The evolution and genetics of superorganisms

进化被几个重大事件打断，这些事件从根本上增加了生命的复杂性和生物多样性。这些改变游戏规则的进化包括性、多细胞和社会性的进化。动物的社会性进化了好几次，涉及到个体之间的劳动分工，这些个体为了群体的利益而合作。在独居物种中，基因突变可以影响个体的特征，这些突变可以随着个体的适应性而传播或减弱。然而，群居动物具有集体的“超有机体”特征，这些特征是由数千个基因不同的个体相互作用组成的复杂系统的涌现特性。超有机体特征的进化和遗传学还没有得到很好的理解，部分原因是研究独居生物遗传学的典型工具不能直接适用于群居动物。凭借蜜蜂这一研究社会行为及其进化的模式生物的独特种群和功能基因组数据集，我将通过以下方式推进社会基因组学的知识：1)超有机体特征的进化和遗传学：我们将整合功能和定量基因组研究与种群基因组调查的积极和消极选择，以测试关于蜜蜂超有机体特征进化的明确假设。2)极端一妻多夫制的遗传和后果：极端一妻多夫制（多次交配）在许多群居昆虫中很常见，但这种遗传特征的遗传和适应性后果尚未得到很好的理解。我们将使用全基因组关联图谱来鉴定蜜蜂多夫制的潜在基因。我们还将直接验证群体内遗传多样性增强劳动分工和群体适应度的假设。3)极端重组的进化：先前的研究表明，群居昆虫的重组率往往比独居昆虫高得多。我们将通过对几组群居昆虫及其独居祖先的重组率进行系统发育独立比较来推进这一领域的知识，并询问是否像我们之前在蜜蜂中发现的那样，工蜂偏向基因倾向于存在于重组热点。最后，我们将从理论上评估社会性昆虫高重组率进化的不同模型。影响：我们的研究将为研究超级有机体的遗传和进化提供第一个综合努力，并将推进对真社会性昆虫的两个常见但鲜为人知的特征的认识：极端多夫制和重组。这将为理解生物学重大转变的最终原因和近因奠定基础。最后，这项研究将为多样化的受训者群体创造肥沃的土壤，使他们在掌握进化基因组学的前沿技术的同时做出重大研究贡献。

Evolution was punctuated by several major events that fundamentally increased the complexity and biodiversity of life. These evolutionary game-changers include the evolution of sex, multicellularity, and sociality. Sociality evolved multiple times in animals and involves division of labour between individuals that cooperate to benefit a group. In solitary species, genetic mutations can influence an individual's traits and these mutations can spread or decline as a function of the individual's fitness. Social animals, however, have collective `superorganismal' traits that are emergent properties of a complex system composed of thousands of genetically distinct individuals interacting together. The evolution and genetics of superorganismal traits are not well understood, in part because the typical tools for studying genetics in solitary organisms are not directly applicable to social animals. Armed with unique population and functional genomic datasets on the honey bee - a model organism for the study of social behaviour and its evolution - I will advance knowledge in sociogenomics by: 1) Evolution and genetics of superorganismal traits: We will integrate functional and quantitative genomic studies with population genomic surveys of positive and negative selection to test explicit hypotheses about the evolution of superorganismal traits in the honey bee. 2) Genetics and consequences of extreme polyandry: Extreme polyandry (multiple mating) is common in many social insects, but the genetics and fitness consequence of this heritable trait is not well understood. We will use genome wide association mapping to identify the genes underlying polyandry in honey bees. We will also directly test the hypothesis that within colony genetic diversity enhances division of labour and colony fitness. 3) The evolution of extreme recombination: A previous study suggested that rates of recombination in social insects tend to be much higher than in solitary insects. We will advance knowledge in this area by carrying out phylogenetically independent comparisons of recombination rates in several groups of social insects and their solitary ancestors, and ask if worker-biased genes tend to reside in recombination hotspots as we previously discovered in honey bees. Finally, we will theoretically evaluate different models for the evolution of hyper recombination rates in social insects. Impact: Our research will provide the first integrative effort to study the genetics and evolution of superorganisms and will also advance knowledge on two common but poorly understood features of eusocial insects: extreme polyandry and recombination. This will lay the foundation for understanding the ultimate and proximate causes of a major transition in biology. Finally, the research will create fertile grounds for a diverse group of trainees to make major research contributions while mastering cutting edge techniques in evolutionary genomics.