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

NSFDEB-NERC 进化重大转变的进化基因组学

• 批准号: NE/S011218/1
• 负责人: Seirian Sumner
• 金额: $ 48.82万
• 依托单位: University College London
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2019
• 资助国家: 英国
• 起止时间: 2019 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FS011218%2F1
• 关键词: NSFDEB; NERC; evolutionary; genomics; major

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.

20多年前，解释生物复杂性出现的进化中的八个主要转变被定义，其中之一是社会性(或超有机体)的进化。在理解支撑重大进化转变的理论方面取得了重大进展；然而，我们缺乏对重大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断断续续的进化过程发生的。区分它们对于我们理解生物的复杂性、自然界和我们自己的起源是至关重要的。我们通过对支撑重大转变的分子过程制定一个新的预测框架来解决这个问题，并使用对16种蜜蜂和蜜蜂的社会性的多水平基因组分析来实证检验这些预测。最近关于重大转变的理论扩展了社会的概念，跨越了生物组织的各个层面。例如，基因在原细胞中形成了一个社会，原生细胞形成了一个多细胞社会，昆虫成为了有社会的超级有机体。所有社会的一个共同特征是在群体内出现不可逆转的承诺表型(例如，昆虫群体中的蜂王和工蚁；多细胞生物体中的组织类型)。这些类比很有说服力，但在很大程度上仍是概念性的，因为我们不了解重大转变(特别是不可逆转性)产生的进化过程。这一点很重要，因为进化过程的性质决定了我们理论理解所基于的假设。因此，我们的首要目标是确定向超有机体的重大转变是通过渐进的过程还是断断续续的过程，使用社会昆虫(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，超级生物是通过分子过程中许多微小变化的逐渐积累而进化的。然而，新的概念性工作表明，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”共荣的特征，但它们并不表现出表明重大转变的一组具体特征(即相互依赖；承诺的(不可逆转的)种姓)。这隐含着这样一种假设，即这种转变需要表型性状的一步改变。最近对黄蜂社会性进化的经验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(以及在社会性的起源)。最近的这些研究提出了一个耐人寻味的问题，即向超有机体的重大转变是否是断断续续的进化的例子，而不是从许多微小的微观进化过程中逐渐出现的特征。在这个提案中，我们引入了一个新的框架来解剖一个重大进化转变的进化过程：我们识别可能代表一条渐进的或断断续续的超有机体的典型分子特征。我们建议对这些预测进行检验。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，这些数据跨越了从孤立个体到超级生物的过渡：其中包括新的基因组、染色体作图、新的转录体和蛋白质组。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转变。最后，我们将召集对生物组织范围内的重大转变感兴趣的专家，讨论在进化的重大转变的机制基础上，存在一般分子签名的程度。如果断断续续的进化过程在推动重大转变方面很重要，那么将需要新类型的理论模型。

项目成果

The molecular basis of socially-mediated phenotypic plasticity in a eusocial paper wasp

真社会性纸黄蜂社会介导的表型可塑性的分子基础

• DOI: 10.21203/rs.3.rs-43815/v1
• 发表时间: 2020
• 作者: Taylor B

Social complexity, life-history and lineage influence the molecular basis of castes in vespid wasps.

• DOI: 10.1038/s41467-023-36456-6
• 发表时间: 2023-02-24
• 期刊: NATURE COMMUNICATIONS
• 影响因子: 16.6
• 作者: Wyatt, Christopher Douglas Robert;Bentley, Michael Andrew;Taylor, Daisy;Favreau, Emeline;Brock, Ryan Edward;Taylor, Benjamin Aaron;Bell, Emily;Leadbeater, Ellouise;Sumner, Seirian
• 通讯作者: Sumner, Seirian

Social complexity, life-history and lineage influence the molecular basis of caste in a major transition in evolution

社会复杂性、生活史和血统在进化的重大转变中影响种姓的分子基础

• DOI: 10.21203/rs.3.rs-835604/v1
• 发表时间: 2021
• 作者: Wyatt C