Evolution and molecular basis of caste differentiation in bees

蜜蜂种姓分化的进化和分子基础

• 批准号: BB/M001482/1
• 负责人: Andrew Bourke
• 金额: $ 49.9万
• 依托单位: University of East Anglia
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2014
• 资助国家: 英国
• 起止时间: 2014 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=BB%2FM001482%2F1
• 关键词: Evolution; molecular; basis; caste; differentiation

A fundamental topic in biology concerns how the switching on and off (differential expression) of genes creates morphological and behavioural diversity. 'Polyphenism' (when different adult morphs arise from the same genome) provides systems in which to address how differential gene expression creates diversity at the level of whole organisms. A major example of polyphenism occurs in the ants, bees and wasps, in which female larvae develop into one of two castes, queens or workers. It is already known that the huge differences between the castes in size, shape, reproduction and behaviour stem from differential gene expression. Hence the process by which castes develop (caste differentiation) allows us to investigate how differential gene expression generates polyphenism. However, our understanding of the genetic basis of caste differentiation is in its early stages. The genes involved, their evolutionary background and the role of microRNAs (miRNAs, small RNA molecules important in regulating gene expression) are all poorly known.In this project we will use bumble bees (Bombus) to elucidate the evolution and regulation of the genes influencing queen-worker caste differentiation. Bumble bees represent excellent models for this purpose. First, species vary in the number of critical stages of larval caste determination (when differentiation is initiated) and the evolutionary history of this variation is known. One species (B. terrestris) has two critical stages in female larvae (early- and late-instar), with the early critical stage being secondary (evolutionarily derived); another (B. hypnorum) has one such stage (late-instar larvae only); and 'cuckoo' bumble bees such as B. vestalis have no critical stages, as they have secondarily lost the worker caste and all females are queens that reproduce in nests of other Bombus species. Second, we have discovered that a miRNA, miR-6001-5p, is overexpressed in queen-destined late-instar B. terrestris larvae, suggesting that it regulates genes influencing caste.These data allow us to create a predictive framework for expected patterns of differential expression in caste-associated genes and miR-6001-5p in Bombus. Specifically, if the critical stages are conserved in evolution via regulation of the same genes, and new critical stages are gained via additional regulatory pathways, B. terrestris and B. hypnorum should share common patterns of differential gene expression among late- but not among early-instar larvae. Likewise, patterns of gene expression specific to worker-destined larvae in these two species should be absent in the cuckoo species B. vestalis. Furthermore, if the role of miR-6001-5p is evolutionarily conserved, similar patterns of expression of miR-6001-5p and its target genes should occur across queen-destined late-instar larvae of all three Bombus species.We will test these predictions by comparing profiles of differentially expressed genes across larval phenotypes, by using our expression data to predict targets of miR-6001-5p and by conducting assays to validate these targets. The proposed work will provide a comprehensive understanding of the evolutionary and genetic basis of changes in the number of critical stages of caste determination in eusocial insects and will elucidate the role of a miRNA in caste differentiation. As well as addressing the fundamental topic of the genetic regulation of polyphenism, the work is novel because no previous study has exploited a comparable predictive framework. It is timely because gene profiling by next-generation sequencing now provides the tools required and our existing data have created an exciting opportunity to make rapid headway in understanding how miRNAs affect caste differentiation. Finally the work fits BBSRC's strategic priorities because it could reveal means of manipulating worker production to maximize pollination services to horticulture provided by commercially-reared bumble bee colonies.

生物学的一个基本主题是关于基因的开启和关闭（差异表达）如何产生形态和行为的多样性。“多表型”（当不同的成年变体来自同一基因组时）提供了一个系统，在这个系统中，研究不同的基因表达如何在整个生物体的水平上创造多样性。多表型的一个主要例子发生在蚂蚁、蜜蜂和黄蜂身上，在这些动物中，雌性幼虫发育成两个等级之一，即蚁后或工蜂。我们已经知道，种姓之间在大小、形状、繁殖和行为上的巨大差异源于不同的基因表达。因此，种姓发展的过程（种姓分化）使我们能够研究差异基因表达如何产生多表型。然而，我们对种姓分化的遗传基础的理解还处于早期阶段。所涉及的基因，它们的进化背景和microrna （miRNAs，在调节基因表达中重要的小RNA分子）的作用都知之甚少。在这个项目中，我们将用大黄蜂（Bombus）来阐明影响工后种姓分化的基因的进化和调控。大黄蜂代表了这方面的优秀典范。首先，物种在幼虫等级决定的关键阶段（当分化开始时）的数量不同，这种变化的进化史是已知的。一个物种（B. terrestris）的雌性幼虫有两个关键阶段（早期和晚期），早期的关键阶段是次要的（进化衍生的）；另一种（B. hypnorum）有一个这样的阶段（只有后期幼虫）；而像B. vestalis这样的“布谷鸟”大黄蜂没有关键阶段，因为它们已经二级失去了工蜂等级，所有的雌性都是在其他大黄蜂物种的巢穴中繁殖的女王。其次，我们发现一种miRNA miR-6001-5p在蚁后命中的晚龄B. terrestris幼虫中过表达，表明它调节影响种姓的基因。这些数据使我们能够为Bombus中种姓相关基因和miR-6001-5p的预期差异表达模式创建一个预测框架。具体来说，如果关键阶段是通过相同基因的调控在进化中保存下来的，而新的关键阶段是通过额外的调控途径获得的，那么陆地芽孢杆菌和海芽孢杆菌应该在后期而不是早期幼虫中具有共同的差异基因表达模式。同样，在这两种物种中，特定于工蚁幼虫的基因表达模式在布谷鸟物种B. vestalis中应该不存在。此外，如果miR-6001-5p的作用在进化上是保守的，那么miR-6001-5p及其靶基因的表达模式应该出现在所有三种蜂属的蜂王终代晚期幼虫中。我们将通过比较不同幼虫表型差异表达基因的谱，通过使用我们的表达数据来预测miR-6001-5p的靶标，并通过进行分析来验证这些靶标，来测试这些预测。这项工作将提供对社会性昆虫种姓决定关键阶段数量变化的进化和遗传基础的全面理解，并将阐明miRNA在种姓分化中的作用。除了解决多表型遗传调控的基本问题外，这项工作还很新颖，因为以前没有研究利用过类似的预测框架。这是及时的，因为下一代测序的基因分析现在提供了所需的工具，我们现有的数据已经创造了一个令人兴奋的机会，在理解mirna如何影响种姓分化方面取得快速进展。最后，这项工作符合BBSRC的战略重点，因为它可以揭示操纵工蜂生产的方法，以最大限度地提高商业饲养的大黄蜂群体为园艺提供的授粉服务。

项目成果

MicroRNAs Associated with Caste Determination and Differentiation in a Primitively Eusocial Insect.

• DOI: 10.1038/srep45674
• 发表时间: 2017-03-31
• 期刊: Scientific reports
• 影响因子: 4.6
• 作者: Collins DH;Mohorianu I;Beckers M;Moulton V;Dalmay T;Bourke AF
• 通讯作者: Bourke AF

Gene expression during larval caste determination and differentiation in intermediately eusocial bumblebees, and a comparative analysis with advanced eusocial honeybees.

• DOI: 10.1111/mec.15752
• 发表时间: 2021-03
• 期刊: Molecular ecology
• 影响因子: 4.9
• 作者: Collins DH;Wirén A;Labédan M;Smith M;Prince DC;Mohorianu I;Dalmay T;Bourke AFG
• 通讯作者: Bourke AFG