Comparative analysis of co-evolving host-parasite associations reveal unique expression patterns and pathways underlying slavemaker raiding and host defensive behavior in ants

The transition to parasitism is a drastic shift in lifestyle, involving rapid changes in gene structure, function, and expression. Evolutionarily 'young' parasites are ideal models for the elucidation of the early steps of this transition. After the establishment of an antagonistic relationship, parasite and host co-evolve through reciprocal adaptations resulting in an evolutionary arms-race. Repeated evolution of social parasitism and slavery among Temnothorax ants allows us to examine gene expression patterns characterizing slavemaker raiding and reciprocal host defensive behavior. Previous studies of Temnothorax provide evidence for co-evolving adaptations between parasites and hosts, as well as diverging raiding strategies between slavemakers. However, under parasite pressure, host defense portfolios shift similarly, suggesting diverging evolution of defensive traits. Through comparative gene expression analyses, we find that slavemaker raiding behavior is characterized by a down-regulation of numerous genes relative to their non-raiding state. Moreover, only a small number of genes shared expression between slavemaking species. In contrast, hosts possess a higher ratio of commonly-to-privately over-expressed genes and metabolic pathways during raids, suggesting that genes of similar function control defensive behavior. Additionally, a number of candidate genes were identified, each potentially playing a major role in shaping slavemaker- and host-specific behaviors. Finally, in two slavemaking species, functional enrichment analyses indicate that genes over-expressed during raiding behavior are associated with ribosomal structure, oxidation-reduction, and metabolic processes. Overall, our analysis revealed evidence for divergent evolution among closely-related ant species, where species-specific gene expression characterize raiding and defensive behavior. Overall design: Gene expression analysis using RNA-Seq data. Six species examined, two behaviors per species, and four replicates per behavior. Please note that 2017July_TemnoClusters.fas-gb.tar.gz includes 5,197 OrthoMCL homologous cluster files (.fas-gb) containing all previously-identified contigs that are present within all six Temnothorax species.