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

Abstract

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.

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

“…Furthermore, Dahlhoff et al (2019) showed that development was slower at higher elevations in the leaf beetle Chrysomela aeneicollis because of a reduction in metabolic rate. That said, in A. iberica, the opposite was observed along the same study gradient as ours: Shik, Arnan, Oms, Cerdá, and Boulay (2019) discovered that the metabolic rates of ants from higher elevations increased faster at low temperatures but that the temperature at which metabolic rates levelled out was the same across populations. They also observed that body size (mg of dry mass) was significantly larger for higher elevation ants than for lower elevation ants.…”

Temperature drives caste‐specific morphological clines in ants

“…Previous studies instead focused either on intraspecific clines for a small number of species, interspecific clines or community-wide clines. At the intraspecific level, previous work shows that ants increase in size with increasing latitude (Heinze et al, 2003) and elevations (Bernadou, Römermann, Gratiashvili, & Heinze, 2016;Purcell, Pirogan, Avril, Bouyarden, & Chapuisat, 2016;Shik, Arnan, Oms, Cerdá, & Boulay, 2019), consistent with the hypothesis that lower temperatures lead to larger body size.…”

Adaptations to thermal stress in social insects: recent advances and future directions

“…Taking into account seasonal variation, social organisation, and life‐history traits, it showed that variation in body size was generally consistent with Bergmann's rule. In ants, Aphaenogaster iberica workers have been found to be larger at higher latitudes (Shik et al ., 2019). Furthermore, in a number of social insect species, researchers have observed a positive relationship between body size and heat tolerance, where larger workers were more heat resistant than smaller workers [ants (Cerdá & Retana, 1997, Cerdá & Retana, 2000, Clémencet et al ., 2010, Oberg, del Toro, & Pelini, 2012, Baudier et al ., 2015, Baudier & O'Donnell, 2016, 2017, Wendt & Verble‐Pearson, 2016); termites (Janowiecki et al ., 2019)].…”

“…In honeybee ( Apis mellifera ) populations adapted to colder climates, major energy‐producing mitochondrial pathways were found to be upregulated (Parker et al ., 2010). In both ants ( Aphaenogaster iberica ; Shik et al ., 2019) and wasps ( Polistes dominula , Kovac et al ., 2017), workers from populations found at higher altitudes had higher metabolic rates than did workers from populations found at lower altitudes.…”