NSFDEB-NERC The evolutionary genomics of a major transition in evolution

20多年前，人们定义了解释生物复杂性出现的8个主要进化转变，其中一个是社会性（或超有机体）的进化。在理解支持重大进化转变的理论方面取得了重大进展；然而，我们缺乏对主要转变的进化模式和过程的综合理解。一个新颖而及时的问题是，重大转变是通过渐进的还是间断的进化过程产生的。区分这些是我们理解生物复杂性、自然世界和我们自身起源的基础。为了解决这个问题，我们对主要转变的分子过程制定了新的预测框架，并利用16种蜜蜂和黄蜂的社会性多层次基因组分析对这些预测进行了实证检验。最近关于重大转变的理论将社会的概念扩展到了生物组织的各个层面。例如，基因在原始细胞中形成社会，原始细胞形成多细胞社会，昆虫成为真社会超级有机体。所有社会的一个共同特征是群体内出现不可逆转的表型（例如，昆虫群落中的蜂王和工蜂；多细胞生物中的组织类型）。这些类比是令人信服的，但在很大程度上仍然是概念性的，因为我们不理解主要转变（特别是不可逆性）产生的进化过程。这一点很重要，因为进化过程的本质塑造了我们的理论理解所基于的假设。因此，我们的首要目标是确定向超级有机体的主要转变是通过渐进的还是间断的过程进化的，使用社会性昆虫（主要转变中研究得最好的）作为模型系统。直到最近，所有对群居昆虫的研究都认为超级有机体是通过分子过程中许多微小变化的逐渐积累而进化而来的。然而，新的概念性研究表明，主要的转变可能会通过一个不那么渐进的过程发生。这一观点认为，尽管许多昆虫物种表现出“经典”的社会性特征，但它们并没有表现出表明重大转变的特定特征（即相互依赖；承诺（不可逆的）种姓）。其中隐含的假设是，这种转变需要表型性状的阶跃变化。最近对黄蜂社会性进化的实证分析暗示了类似的模式，种姓承诺突然出现在黄蜂的社会性中（并在起源处）。这些最近的研究提出了一个有趣的问题，即向超有机体的主要转变是否是间断进化的一个例子，而不是从许多小的微进化过程中逐渐出现的特征。在本提案中，我们引入了一个新的框架来剖析一个主要进化转变的进化过程：我们确定了可能代表一个渐进或间断的超有机体路径的假定分子特征。我们打算检验这些预测。首先，我们将为16种蜜蜂和黄蜂生成适当的多层基因组数据集，这些数据集跨越了从孤立个体到超级有机体的过渡：这些数据集包括新的基因组、染色体作图、新的转录组和蛋白质组。然后，我们将使用这些数据集来找出哪条进化路线（渐进的或间断的）最能解释向超有机体的过渡。最后，我们将汇集对生物组织的重大转变有共同兴趣的专家，讨论在进化中重大转变的机制基础上存在一般分子特征的程度。如果间断的进化过程在推动重大转变方面很重要，那么就需要新的理论模型。

Over 20 years ago, eight major transitions in evolution that explain the emergence of biological complexity were defined, one of which is the evolution of sociality (or superorganismality). Significant advances have been made in understanding the theory underpinning major evolutionary transitions; however, we lack an integrated understanding of the evolutionary patterns and processes of the major transitions. A novel and timely question is whether major transitions arise via gradual or punctuated evolutionary processes. Distinguishing between these is fundamental to our understanding of biological complexity, the natural world and our own origins. We address this question by formulating new a predictive framework on the molecular processes underpinning major transitions, and testing these predictions empirically using multi-level genomic analyses of sociality in 16 species of bees and wasps.Recent theory on major transitions has extended the concept of the society across levels of biological organization. E.g. genes form a society in protocells, protist cells form a multicellular society, and insects become eusocial superorganisms. A common trait for all societies is the emergence of irreversibly committed phenotypes within the group (e.g. queens and workers in insect colonies; tissue types in multicellular organisms). These analogies are compelling but remain largely conceptual because we do not understand the evolutionary processes by which major transitions (and specifically irreversibility) arise. This is important because the nature of the evolutionary processes shapes the assumptions on which our theoretical understanding is based. Our overarching goal, therefore, is to determine whether the major transition to superorganismality evolved via gradual or punctuated processes, using social insects (the best studied of the major transitions) as a model system. Until very recently, all studies in social insects assumed that superorganisms evolved via the gradual accumulation of many small changes in molecular processes. However, new conceptual work suggests that the major transition may occur via a less gradual process. This idea proposes that, although many insect species display the hallmarks of 'classic' eusociality, they do not express the specific set of traits that indicate a major transition (i.e. mutual dependency; committed (irreversible) castes). Implicit in this is the assumption that the transition requires a step change in phenotypic traits. A recent empirical analysis of the evolution of sociality in wasps implies a similar pattern, with caste commitment appearing suddenly in (and at the origin of) sociality in wasps. These recent studies raise the intriguing question of whether the major transition to superorganismality is an example of punctuated evolution and not a trait that emerges gradually from many, small micro-evolutionary processes. In this Proposal we introduce a new framework for dissecting the evolutionary processes of a major evolutionary transition: we identify putative molecular signatures that are likely to typify a gradual or punctuated route to superorganismality. We propose to test these predictions. First, we will generate appropriate multi-layered genomic datasets for 16 species of bees and wasps that span the transition from solitary individuals to superorganisms: these include new genomes, chromosome mapping, new transcriptomes and proteomes. We will then use these datasets to find out which of the evolutionary routes (gradual or punctuated) best explain the transition to superorganismality. Finally, we will bring together experts who share an interest in major transitions across the spectrum of biological organization to discuss the extent to which there are general molecular signatures on the mechanistic basis of a major transition in evolution. If punctuated evolutionary processes are important in driving major transitions, new types of theoretical models will be required.