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

Abstract

Metabolic flexibility is an important component of adaptation to stressful environments, including thermal stress and latitudinal adaptation. A long history of population genetic studies suggest that selection on core metabolic enzymes may shape life histories by altering metabolic flux. However, the direct relationship between selection on thermal stress hardiness and metabolic flux has not previously been tested. We investigated flexibility of nutrient catabolism during cold stress in Drosophila melanogaster artificially selected for fast or slow recovery from chill coma (i.e. cold-hardy or -susceptible), specifically testing the hypothesis that stress adaptation increases metabolic turnover. Using 13 C-labelled glucose, we first showed that cold-hardy flies more rapidly incorporate ingested carbon into amino acids and newly synthesized glucose, permitting rapid synthesis of proline, a compound shown elsewhere to improve survival of cold stress. Second, using glucose and leucine tracers we showed that cold-hardy flies had higher oxidation rates than coldsusceptible flies before cold exposure, similar oxidation rates during cold exposure, and returned to higher oxidation rates during recovery. Additionally, cold-hardy flies transferred compounds among body pools more rapidly during cold exposure and recovery. Increased metabolic turnover may allow cold-adapted flies to better prepare for, resist and repair/tolerate cold damage. This work illustrates for the first time differences in nutrient fluxes associated with cold adaptation, suggesting that metabolic costs associated with cold hardiness could invoke resource-based trade-offs that shape life histories. BackgroundTemperature fluctuates markedly on daily and seasonal time scales in temperate regions, and for ectotherms these fluctuations can shape organismal performance and fitness [1], predict distributional limits [2], and may even exert greater selective pressure than mean temperatures [3]. Temperature fluctuations challenge energetic homeostasis in ectothermic animals, and thermal adaptation probably involves modulation of the thermal sensitivity of metabolic pathways. Demand for ATP regulates rates of substrate catabolism, and, under normal conditions, energy supply is matched to demand [4]. However, environmental fluctuations can upset the balance between energy supply and demand, and persistent energetic perturbations can result in declines in performance or death [5]. Resistance or tolerance to stressful

Life-extending dietary restriction, but not dietary supplementation of branched-chain amino acids, can increase organismal oxidation rates of individual branched-chain amino acids by grasshoppers

“…This represents the BCAAs that are oxidized immediately, probably before incorporation into a protein; additional BCAAs would be oxidized later. Further, similar magnitudes of 13 C-amino acid recovery in the breath have been reported in other insects [40,41], amphibians [42], reptiles [43], birds [44], and mammals [45]. Does this reduction in available BCAAs due to mild (but often statistically significant) increases in oxidation contribute to health?…”

Colder environments did not select for a faster metabolism during experimental evolution of Drosophila melanogaster

“…We cannot dismiss the possibility that a selective treatment with a constant temperature below 16°C might select for a higher metabolic rate, especially if there are metabolic costs associated with cold hardiness (Williams et al. , b); however, 16°C is close to the minimum temperature for reproduction in D. melanogaster (∼13°C: Cooper et al. ; Condon et al.…”

Cold adaptation drives population genomic divergence in the ecological specialist,Drosophila montana

“…Importantly, there is evidence for a close link between the desiccation stress response and cold tolerance across species and in Drosophila in particular, suggesting an overlap in some of the mechanisms involved (Sinclair, Nelson, Nilson, Roberts, & Gibbs, 2007). Moreover, cold-hardy lines of D. melanogaster are known to exhibit elevated lipid metabolism, perhaps in order to allow rapid lipid membrane modification (Williams et al, 2016) in different environmental conditions. Furthermore, Pleckstrin homology (PH) domain was one of the functional clusters found in both the current study and in the species comparison of Parker et al, (2018).…”