The Sociogenomic Foundations of the Major Transition to Eusociality

Social behaviour is widespread in nature and lies at the core of the major transitions in evolution, where lower level biological units cooperate to form higher level entities of increased complexity. In some advanced insect societies, colonies function so cohesively that they are often described as superorganisms, with reproductive and nonreproductive castes playing roles analogous to the germ and soma in multicellular organisms. Yet major questions remain about how sociality first arose and how it diversified across evolutionary history. The main goal of SOCIAL LADDER is to identify the behavioural, physiological and molecular mechanisms that enabled the major evolutionary transition to sociality in insects. The project will address three critical stages in the evolution of social complexity. First, it will determine which preadaptations in solitary insects facilitated the emergence of helper behaviour and the early ontogeny of division of labour. Second, it will investigate reproductive plasticity and dominance behaviour in primitively eusocial species. Third, it will examine how behavioural specialisation between castes evolved in advanced eusocial species, a point of no return in the evolution of sociality. SOCIAL LADDER will take advantage of the latest advances in computational and genomic technologies to study the evolution of sociality in an entirely novel angle, using key social insect species with varying degrees of social organization with an unprecedented level of detail. By combining behavioural observation, experimental manipulation, and transcriptome research, SOCIAL LADDER will bridge major knowledge gaps in our understanding of the major evolutionary transition to sociality. Impacto científico técnico o internacional esperable: This project stands out for its high level of innovation, as it seamlessly integrates classical behavioral observations with cutting-edge experimentation. Employing state-of-the-art techniques such as next-gen RNA sequencing assays alongside controlled experimental manipulations, the project aims to rigorously test specific hypotheses concerning the origin and evolution of eusociality. By doing so, it promises to yield unprecedented evolutionary insights into the remarkable transition that is the evolution of eusociality. Notably, the genomes of several social insect species, crucial for this study due to their key phylogenetic placement and unique social organization, have only recently become available. Hence, this is the perfect timing to tackle these outstanding evolutionary questions. Studies on the origin of sociality have always caught a great deal of attention and have been featured in top scientific journals as well as major media outlets. More specifically, recent genomic advances have enabled the study of the evolution of social traits to an unprecedented level of detail. This project will be able to make a major contribution to our understanding of the evolution of sociality and other major transitions in evolution, and will lead to publications in top general biology journals as well as major evolutionary biology journals. Topics related to the evolution of sociality and/or the techniques explored in this proposal have always a strong appeal not only to scientists but also to media outlets, as well as to the broader public. I therefore expect that the results from this project will be highly cited and covered by media outlets and will have an impact beyond its primary field of evolutionary biology. The project aims to understand fundamental aspects of a major transition in evolution to sociality. Although not directly applicable to society, many of the findings related to the field of sociobiology initially derived from social insects of theoretical models were later found to be applicable to our societies as well. A main example is perhaps the field of evolutionary game theory which is now widely applied in the fields of Economics and Behavioural Psychology, for example. Some of the studied bee species are already stablished as commercially important pollinators such as the red mason bee Osmia bicornis and the buff- tailed bumblebee Bombus terrestris and others are currently being studied with the same purpose (i.e. M. quadrifasciata). Therefore, despite not being among the main objectives of the proposal, expanding our knowledge about their biology might aid in improving the rearing techniques and applicability of species as crop pollinators. The project includes a robust plan for scientific communication and outreach, aligned with the objectives of the Spanish State Plan for knowledge transfer and public engagement in science. The proposed activities will strengthen scientific culture and bring the results closer to society, increasing the overall impact of the project beyond the academic sphere.