The molecular basis of phenotypic transitions in eusocial evolution

重大的进化转变是自然界多样性的关键来源。然而，我们对它们产生的机制，特别是它们的分子基础知之甚少。一个悬而未决的问题是，这些转变在多大程度上是通过祖先基因和性状的分离或新基因组材料的进化来实现的。这一点很重要，因为它告诉我们，分子机制是否制约着重大的进化变化。这个项目旨在探索分子基础，这是一个重大的进化转变。社会性的进化是八大进化转变之一，在生物组织的各个层面上都可以找到这样的例子：基因聚集成基因组，细胞聚集成多细胞有机体，昆虫聚集成社会。在每一种情况下，较小的实体联合起来，组成具有分工、合作和专门作用的较大的较高级别的实体。在向社会性转变的过程中，生殖和非生殖任务的祖先特征被认为是脱钩的，从而在群体成员之间形成了分工。例如，在从单细胞到多细胞的转变中，细胞成为专门化的生殖性(配子)或非生殖性(体细胞)单位；在昆虫从独居生活向社会性的转变中，个体变成专门化的产蛋者(女王)或供给者(工蚁)。祖先特征的脱钩形成社会特征是解释社会性进化机制的主要假说。然而，脱钩假说没有考虑到在重大转变期间出现的新行为或特征的演变。这包括：(1)群体从孤立的祖先状态进化而来；(2)利他行为从祖先的自私行为进化而来；(3)僵化(承诺)表型从灵活(未承诺)表型进化而来。因此，将向社会性的转变简单地定义为祖先生殖和供养特征的重新组织可能过于简单化，因为它没有考虑到基本新奇特征的出现。该项目将确定在群居黄蜂中导致祖先特征(繁殖和供应)和新的社会特征(群体生活、利他主义和忠诚的种姓)脱钩的基因和蛋白质。社会性昆虫是研究社会性机制和进化的有力模型。从可以选择是否社交的物种，到具有极端任务专家和复杂社会的高度复杂、承诺的社会，社会上的黄蜂包括各种社会复杂性的物种代表。我们将生成基因组序列，并询问5种真社会性黄蜂的表型特异性转录本和蛋白质组。这项工作将是第一次系统地询问整个社会多样性范围内昆虫行为的分子基础。我们将现场操作实验与最先进的基因组和生物信息学方法相结合，在生态相关的背景下剖析社会行为。该工作方案包括3个独立的物种层面的黄蜂研究，代表了社会进化的不同阶段。我们使用现场操作实验作为一种“自上而下”的方式来识别与每一种行为创新相关的基因。然后，我们利用这些研究产生的数据集来解决社会进化的分子基础上的比较问题。转录组学和蛋白质组学的结合是一种强大但很少被利用的方法，很可能导致重大的科学突破。因此，我们的方法试图揭示社会行为关键创新背后的最接近的机制，以解决关于这一重大进化转变的性质的终极问题。

Major evolutionary transitions are key sources of diversity in the natural world. Yet we understand little about the mechanisms by which they arise, and specifically their molecular basis. An outstanding question is to what extent do these transitions arise via decoupling of ancestral genes and traits, or the evolution of new genomic material for new traits. This is important as it tells us whether molecular mechanisms constrain major evolutionary change. This project aims to explore the molecular basis a major evolutionary transition. The evolution of sociality is one of eight major evolutionary transitions and examples can be found across levels of biological organisation: genes aggregate into genomes, cells into multicellular organisms, and insects into societies. In each case, smaller entities unite to form larger higher-level entities, with division of labour, cooperation and specialized roles. In the transition to sociality the ancestral traits of reproduction and non-reproductive tasks, are thought to be decoupled to form a division of labour among group members. For example, in the transition from single- to multi-cellularity, cells become specialised as reproductive (gametes) or non-reproductive (somatic) units; in the transition from solitary living to sociality in insects, individuals become specialised as egg-layers (queens) or provisioners (workers). The decoupling of ancestral traits to form social traits is the main hypothesis to explain the mechanism by which sociality evolves. However, the decoupling hypothesis fails to consider the evolution of new behaviours or traits that arise during major transitions. These include: (1) the evolution of group living from a solitary, ancestral state; (2) the evolution of altruistic behaviour from an ancestral, selfish behaviour; (3) the evolution of inflexible (committed) phenotypes, from flexible (uncommitted) phenotypes. Therefore, defining the transition to sociality simply as a re-organisation of ancestral reproductive and provisioning traits maybe too simplistic, as it does not account for the emergence of essential novel traits. This Project will identify the genes and proteins underlying the decoupling of ancestral traits (reproduction and provisioning) and novel social traits (group living, altruism and committed castes) in the eusocial wasps. Eusocial insects are powerful models for studying the mechanisms and evolution of sociality. The eusocial wasps include species representatives across the spectrum of social complexity from species that can choose whether to be social or not, to highly complex, committed societies with extreme task specialists and complex societies. We will generate genome sequences and interrogate phenotype-specific transcriptomes and proteomes for 5 species of eusocial wasps. This work will be the first systematic interrogation of the molecular basis of insect behaviours across the spectrum of social diversity. We combine field manipulation experiments with state-of-the art genomic and bioinformatic approaches to dissect social behavior in an ecologically relevant context. The Work Programme consists of 3 stand-alone species-level studies on wasps representing different stages in social evolution. We use field manipulation experiments as a 'top-down' way of identifying genes associated with each behavioural innovation. Then, we exploit the datasets generated by these studies to address comparative questions on the molecular basis of social evolution. The combination of transcriptomics and proteomics is a powerful yet little exploited approach that is likely to lead to significant scientific breakthroughs. Our approach, therefore, seeks to uncover proximate mechanisms underlying key innovations in social behaviour in order to address ultimate questions on the nature of this major transition in evolution.