Cold adaptation shapes the robustness of metabolic networks inDrosophila melanogaster

Abstract

When ectotherms are exposed to low temperatures, they enter a cold-induced coma (chill coma) that prevents resource acquisition, mating, oviposition, and escape from predation. There is substantial variation in time taken to recover from chill coma both within and among species, and this variation is correlated with habitat temperatures such that insects from cold environments recover more quickly. This suggests an adaptive response, but the mechanisms underlying variation in recovery times are unknown, making it difficult to decisively test adaptive hypotheses. We use replicated lines of Drosophila melanogaster selected in the laboratory for fast (hardy) or slow (susceptible) chill-coma recovery times to investigate modifications to metabolic profiles associated with cold adaptation. We measured metabolite concentrations of flies before, during, and after cold exposure using NMR spectroscopy to test the hypotheses that hardy flies maintain metabolic homeostasis better during cold exposure and recovery, and that their metabolic networks are more robust to cold-induced perturbations. The metabolites of cold-hardy flies were less cold responsive and their metabolic networks during cold exposure were more robust, supporting our hypotheses. Metabolites involved in membrane lipid synthesis, tryptophan metabolism, oxidative stress, energy balance, and proline metabolism were altered by selection on cold tolerance. We discuss the potential significance of these alterations.

Arginine and proline applied as food additives stimulate high freeze tolerance in larvae of Drosophila melanogaster

“…Similarly complex perturbation of metabolic pathways and metabolomic composition was also documented in response to a change of temperature (Williams et al, 2014). Such complexity complicates interpretation of the results.…”

Cold adaptation increases rates of nutrient flow and metabolic plasticity during cold exposure inDrosophila melanogaster

“…Chill coma recovery time has a genetic basis and responds to climatic selection, showing latitudinal clines on multiple continents whereby insects from colder regions recover more quickly [10,11], and a robust response to artificial selection [12][13][14]. Chill coma onset occurs due to failure of the neuromuscular system, and ionic and osmotic homoeostasis are progressively lost during low-temperature exposure [15,16].…”

Hemolymph metabolites and osmolality are tightly linked to cold tolerance ofDrosophilaspecies: a comparative study

“…Drosophila equinoxialis and D. melanogaster showed smaller but qualitatively similar responses with the addition of an increase in the possible purine. Increases in maltose levels have previously been found in response to cold shock treatments in D. melanogaster (Overgaard et al, 2007;Pedersen et al, 2008) and maltose has also been found to increase in D. melanogaster selected for high chill susceptibility (Williams et al, 2014). Maltose has been linked to the protection and function of proteins and membranes during temperature stress (Kaplan and Guy, 2004;Pereira and Hünenberger, 2006), and maltose accumulation has been linked to a stress-induced increase in amylase activity in plants ( Kaplan and Guy, 2004).…”

“…The relatively small response to cold exposure suggests that these species maintain their metabolite homeostasis far better than the chill-susceptible species. Similarly, the metabolomes of cold-selected, cold-acclimated and rapidly cold-hardened D. melanogaster are less responsive to cold exposure than warm-acclimated flies or flies directly exposed to a cold shock (Overgaard et al, 2007;Colinet et al, 2012;Williams et al, 2014). The increases in trehalose and the possible purine found in response to cold in D. persimilis and D. montana seem to be adaptive for coping with the cold stress.…”