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

A bstract Adaptation to extreme environments is commonly assumed to occur through microevolutionary change. However, studies of high-altitude human populations show that organisms can also respond to nutritional stress through developmental plasticity, producing thrifty phenotypes that prioritize essential function over costly structures. Whether this adaptive strategy extends beyond humans, and how it operates in natural systems, remains largely unexplored. Here, we test the thrifty phenotype hypothesis (TPH) in a widely distributed superorganism, the carpenter ant Camponotus herculeanus , which inhabits some of the most environmentally challenging regions of the Northern Hemisphere. Colonies comprise inexpensive minor workers and energetically costly major workers, providing a powerful system for examining plastic investment under resource limitation. We quantified relationships between caste structure and climate and conducted a common-garden experiment to test the TPH. We show that the proportion of major workers declines with increasing latitude, independently of body size and colony size, and is best predicted by the number of days, annually, during which workers can nurse brood. Experimental results further demonstrate that colonies rapidly and plastically adjust caste structure in response to environmental conditions. Our findings reveal that thrifty phenotypes can emerge in superorganisms and could represent a conserved developmental response to environmental stress. By extending a central hypothesis from human biology to social insects, this work provides a unifying framework for understanding how developmental plasticity shapes adaptation across levels of biological organization.