Does social thermal regulation constrain individual thermal tolerance in an ant species?

In ants, social thermal regulation is the collective maintenance of a nest temperature that is optimal for individual colony members. In the thermophilic ant Aphaenogaster iberica, two key behaviours regulate nest temperature: seasonal nest relocation and variable nest depth. Outside the nest, foragers must adapt their activity to avoid temperatures that exceed their thermal limits. It has been suggested that social thermal regulation constrains physiological and morphological thermal adaptations at the individual level. We tested this hypothesis by examining the foraging rhythms of six populations of A. iberica, which were found at different elevations (from 100 to 2,000 m) in the Sierra Nevada mountain range of southern Spain. We tested the thermal resistance of individuals from these populations under controlled conditions. Janzen's climatic variability hypothesis (CVH) states that greater climatic variability should select for organisms with broader temperature tolerances. We found that the A. iberica population at 1,300 m experienced the most extreme temperatures and that ants from this population had the highest heat tolerance (LT50 = 57.55°C). These results support CVH's validity at microclimatic scales, such as the one represented by the elevational gradient in this study. Aphaenogaster iberica maintains colony food intake levels across different elevations and mean daily temperatures by shifting its rhythm of activity. This efficient colony-level thermal regulation and the significant differences in individual heat tolerance that we observed among the populations suggest that behaviourally controlled thermal regulation does not constrain individual physiological adaptations for coping with extreme temperatures.

En hormigas, la termorregulación social es el mantenimiento colectivo de la temperatura del nido óptima para los individuos de la colonia. En la hormiga termófila Aphaenogaster iberica, hay dos comportamientos clave que regulan la temperatura del nido: la reubicación estacional y la profundidad variable del nido. Fuera del nido, las obreras recolectoras deben adaptar su actividad para evitar las temperaturas que excedan sus límites térmicos. Se ha sugerido que la termorregulación social limita las adaptaciones térmicas a nivel individual, fisiológicas y morfológicas. Examinamos esta hipótesis, estudiando los ritmos de actividad de recolección de alimento en seis poblaciones de A. iberica, a distinta altitud, desde 100 m a 2,000 m, en las montañas de Sierra Nevada, en el sur de España. Y analizamos la resistencia térmica de los individuos de estas poblaciones, en condiciones controladas. La Hipótesis de la Variabilidad Climática de Janzen (CVH) postula que una mayor variabilidad climática selecciona organismos con tolerancias térmicas más amplias. Encontramos que la población de 1,300 m era la que presentaba la mayor variabilidad climática, y que las hormigas de esta población tiene la mayor resistencia térmica individual (LT50 = 57.55°C), lo que confirma la validez de la CVH a una escala microclimática en el gradiente altitudinal estudiado. Encontramos que A. iberica puede compensar por la disminución de la temperatura media que acompaña al incremento en elevación. Las hormigas pueden cambiar sus ritmos de actividad sin afectar la entrada de alimento en la colonia, que tampoco se ve afectada por la elevación o la temperatura media diaria. A pesar de esta eficiente termorregulación a nivel de colonia, las diferencias estadísticamente significativas entre poblaciones observadas en la tolerancia térmica individual sugieren que la termorregulación controlada comportalmente no limita las adaptaciones fisiológicas individuales para enfrentarse a temperaturas extremas.

Evidence for locally adaptive metabolic rates among ant populations along an elevational gradient.

As global temperatures rise, the mechanistic links between temperature, physiology and behaviour will increasingly define predictions of ecological change. However, for many taxa, we currently lack consensus about how thermal performance traits vary within and across populations, and whether and how locally adaptive trait plasticity can buffer warming effects. The metabolic cold adaptation hypothesis posits that cold environments (e.g. high elevations and latitudes) select for high metabolic rates (MR), even after controlling for body size differences, and that this enables high activity levels when an organism is near its cold lower thermal limits. Steep MR reaction norms are further predicted at cold temperatures to enable rapid behavioural activation with rising temperatures needed to exploit brief thermal windows suitable for performing eco-evolutionary tasks. We tested these predictions by performing common garden experiments comparing thermal reaction norms of MR (from 15 to 32°C) and behaviour (from 10 to 40°C) across populations of the ant Aphaenogaster iberica sampled from a 2 km elevation gradient in the Sierra Nevada Mountains of southern Spain. As predicted, high-elevation ants had higher MR and steeper MR-temperature reaction norms. However, higher rates of energy use did not yield the predicted benefits of steeper activity-level reaction norms. The evidence for locally adaptive metabolic physiology only became apparent at intermediate temperatures, highlighting the importance of testing thermal performance hypotheses across thermal gradients, rather than focusing only on performance at thermal limits (i.e. critical thermal values). The partial support for the metabolic cold adaptation hypothesis highlights that while organisms likely show a wealth of unexplored metabolic temperature plasticity, the physiological mechanisms and eco-evolutionary trade-offs underlying such local adaptation remain obscure.

Is phenotypic plasticity a key mechanism for responding to thermal stress in ants?

Unlike natural selection, phenotypic plasticity allows organisms to respond quickly to changing environmental conditions. However, plasticity may not always be adaptive. In insects, body size and other morphological measurements have been shown to decrease as temperature increases. This relationship may lead to a physiological conflict in ants, where larger body size and longer legs often confer better thermal resistance. Here, we tested the effect of developmental temperature (20, 24, 28 or 32 °C) on adult thermal resistance in the thermophilic ant species Aphaenogaster senilis. We found that no larval development occurred at 20 °C. However, at higher temperatures, developmental speed increased as expected and smaller adults were produced. In thermal resistance tests, we found that ants reared at 28 and 32 °C had half-lethal temperatures that were 2 °C higher than those of ants reared at 24 °C. Thus, although ants reared at higher temperatures were smaller in size, they were nonetheless more thermoresistant. These results show that A. senilis can exploit phenotypic plasticity to quickly adjust its thermal resistance to local conditions and that this process is independent of morphological adaptations. This mechanism may be particularly relevant given current rapid climate warming.