Stress, cooperation, and cheating during the evolution of multicellularity

多细胞生物进化了多次（例如，藻类、植物、动物、真菌），并为地球上生命的复杂性和多样性的增加奠定了基础。然而，这些主要的进化事件的一般原则和机制还没有得到很好的理解。从概念上讲，多细胞生物的进化被视为个体的一种转变，以前独立的单位被整合成一种新的个体。这种转变依赖于合作相互作用的建立，包括将生殖潜力限制在种系，而大多数细胞（索马）表现出利他行为。然而，作弊者（例如，癌细胞）可能出现并威胁多细胞个体的稳定性。 我的NSERC资助的研究计划的长期目标是了解压力在多细胞合作和复杂性进化中的作用。我们的模型系统一直是volvocine谱系-一组绿色藻类，包括单细胞（例如，莱茵衣藻）和具有不同复杂程度的多细胞物种，包括具有不育体细胞的物种（例如，团藻（Volvox carteri）。从概念上讲，我们认为生殖体分离的进化需要营养和生殖功能的表达从时间（如单细胞个体）到空间（即，在索马和胚芽之间）上下文。从机制上讲，我们认为索马的进化涉及单细胞祖先中由环境压力诱导的生活史基因的协同选择（以直接繁殖为代价来提高生存率），通过将它们的表达从环境背景转移到发育背景。本提案的短期目标是围绕理解压力在以下方面的作用：（i）简单多细胞性（协同合作）和索马（利他合作）的进化，以及（ii）通过对作弊施加强大的成本来稳定合作。为了实现我们的目标，我们将（i）进行全基因组表达分析，以确定与实验进化和应激诱导的多细胞C中环境诱导的应激反应和多细胞特征相关的共同途径。reinhardtii菌株，和V. carteri体细胞中;和（ii）评估多细胞/合作性状缺陷突变体对胁迫的敏感性。 总的来说，我们正在开发一个新的框架（概念和机制），重点是压力反应的共同选择。我们还制定和测试两个新的进化模型的形态创新和基因的进化co-option，涉及适应不良突变和环境信号的模拟在发展的背景下。将压力敏感性确定为作弊的一般成本也可能为我们理解和治疗癌症提供新的见解。

Multicellularity evolved multiple times (e.g., in algae, plants, animals, fungi) and set the stage for the increased complexity and diversity that characterizes life on Earth. Nevertheless, the general principles and mechanisms governing these major evolutionary events are not well understood. Conceptually, the evolution of multicellularity is seen as a transition in individuality, whereby previously independent units become integrated into a new type of individual. Such transitions are dependent on the establishment of cooperative interactions, including restricting the reproductive potential to the germline, while the majority of cells (the soma) express an altruistic behaviour. However, cheaters (e.g., cancer cells) can arise and threaten the stability of the multicellular individual. The long-term objective of my NSERC-funded research program is to understand the role of stress in the evolution of multicellular cooperation and complexity. Our model-system has been the volvocine lineage - a group of green algae that encompasses both unicellular (e.g., Chlamydomonas reinhardtii) and multicellular species with different levels of complexity, including species with sterile somatic cells (e.g., Volvox carteri). Conceptually, we argue that the evolution of germ-soma separation requires a change in the expression of vegetative and reproductive functions from a temporal (as in unicellular individuals) to a spatial (i.e., between soma and germ) context. Mechanistically, we suggest that the evolution of soma involved the co-option of life-history genes induced by environmental stress in unicellular ancestors (to enhance survival at an immediate cost to reproduction), through shifting their expression from an environmental context into a developmental context. The short-term objectives of this proposal are centered around understanding the role of stress in (i) the evolution of simple multicellularity (synergistic cooperation) and soma (altruistic cooperation), and (ii) stabilizing cooperation by imposing a strong cost on cheating. To achieve our goals, we will (i) perform genome-wide expression analyses to identify common pathways that are associated with environmentally-induced stress responses and multicellular traits in experimentally-evolved and stress-induced multicellular C. reinhardtii strains, and in V. carteri somatic cells; and (ii) assess the sensitivity to stress of mutants defective in multicellular/cooperative traits. Overall, we are developing a new framework (both conceptual and mechanistic) focused on the co-option of stress responses. We are also formulating and testing two new evolutionary models for the evolution of morphological innovations and gene co-option, involving maladaptive mutations and the simulation of environmental signals in a developmental context. Identifying stress sensitivity as a general cost of cheating might also provide new insight into our understanding and treatment of cancer.