Cataglyphis desert ants use distinct behavioral and physiological adaptations to cope with extreme thermal conditions

Abstract

Some ant species live in hot and arid environments, such as deserts and savannas. Worker polymorphism-variation in worker size and/or morphology within colonies-is adaptive in such ecosystems because it enhances resistance to heat stress and increases the efficiency of resource exploitation. However, species with small, monomorphic workers are also frequently found in these environments. How species with distinct worker size and degrees of polymorphism deal with such stressful environments remains poorly studied. We investigated the behavioral, physiological, and molecular adaptations that may enhance heat and desiccation tolerance in two sympatric species of Cataglyphis desert ants that differ dramatically in worker size and polymorphism: C. viatica is polymorphic, while C. cubica is small and monomorphic. We found that worker size, water content, water loss, and protein regulation play a key role in thermal resistance. (i) Large C. viatica workers better tolerated heat and desiccation stress than did small C. viatica or C. cubica workers. The former had greater water content and lost proportionally less water to evaporation under thermal stress. (ii) Despite their similar size distribution, workers of C. cubica are more heat tolerant than small C. viatica. This higher degree of tolerance likely stemmed from C. cubica workers having greater relative water content. (iii) Under thermal stress, small C. viatica workers metabolized larger quantities of fat and differentially expressed proteins involved in cellular homeostasis. In contrast, C. cubica downregulated the expression of numerous proteins involved in mitochondrial respiration likely reducing ROS accumulation. (iv) Consistent with these results, large C. viatica workers remained active throughout the day; C. cubica workers displayed a bimodal activity pattern, and small C. viatica remained poorly active outside the nest. Our study shows that ecologically similar ant species with different degrees of worker size polymorphism evolved distinct strategies for coping with extreme heat conditions.

Keywords: Ants; Desiccation; Heat shock response; Polymorphism; Proteome; Thermal tolerance.