The genetic basis and ground plan of eusocial worker evolution

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The major transitions are foundational to the evolution of individuality and the hierarchical structure of all life on Earth. In these events, previously independent individuals come together to form a new, higher-level cooperative group resembling an individual in its own right. Classic examples are the evolution of multicellularity and eusociality. Eusocial societies are those in which some members (workers) act altruistically towards their fellow members, as in the ants, bees and wasps. Evolutionary biology has successfully explained the ultimate reasons for transitions like the evolution of multicellularity and eusociality in terms of kin selection. But the actual genes involved in these major transitions remain very poorly known. Just as researchers need to know what genes lead a cell to become a somatic (altruistic) or germline (reproductive) cell, so do we need to know what genes lead workers in eusocial societies to be non-reproductive (altruistic) workers or reproductive workers. This project aims to fill this key gap by using new technologies to determine the genetic basis of worker altruism versus worker reproduction in a eusocial insect. The study system will be the bumble bee, Bombus terrestris, whose workers can either be non-reproductive sterile altruists (with inactive ovaries) or reproductive egg-layers. Bumble bees are the living group most closely resembling the primitively eusocial common ancestor of the two independently-evolved advanced eusocial bee taxa, the honey bees and stingless bees. Gene expression in reproductive and non-reproductive workers has previously been profiled in honey bees, but only studies in primitively eusocial insects can provide an evolutionary perspective on the critical gene expression differences. Hence primitive eusociality in B. terrestris, and the position of B. terrestris in the bee phylogeny, make it an excellent study system for the proposed work.Using B. terrestris, the research will (1a) determine the gene expression differences within selected tissues (brain, fat body and ovary) that underpin the differences between reproductive and non-reproductive workers, (1b) validate the most salient of these differences using independent gene expression assays, (1c) determine how key genes change expression over time as the worker reproductive phenotype arises (so separating out upstream- and downstream-acting genes in the regulatory pathways), (2) establish how reversals in workers' reproductive phenotype are tracked by gene expression changes, and (3) test a highly influential hypothesis for the evolution of the worker reproductive phenotype. This hypothesis, the reproductive ground plan hypothesis, proposes that division of labour (e.g. changes in task with age) in workers is regulated by genetic pathways co-opted from pathways regulating reproduction in females of workers' non-social ancestors (the 'ground plan'). It is important because it represents a key example of the general idea that evolutionary novelties like worker altruism can arise through the co-option of existing gene pathways.Methods will consist of laboratory and field experiments, next-generation sequencing (RNA-Seq transcriptomics), quantitative PCR (qRT-PCR) and bioinformatics. The research is fundamental because it deals with phenomena of basic importance and broad interest in evolutionary ecology, genetics and transcriptomics. It is novel because, although a growing number of studies are elucidating molecular aspects of social evolution, an evolutionary perspective on the genetic basis of workers' loss of reproductive ability is lacking, the relationship between flexibility in the workers' reproductive phenotype and gene expression is not understood and the important reproductive ground plan hypothesis requires testing. The work will therefore substantially advance our deep understanding of the genetic foundations of eusociality and the major transitions.