Abstract

The invasive fruit fly pest, Drosophila suzukii, is a chill susceptible species, yet it is capable of overwintering in rather cold climates, such as North America and North Europe, probably thanks to a high cold tolerance plasticity. Little is known about the mechanisms underlying cold tolerance acquisition in D. suzukii. In this study, we compared the effect of different forms of cold acclimation (at juvenile or at adult stage) on subsequent cold tolerance. Combining developmental and adult cold acclimation resulted in a particularly high expression of cold tolerance. As found in other species, we expected that cold-acclimated flies would accumulate cryoprotectants and would be able to maintain metabolic homeostasis following cold stress. We used quantitative target GC-MS profiling to explore metabolic changes in four different phenotypes: control, cold acclimated during development or at adult stage or during both phases. We also performed a time-series GC-MS analysis to monitor metabolic homeostasis status during stress and recovery. The different thermal treatments resulted in highly distinct metabolic phenotypes. Flies submitted to both developmental and adult acclimation were characterized by accumulation of cryoprotectants (carbohydrates and amino acids), although concentrations changes remained of low magnitude. After cold shock, non-acclimated chill-susceptible phenotype displayed a symptomatic loss of metabolic homeostasis, correlated with erratic changes in the amino acids pool. On the other hand, the most cold-tolerant phenotype was able to maintain metabolic homeostasis after cold stress. These results indicate that cold tolerance acquisition of D. suzukii depends on physiological strategies similar to other drosophilids: moderate changes in cryoprotective substances and metabolic robustness. In addition, the results add to the body of evidence supporting that mechanisms underlying the different forms of acclimation are distinct.

Highlights

  • Extreme temperatures often negatively affect survival of ectothermic animals as well as their biological functions such as reproduction, respiration, digestion, or excretion (Chown and Nicolson, 2004; Angilletta, 2009)

  • This study revealed that combining both developmental and adult cold acclimation resulted in a high expression of cold tolerance in D. suzukii

  • Our results indicate that cold tolerance plasticity of D. suzukii relies on physiological strategies similar to other drosophilids

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Summary

Introduction

Extreme temperatures often negatively affect survival of ectothermic animals as well as their biological functions such as reproduction, respiration, digestion, or excretion (Chown and Nicolson, 2004; Angilletta, 2009). In order to reduce the negative effects of temperature on their performances, ectotherms are capable of modulating thermal tolerance during their lifetime using a range of physiological adjustments that take place after pre-exposure to sub-lethal temperatures, a phenomenon referred to as thermal acclimation (Angilletta, 2009; Colinet and Hoffmann, 2012). Physiological adjustments occurring during development, like those related to acquired cold tolerance, are not necessarily everlasting (Piersma and Drent, 2003). Cold tolerance acquired during development is readily adjusted to the prevailing conditions during adult acclimation without a detectable developmental constraint (Slotsbo et al, 2016). The different forms of acclimation probably lie along a continuum of shared common mechanisms; several lines of evidence suggest that physiological underpinnings of each acclimation form show some specificity (Colinet and Hoffmann, 2012; Teets and Denlinger, 2013; Gerken et al, 2015)

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