Stress, cooperation, and cheating during the evolution of multicellularity

多细胞生物进化了多次（例如，在藻类、植物、动物、真菌中），并为地球上生命特征的复杂性和多样性的增加奠定了基础。然而，控制这些主要进化事件的一般原理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看作是个体的转变，以前独立的单位变成了一种新的个体。这种转变依赖于合作相互作用的建立，包括将生殖潜能限制在生殖系，而大多数细胞（体细胞）则表现出利他行为。然而，骗子（如癌细胞）可能出现并威胁到多细胞个体的稳定性。我的nserc资助的研究项目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。我们的模型系统是volvocine谱系——一组绿藻，包括单细胞（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（如Volvox carteri）。从概念上讲，我们认为胚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（即在体细胞和胚芽之间）的变化。从机制上讲，我们认为体细胞的进化涉及单细胞祖先的环境胁迫诱导的生活史基因的共同选择（以直接牺牲繁殖为代价来提高生存），通过将它们的表达从环境背景转移到发育背景。这个建议的短期目标集中在理解压力在(i)简单多细胞（协同合作）和躯体（利他合作）的进化中的作用，以及（ii）通过施加欺骗的强大成本来稳定合作。为了实现我们的目标，我们将(i)进行全基因组表达分析，以确定在实验进化和应激诱导的多细胞莱茵哈特氏梭菌菌株和V. carteri体细胞中与环境诱导的应激反应和多细胞性状相关的共同途径；（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（包括概念和机制），专注于压力反应的共同选择。我们还制定和测试了两种新的进化模型，用于形态创新和基因协同选择的进化，包括不适应突变和发育背景下环境信号的模拟。将压力敏感性作为作弊的一般代价，也可能为我们对癌症的理解和治疗提供新的见解。

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.