Thrifty superorganism phenotypes emerge as a plastic response to extreme environments in the Hercules ant

High-altitude human populations are a classic example of adaptation to extremely stressful environments through thrifty phenotypes, where individuals adapt plastically by reducing specific organ size, like limbs, while maintaining overall size. However, it remains unknown, whether other organisms exhibit thrifty phenotypes, and which external factors may shape them. Here, we address these questions in ant colonies, considered superorganisms. The thrifty phenotype hypothesis applied to eusocial organisms predicts that colonies experiencing food shortage should reduce investment in costly individuals. In polymorphic colonies, the largest workers known as “majors” are costly to produce and should therefore be less abundant in colonies experiencing food shortage. Alternatively, the starvation resistance hypothesis posits that colonies in stressful environments should maintain larger colonies, which provide a nutritional buffer in times of food shortage. We show that the proportion of majors in colonies of the Hercules ant, Camponotus herculeanus , decreases plastically with increasing latitude across the temperate and boreal forest biomes of eastern Canada, independently of their average body size, or colony size, resulting in a thrifty superorganism phenotype. Furthermore, we find that the low number of days, annually, when workers can nurse the brood, best predicts these phenotypes. Our study reinforces claims that eusocial organisms may adapt plastically to fluctuating environments, and that extreme environments favour thrifty phenotypes in both humans and ants.