Co-option of sex determination and differentiation pathways in caste differentiation in ants

• Applicant: Dr. Eva Schultner
• Subject Area: Evolution, Anthropology
• Term: since 2025
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 570448082

Major evolutionary transitions are key events in evolutionary history leading to an increase in the complexity of life. All major transitions - from the formation of genomes from single replicators to the evolution of superorganismal insects - can be explained by a single evolutionary mechanism, kin selection. The proximate, molecular mechanisms underlying each individual transition, however, are much less clear. Following the major transition to sexual reproduction, sex determination and differentiation pathways evolved which encode sex-specific phenotypes from the same genome; the same mechanisms have been shown to modulate alternative phenotypes within sexes in some species. We hypothesize that due to their prominent role in the regulation of phenotypic variation, sex differentiation mechanisms have been co-opted in the major transition to superorganismality in ants, explaining the modular development of fertile queens and non-reproductive workers. Support for this idea comes from our model species Cardiocondyla obscurior, as well as from other social Hymenoptera. In C. obscurior embryos with known sex and caste, many microRNAs and mRNAs with sex-biased expression are expressed in a caste-biased manner, similar to previous findings showing caste-specific differential splicing of genes expressed in a sex-biased manner in final stage larvae. Using a comparative approach, we aim to investigate the evolution of co-option of sex differentiation mechanisms in caste differentiation in three ant species with obligately sterile workers, Cardiocondyla obscurior, Solenopsis invicta and Pheidole pallidula. These three species belong to the largest ant subfamily, the Myrmicinae, and each represents one of the three most diverse taxa within the subfamily (Crematogastrini, Solenopsidini, Attini), thus covering substantial phylogenetic breadth. This will be complemented with a functional, experimental approach using RNAi knockdowns of doublesex in the lab model C. obscurior. Our project will assess the molecular mechanisms underlying sex and caste differentiation across the entire course of ant development, thus providing the opportunity to study conserved regulatory mechanisms acting in both processes, and their evolution. The proposed work aligns perfectly with the aims of the SPP GEvolve because it will contribute knowledge about highly-conserved features of insect genomes – sex differentiation pathways - and their role in the regulation of a major evolutionary innovation, caste polyphenism in ants. Our project incorporates a low risk, comparative transcriptomics and genomics component and a higher risk, functional experimental component, both of which promise high reward in the form of contributing basic knowledge about the mechanistic links between two major evolutionary transitions.

• DFG Programme: Priority Programmes
• Subproject of: SPP 2349: Genomic Basis of Evolutionary Innovations (GEvol)
• International Connection: United Kingdom
• Cooperation Partner: Dr. Mark C. Harrison