Stress, cooperation, and cheating during the evolution of multicellularity

点击翻译按钮获取中文摘要

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.