进化生物学已经成功地解释了过渡的最终原因，如多细胞和真社会性的进化。但是参与这些主要转变的实际基因仍然知之甚少。正如研究人员需要知道是什么基因导致细胞成为体细胞（利他）或生殖细胞（生殖）一样，我们也需要知道是什么基因导致真社会的工人成为非生殖工人（利他）或生殖工人。该项目旨在通过使用新技术来确定真社会性昆虫中工人利他主义与工人生殖的遗传基础来填补这一关键空白。研究系统将是熊蜂，熊蜂terrestris，其工人可以是非生殖不育利他主义者（卵巢不活跃）或生殖产卵。熊蜂是与蜜蜂和无刺蜂这两个独立进化的高级真社会性蜜蜂类群的真社会性共同祖先最相似的生活类群。生殖和非生殖工人的基因表达以前曾在蜜蜂中进行过分析，但只有在昆虫中的研究才能提供关键基因表达差异的进化观点。因此，在B中存在原始的真社会性。terrestris，以及B的位置。terrestris在蜜蜂繁殖中的作用，使其成为一个很好的研究系统。terrestris，该研究将（1a）确定选定组织内的基因表达差异（脑，脂肪体和卵巢），这些差异是生殖和非生殖工人之间的差异的基础，（1b）使用独立的基因表达测定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改变表达（因此分离出调控途径中的上游和下游作用基因），（2）建立如何通过基因表达变化跟踪工蜂生殖表型的逆转，和（3）测试一个非常有影响力的假说的进化的工人生殖表型。这一假说，生殖地面计划假说，提出劳动分工（例如，随着年龄的变化，在任务）在工人是由遗传途径从途径增选调节生殖在女性工人的非社会祖先（“地面计划”）。这是重要的，因为它代表了一个关键的例子，一般的想法，进化的新奇，如工人利他主义可以通过现有的基因途径的共同选择出现。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PCR（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的基本重要性和广泛兴趣的现象。它是新颖的，因为虽然越来越多的研究正在阐明社会进化的分子方面，但缺乏对工蚁生殖能力丧失的遗传基础的进化观点，工蚁生殖表型的灵活性与基因表达之间的关系尚不清楚，重要的生殖基础假设需要检验。因此，这项工作将大大推进我们对真社会性的遗传基础和主要转变的深刻理解。

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.