Endogenous colony dormancy shapes seasonal cold tolerance in temperate ants

Abstract As eusocial superorganisms, cold‐adapted ants must survive multiple consecutive winters and are shaped by selective pressures acting at both individual and colony‐level. Following winter reactivation, colonies enter a fixed developmental phase whose duration is regulated by ‘Kipyatkov's sand‐glass device’, an endogenous timer that enforces the onset of a new dormancy period after a set interval even under permissive light and temperature conditions. However, how this obligate colony‐level programming interacts with worker physiological responses to produce cold‐tolerant phenotypes capable of withstanding seasonality remains unknown. Here, we leveraged obligate colony‐level seasonal programming in five temperate ant species to disentangle the relative contributions of endogenous colony dormancy and exogenous thermal exposure (acclimation) on worker metabolic rates, metabolomic profiles and cold tolerance. We show that across the tested species, the onset of colony dormancy alone is sufficient to modulate both the critical thermal minimum (CT min ) and the temperature causing 50% mortality during acute cold exposure (LTe 50 ) and further interacts with acclimation to shape worker cold tolerance. Cold acclimation triggered the accumulation of metabolites (e.g. trehalose, glycerophosphoethanolamine) potentially involved in osmotic balance and membrane reorganization in individuals. Our results highlight that programmed, obligate colony dormancy in temperate ants can drive cold hardening in workers independently of environmental exposure. This suggests that cold tolerance in temperate social insects can emerge from the interplay between colonial seasonal programming and individual responses to environmental cues, reflecting their unique evolutionary history and social organization. Read the free Plain Language Summary for this article on the Journal blog.