Comparative evolutionary genomics of slave-making ants and their hosts

• Applicants: Professor Dr. Erich Bornberg-Bauer; Dr. Barbara Feldmeyer; Professorin Dr. Susanne Foitzik; Professor Dr. Jürgen Heinze
• Subject Area: Evolution, Anthropology ; General Genetics and Functional Genome Biology ; Bioinformatics and Theoretical Biology ; Sensory and Behavioural Biology
• Term: since 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 528337128

This project aims to unravel the genomic basis underlying the remarkable, repeated transitions to slave-making in ants. The slave-makers and their hosts are in a constant arms race evolving counter acting attack and defense strategies respectably. The parasites and their hosts have diverged from common ancestors recently. Therefore, this system provides a unique opportunity to elucidate the evolutionary forces underlying convergent evolution, and thus to understand the interplay between random mutations and adaptation. During the first phase we have sequenced and assembled genomes and transcriptomes of multiple host-parasite pairs and compared them with other available ant genomes. We found that parasites, in contrast to hosts, have lost numerous odorant receptors (OR) and underwent and regulatory changes which mainly affected later developmental stages suggesting the influence of epigenetic regulation. Building on these results and accrued resources we will now study further gene family reductions and expansions, as well as changes in genomic features, and verify some of these experimentally. First, in addition to the now denser phylogenetic sampling, we will analyse one additional genome from a ”degenerate slave-maker”, which produces very few workers and which we hypothesise has lost even more receptors than the so far investigated slave-makers. Second, assuming lost receptors were less essential for parasites because they were related to social behaviour, we will use phylostratigraphy to study their evolutionary origin and conduct odour perception screens using antennal electrophysiology to determine whether indeed parasites perceive fewer odours than hosts. We corroborate this by antennal transcriptomes to investigate whether fewer OR genes are expressed and investigate whether the reduction of OR genes in slave-makers is linked to a smaller number of glomeruli in the antennal lobes. Third, we will use genome scans to examine whether other gene families are expanding or contracting and whether they are subject to positive or relaxed selection in either hosts or slave-makers. We will furthermore elucidate the role of transposable elements in this process. Experimentally, we will study the function of parasite specific genes using RNAi, corroborated by behavioural screens. Moreover, we will analyse co-expression networks expecting that genes convergently lost in slave-makers are highly connected in hosts, suggesting that their loss releases adaptive ratchets. Comparing network topologies in parasites during raids with those from foraging hosts shall clarify whether the former derived from the latter, more ancestral behavior. With this project, we will thus contribute to the understanding of convergent evolution and its genomic basis.

• DFG Programme: Research Grants