Genomic Signatures of Selection Across Climate Gradients and a Geographic Mosaic of Coevolution in an Ant Social Parasite–Host System

Coevolutionary dynamics in host-parasite systems are shaped by reciprocal selection and environmental context. When hosts and parasites share ancestry and ecological overlap, selection can act on similar traits, but population structure and geography may generate adaptive mosaics. Here, we present the first study to investigate genome-wide signatures of selection in response to a broad climatic gradient and a geographic mosaic of coevolution between a social parasite and its host. We examined these processes in the dulotic ant Temnothorax americanus and its congeneric host Temnothorax longispinosus using population genomics, genome-wide association analyses, and transcriptomics. Host populations showed very weak and parasites stronger population structure, enabling geographic mosaic dynamics. Genomic responses to parasite prevalence were divergent: Hosts showed signatures of selection on immune genes, whereas regulatory genes associated with raiding were under selection in parasites. Both species displayed convergent signatures of climate adaptation, including loci related to desiccation resistance, stress response, and parasite prevalence, with signals in communication and recognition genes involved in hydrocarbon biosynthesis, chemosensory perception, circadian rhythms, and venom production. Transcriptome analyses revealed contrasting patterns, with host gene expression linked to parasite prevalence and parasite expression more strongly shaped by climate. Together, our results reveal a genomic mosaic of coadaptation, in which population structure, asymmetric selection, and ecological variation interact to generate divergent yet interconnected evolutionary trajectories. Our findings highlight communication and recognition as recurrent arenas of antagonistic coevolution, underscore climate as a pervasive selective force, and establish a framework for investigating molecular coevolution in social parasite systems.