Comparative analyses of co-evolving host-parasite associations reveal unique gene expression patterns underlying slavemaker raiding and host defensive phenotypes

Abstract

The transition to parasitism is a drastic shift in lifestyle, involving rapid changes in gene structure, function, and expression. After the establishment of antagonistic relationships, parasites and hosts co-evolve through reciprocal adaptations, often resulting in evolutionary arms-races. Repeated evolution of social parasitism and slavery among Temnothorax ants allows us to examine those gene expression patterns that characterize slavemaker raiding and reciprocal host defensive phenotypes. Previous behavioural studies have established that raiding strategies between Temnothorax slavemakers diverge, while host defense portfolios shift similarly under parasite pressure. We are the first to confirm this at the molecular level, revealing that slavemaking species exhibit a wider variety of genes with species-specific patterns of expression within their raiding phenotypes, whereas expression similarity is commonly found during the non-raiding phenotype. Host species response to slavemaker aggression, however, is indicated by strong changes in the expression of a relatively few number genes. Additionally, the expression of individual genes such as Acyl-CoA-Delta(11) desaturase and Trypsin-7 is strongly associated with the raiding phenotype of all three slavemaking species. Here, we provide novel insight into the gene expression patterns associated with raiding and nest defense behavior in Temnothorax ants, suggesting lineage-specific evolutionary patterns among both slavemakers and hosts.