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

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.

Who will benefit from this research?
This Project will generate important insights into the molecular basis of behaviour, with specific reference to group living in animal societies. The outcomes are therefore of a fundamental, 'blue-skies' nature, generating basic information on the building blocks of the natural world, using a charismatic and ecologically important group of organisms. Apart from academic beneficiaries, the main beneficiaries will be the general public, and specifically those in the UK and US. Public understanding of science is essential for the future of our societies and economies.
How will they benefit from this research?
1) Through an understanding the science behind their own social behaviour
People are intrinsically interested in their own actions and behaviors. Social insect societies have many parallels with our own, and social insect research provides a tractable dialogue with the public and the theory and mechanisms of social behaviour. For example, social insects resolve conflicts with neighbours and use division of labour to enhance social group performance and cohesion. Human societies are driven by division of labour, in both our work places and homes. The analogies with human societies are particularly compelling for the simple societies of bees and wasps, where individuals have choices on what roles they play. Individuals can be uniquely marked and their behaviours followed: this evokes a special curiosity in the public as the behaviours of individuals can be viewed through the eyes of a 'soap-opera', where individuals can be observed acting in their own interests (selfishness) or go out of their way to help others (altruism).
2) Through an understanding how their behaviours are products of their genomes.
The general public broadly understands genetic inheritance (e.g. in disease etc.), but the interaction between genes and the environment, and how a genomes' responsiveness determines adaptation and plasticity at the whole organism level, remains less well appreciated by the public. An education of how behavior is not 'hardwired' and that the environment can affect how your genes behave has important health and societal consequences for the general public.
3) By learning about the diversity of social insects and how they came to be
The public are exposed regularly to stories about beneficial bees, invading ants and killer wasps in the media these days. This results in most social insects (with the exception of bees) being viewed as pests, unimportant and undesirable. Yet, wasps and ants (as well as bees) are vital components of global ecosystems as pest controllers, pollinators, seed dispersers and decomposers. The public will benefit from a more balanced education of the diversity of social insects that can be found, how this diversity evolves and the importance to our planet.
4) Through an understanding of the importance inter-disciplinary collaborations in modern-day science
The general public have a pre-conceived idea of what a modern scientist does, specifically that scientists are insular creatures who live in labs with expensive equipment, and that their science is somewhat detached from the real world. The public would benefit from the chance to understand how modern science is highly inter-disciplinary, and that science progresses best when scientists from different skill sets interact and share ideas. Our Collaborative Project will benefit the public as it is an explicit example of how 'welly boot' science can be married with computational science and molecular biology to advance our understanding of the natural world.