The molecular basis of phenotypic transitions in eusocial evolution

社会进化中表型转变的分子基础

• 批准号: NE/M012913/2
• 负责人: Seirian Sumner
• 金额: $ 63.52万
• 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: 2016
• 资助国家: 英国
• 起止时间: 2016 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FM012913%2F2
• 关键词: molecular; basis; phenotypic; transitions; eusocial

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.

主要的进化转型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。一个突出的问题是，这些转变在多大程度上是通过祖先基因和性状的解耦，或新的基因组材料进化为新的性状而产生的。这一点很重要，因为它告诉我们分子机制是否限制了主要的进化变化。这个项目的目的是探索一个主要的进化转变的分子基础.社会性的进化是八个主要的进化转变之一，可以在生物组织的各个层次上找到例子：基因聚集成基因组，细胞聚集成多细胞生物，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较大的较高级别的实体，进行分工、合作和发挥专门作用。在向社会性过渡的过程中，生殖和非生殖任务的祖先特征被认为是分离的，形成了群体成员之间的劳动分工。例如，在从单细胞到多细胞的转变中，细胞成为专门的生殖（配子）或非生殖（体细胞）单位;在昆虫从独居到社会性的转变中，个体成为专门的产卵者（女王）或provisioners（工人）。祖先特征与社会特征的分离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型期间出现的新行为或特征的演变。其中包括：（1）从一个孤独的祖先状态进化出群体生活;（2）从一个祖先的自私行为进化出利他行为;（3）从灵活的（不承诺的）表型进化出不灵活的（承诺的）表型。因此，将向社会性的转变简单地定义为祖先生殖和供给特征的重组可能过于简单化，因为它没有解释基本新特征的出现。该项目将确定真社会性黄蜂中祖先特征（生殖和供应）和新社会特征（群体生活，利他主义和承诺种姓）脱钩的基因和蛋白质。真社会性昆虫是研究社会性机制和进化的有力模型。真社会性黄蜂包括各种社会复杂性的物种代表，从可以选择是否社会化的物种，到高度复杂的，具有极端任务专家和复杂社会的忠诚社会。我们将产生基因组序列和查询表型特异性转录组和蛋白质组的5种真社会性黄蜂。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。我们将联合收割机现场操作实验与最先进的基因组学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。该工作方案包括对代表社会进化不同阶段的黄蜂进行3项独立的物种一级研究。我们使用现场操作实验作为一种“自上而下”的方式来识别与每个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利用的方法，可能会导致重大的科学突破。因此，我们的方法旨在揭示社会行为中关键创新背后的近似机制，以解决进化中这一重大转变的性质的最终问题。

项目成果

DNA barcodes and new primers for nature's pest controllers: the social wasps.

DNA 条形码和自然害虫控制者的新引物：群居黄蜂。

• DOI: 10.1139/gen-2019-0193
• 发表时间: 2021
• 期刊: Genome
• 影响因子: 3.1
• 作者: Onah IE

Why we love bees and hate wasps

为什么我们喜欢蜜蜂而讨厌黄蜂

• DOI: 10.1111/een.12676
• 发表时间: 2018
• 期刊: Ecological Entomology
• 影响因子: 2.2
• 作者: Sumner S

Diminishing returns drive altruists to help extended family.

• DOI: 10.1038/s41559-020-01382-z
• 发表时间: 2021-04
• 期刊: Nature ecology & evolution
• 影响因子: 16.8
• 作者: Kennedy P;Sumner S;Botha P;Welton NJ;Higginson AD;Radford AN
• 通讯作者: Radford AN

Behavioural and neurogenomic responses of host workers to social parasite invasion in a social insect

• DOI: 10.1007/s00040-020-00765-6
• 发表时间: 2020-05-15
• 期刊: INSECTES SOCIAUX
• 影响因子: 1.3
• 作者: Cini, A.;Branconi, R.;Sumner, S.
• 通讯作者: Sumner, S.

Altruism in a volatile world.

• DOI: 10.1038/nature25965
• 发表时间: 2018-03-15
• 期刊: Nature
• 影响因子: 64.8
• 作者: Kennedy P;Higginson AD;Radford AN;Sumner S
• 通讯作者: Sumner S