Physiological responses of cold acclimation in Drosophila suzukii

The spotted wing drosophila (SWD) Drosophila suzukii is an invasive pest. To control this pest, information about its cold tolerance is required. Several studies have focused on SWD overwintering strategies and reported increased cold tolerance of winter morph (WM) compared to summer morph (SM). However, underlying mechanisms of this difference are not yet known. Our first goal was to study the impact of WM-inducing conditions on SWD cold tolerance and their metabolites composition. We expected to find an accumulation of cryoprotectant metabolites in cold hardy WM flies. Flies were reared at 25°C to induce SM, or at 10°C to induce WM. Cold tolerance was assayed by measuring survival after a stress at
-5°C/1h40, minimal critical temperature and chill coma recovery. All metrics confirmed that WM-inducing conditions deeply promoted cold tolerance. SM and WM metabotypes were compared using target and quantitative GC/MS profiling. WM were characterized by an accumulation of several carbohydrates and amino acids, but quantitative changes were rather small (max 6 fold-change). Because robustness in metabolic networks is supposed to be a key element of cold tolerance, we assessed whether different levels of cold acclimation would favor metabolic stability. We generated four different phenotypes: development at 10°C to generate WM that were next acclimated as adults for 7 days at 10 or 25°C (WM10 or WM25) and development at 25°C to generate SM that were next acclimated as adults for 7 days at 10 or 25°C (SM10 or SM25). Using the same measures of cold tolerance, we found that cold tolerance ranked as follow: WM10>SM10>WM25>SM25. Stability of metabolic homeostasis was assessed in these four phenotypic groups using time-series GC/MS profiling. We monitored profiles before, right after, 4h, 8h or 12h after an acute cold shock. During recovery, both WM25 and SM25 metabotypes strongly deviated from origin, and did not return to initial state. This alteration was correlated with uncontrolled augmentation of the total amount of amino acids, which is symptomatic of cold injuries. WM10 presented the strongest temporal stability of metabolic profiles, suggesting a capacity to maintain homeostasis in this cold hardy phenotype. Finally, SM10 presented an intermediate response (as for cold tolerance). Data suggest that the proximal acclimation treatment (ie. at adult stage) is more critical in promoting cold tolerance that acclimation during development. Data corroborate that cold hardiness is associated to metabolic stability during stress and recovery. These results give new information to understand SWD cold tolerance.