Evolutionary genomics of royalty in messor hybridogenetic ants – RoyalMess

Royalty in social insects is typically environmentally acquired rather than genetically determined. However, this is not the case in an exceptional reproductive system, known as social hybridogenesis. Here, two distinct royal lineages of ants can only produce queens by their own while they need to hybridize to produce workers. Eggs with a pure royal genome are thus genetically fated to become queens while hybrid genomes are fated to become workers. Convergent evolution toward such a baroque reproductive strategy appears common in harvester ant species (four times in Pogonomyrmex and Messor genera), but its origin is still completely mysterious. In this project, I plan to unravel the evolution of this unique system via cutting-edge genomic and molecular approaches.

1. Prevalence of social hybridogenesis: I will use genome-wide sequence data to identify novel occurrences of social hybridogenesis across ~500 ant species, in search for potential ecological determinants (e.g. climate or diet) that could favour evolution towards genetic caste determination.

2. History of royal lineages: I will use population genomics in three pairs of Messor royal lineages to trace back their evolutionary origin. For this, I will develop a novel ABC method to map introgressions and selective sweeps along royal lineage genomes to detect past hybridization events or fixation of potentially selfish caste-biasing alleles.

3. Identifying caste-determining genes: I will use comparative transcriptomics in early ant embryos to identify genes differentially expressed between castes before developmental divergence. Candidate genes will be experimentally validated via i) controlled matings between pure-lineage queens and lab-produced recombinant males and ii) genome editing via the CRISPR-Cas9 technology.

If successful, this project will enable the first genetic manipulation of ant royalty, deciphering how such an iconic example of phenotypic plasticity can become genetically hardwired.