NSFDEB-NERC The evolutionary genomics of a major transition in evolution

点击翻译按钮获取中文摘要

Over 20 years ago, eight major transitions in evolution that explain the emergence of biological complexity were defined, one of which is the evolution of sociality (or superorganismality). Significant advances have been made in understanding the theory underpinning major evolutionary transitions; however, we lack an integrated understanding of the evolutionary patterns and processes of the major transitions. A novel and timely question is whether major transitions arise via gradual or punctuated evolutionary processes. Distinguishing between these is fundamental to our understanding of biological complexity, the natural world and our own origins. We address this question by formulating new a predictive framework on the molecular processes underpinning major transitions, and testing these predictions empirically using multi-level genomic analyses of sociality in 16 species of bees and wasps.Recent theory on major transitions has extended the concept of the society across levels of biological organization. E.g. genes form a society in protocells, protist cells form a multicellular society, and insects become eusocial superorganisms. A common trait for all societies is the emergence of irreversibly committed phenotypes within the group (e.g. queens and workers in insect colonies; tissue types in multicellular organisms). These analogies are compelling but remain largely conceptual because we do not understand the evolutionary processes by which major transitions (and specifically irreversibility) arise. This is important because the nature of the evolutionary processes shapes the assumptions on which our theoretical understanding is based. Our overarching goal, therefore, is to determine whether the major transition to superorganismality evolved via gradual or punctuated processes, using social insects (the best studied of the major transitions) as a model system. Until very recently, all studies in social insects assumed that superorganisms evolved via the gradual accumulation of many small changes in molecular processes. However, new conceptual work suggests that the major transition may occur via a less gradual process. This idea proposes that, although many insect species display the hallmarks of 'classic' eusociality, they do not express the specific set of traits that indicate a major transition (i.e. mutual dependency; committed (irreversible) castes). Implicit in this is the assumption that the transition requires a step change in phenotypic traits. A recent empirical analysis of the evolution of sociality in wasps implies a similar pattern, with caste commitment appearing suddenly in (and at the origin of) sociality in wasps. These recent studies raise the intriguing question of whether the major transition to superorganismality is an example of punctuated evolution and not a trait that emerges gradually from many, small micro-evolutionary processes. In this Proposal we introduce a new framework for dissecting the evolutionary processes of a major evolutionary transition: we identify putative molecular signatures that are likely to typify a gradual or punctuated route to superorganismality. We propose to test these predictions. First, we will generate appropriate multi-layered genomic datasets for 16 species of bees and wasps that span the transition from solitary individuals to superorganisms: these include new genomes, chromosome mapping, new transcriptomes and proteomes. We will then use these datasets to find out which of the evolutionary routes (gradual or punctuated) best explain the transition to superorganismality. Finally, we will bring together experts who share an interest in major transitions across the spectrum of biological organization to discuss the extent to which there are general molecular signatures on the mechanistic basis of a major transition in evolution. If punctuated evolutionary processes are important in driving major transitions, new types of theoretical models will be required.