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Bitao Qiu:
The genetic regulatory network mediating caste differentiation in ants: a transcriptomic view

Date: 31-08-2019    Supervisor: Guojie Zhang & Jacobus Jan Boomsma

An ant colony can be conceptualized as a higher-level organism with permanent reproductive division of labour between inseminated queen (germ) and worker (soma) individuals, analogous to the germ-cells and somatic cells in a multicellular organism. In this context, the ant colony has been recognized as a superorganism, a social system regulated and maintained by epigenetic processes involving genetic regulatory networks (GRNs) to produce different individual phenotypes from the same genomic blueprint. While the systematic study of GRNs for metazoan cell differentiations has become well established, the GRNs mediating evolutionary origins and later developmental changes in caste differentiation are still very fragmentary known.

This PhD thesis is an attempt to systematically explore the roles of GRNs in ant caste differentiation. In the first chapter, we compared brain transcriptomes across five typical ant species and identified the GRN underlying the homologous gyne (virgin queen) and worker caste phenotypes. This study also showed that maturation processes that produce reproductive workers in evolutionarily derived queenless ants do not share the GRN for caste differentiation in typical ant species. The genes regulating caste differentiation in ants and honeybees only partly overlap, consistent with these clades having evolved superorganismality independently.

In the second chapter, we investigated the neuroanatomical and transcriptomic dynamics underlying the reproductive transition from virgin gyne to inseminated queen in the ant Monomorium pharaonis. We found that the GRN mediating this transition is different from the GRN for caste differentiation and that it appears to have been co-opted to replace the queenworker caste GRN in distantly related queenless ants, where reproductive workers fulfil queen roles.

In the third chapter, we profiled the developmental trajectories in M. pharaonis by producing transcriptomes for over 560 individuals covering all major developmental stages of both gynes and workers (from embryos within eggs to adults). We found that caste differentiation is being canalized similar to cell differentiation in metazoan embryogenesis. We developed a new computational method that can predict caste identity in early developmental stages where caste phenotypes are not yet morphologically distinct. We identified a substantial fraction of the coreset of genes that show consistent caste-biased expression across all developmental stages and conclude that these genes are components of a core GRN to maintain caste phenotypes after caste fate has been determined early in development. The discussion sections on the three chapters evaluated how these findings match early thinking of ant colonies as ‘superorganisms’ from transcriptomic characteristics.