Climate and parasite pressure jointly shape traits mediating the coevolution between an ant social parasite and its host

Abstract

Host–parasite relationships are often shaped by coevolutionary arms races. While abiotic influences on these dynamics are well documented, a combined analysis of abiotic and biotic factors is essential for understanding coevolution, particularly under climate change. In this study, we analysed the interactions of the obligate social parasite Temnothorax americanus, a dulotic ant, and its primary host, the ant T. longispinosus, focusing on behavioural and cuticular hydrocarbon (CHC) traits that govern parasite invasion and host defence. We studied the link between these traits and local climate as well as parasite prevalence. Our results revealed that behavioural interactions were more strongly associated with climate than parasite prevalence. Hosts from warmer, drier regions exhibited reduced aggression during parasite encounters, opting to pick up the brood and flee, while parasites from these regions exhibited greater aggression and activity. CHCs mediating enemy recognition in these ants were linked to local climate and parasite prevalence in both species. As all colonies were maintained under standardized conditions for a year, we attribute the observed phenotypic traits to evolutionary adaptation rather than phenotypic plasticity. Our findings suggest that both abiotic and biotic factors play critical roles in shaping co-evolving traits, sometimes leading to unexpected patterns that would potentially be overlooked when considering only a single factor. These insights provide a framework for understanding how climate influences coevolution of interacting species.