Molecular adaptations to heat stress in the thermophilic ant genus Cataglyphis

Abstract

Over the last decade, increasing attention has been paid to the molecular adaptations used by organisms to cope with thermal stress. However, to date, few studies have focused on thermophilic species living in hot, arid climates. In this study, we explored molecular adaptations to heat stress in the thermophilic ant genus Cataglyphis, one of the world's most thermotolerant animal taxa. We compared heat tolerance and gene expression patterns across six Cataglyphis species from distinct phylogenetic groups that live in different habitats and experience different thermal regimes. We found that all six species had high heat tolerance levels with critical thermal maxima (CT max ) ranging from 43℃ to 45℃ and a median lethal temperature (LT50) ranging from 44.5℃ to 46.8℃. Transcriptome analyses revealed that, although the number of differentially expressed genes varied widely for the six species (from 54 to 1118), many were also shared. Functional annotation of the differentially expressed and co-expressed genes showed that the biological pathways involved in heat-shock responses were similar among species and were associated with four major processes: the regulation of transcriptional machinery and DNA metabolism; the preservation of proteome stability; the elimination of toxic residues; and the maintenance of cellular integrity. Overall, our results suggest that molecular responses to heat stress have been evolutionarily conserved in the ant genus Cataglyphis and that their diversity may help workers withstand temperatures close to their physiological limits.

Facing lethal temperatures: heat shock response in desert and temperate ants

“…We characterized and compared the heat tolerance and the heat stress transcriptomic response of four ecological equivalent desert ant species from three distinct genera, and of two outgroup species living in a temperate region. From all 6 studied species, the red honey ant Melophorus bagoti was the most heat tolerant, withstanding the highest temperatures ever reported in ants [10,32–34]. However, in natural habitats, the Sahara silver ant Cataglyphis bombycina is the species known to endure the most environmental heat, with a mean temperature in the warmest quarter of 30.8°C and maximum temperature of 42.3°C (Table S1).…”

“…Likewise, the production of antioxidants and detoxification enzymes, like super oxide dismutase (SOD) or glutathione peroxidase (GPx), helps reducing the accumulation of reactive oxygen species (ROS) [9]. Under heat stress, these molecular pathways interact composing an intricate multi-level response that, despite its complexity, must be rapidly activated to optimize survival [10]. This response is expected to be particularly important in small ectotherms – like insects – whose body temperature is highly correlated to that of their local environment [11].…”

“…They can withstand body temperature exceeding 45°C during a long period of time [22–24]; their legs are considerably longer relatively to their body size, which maximizes the distance between their body and the burning ground and allows higher running speed reducing foraging time and enhancing forced convective cooling [25,26]; and they periodically exploit thermal refuges in shaded areas or ground elevated places to benefit from cooler spots [20]. Recently, our group has characterized the transcriptomic heat shock response of six Cataglyphis species from different habitats and thermal regimes [10,27]. We found that the Cataglyphis heat stress response builds upon the co-expression of gene clusters mainly involved in proteome stability, elimination of toxic residues, DNA/RNA metabolism and the maintenance of cell integrity through membrane modification and cytoskeletal rearrangements.…”

Egg-Laying Behavior of Cataglyphis niger Ants Is Influenced More Strongly by Temperature Than Daylength

“…Cataglyphis species are day-active at high temperatures [ 19 , 20 ] and possess several molecular and physiological tools to cope with heat stress, such as a mechanism to maintain cellular integrity [ 21 , 22 ]. They are solitary foragers and lack pheromone-based recruitment while foraging although information on the existence of food nearby triggers workers to leave the nest and forage [ 23 , 24 ].…”

Chromosome-level genome assembly and annotation of two lineages of the ant Cataglyphis hispanica: stepping stones towards genomic studies of hybridogenesis and thermal adaptation in desert ants

“…For instance, workers of the silver ant Cataglyphis bombycina have been observed to forage when ground temperatures exceed 60°C (Wehner et al 1992), which supposedly provides a competitive advantage against lizard predators who avoid such harsh conditions. The high thermal tolerance seen in Cataglyphis species relies on a range of behavioral, morphological, physiological and molecular adaptations, such as exploitation of thermal refuges, elongated legs, high speed of movement and intense recruitment of heat-shock chaperone proteins (Aron and Wehner 2021;Gehring and Wehner 1995;Perez and Aron 2020;Perez et al 2021;Pfeffer et al 2019;Sommer and Wehner 2012;Willot et al 2017).…”