Rapid Adjustments in Thermal Tolerance and the Metabolome to Daily Environmental Changes - A Field Study on the Arctic Seed Bug Nysius groenlandicus.

Natasja Krog Noer,Mathias Hamann Sørensen,Torsten Nygaard Kristensen,Hervé Colinet,Simon Bahrndorff,David Renault

doi:10.3389/fphys.2022.818485

Abstract

Laboratory investigations on terrestrial model-species, typically of temperate origin, have demonstrated that terrestrial ectotherms can cope with daily temperature variations through rapid hardening responses. However, few studies have investigated this ability and its physiological basis in the field. Especially in polar regions, where the temporal and spatial temperature variations can be extreme, are hardening responses expected to be important. Here, we examined diurnal adjustments in heat and cold tolerance in the Greenlandic seed bug Nysius groenlandicus by collecting individuals for thermal assessment at different time points within and across days. We found a significant correlation between observed heat or cold tolerance and the ambient microhabitat temperatures at the time of capture, indicating that N. groenlandicus continuously and within short time-windows respond physiologically to thermal changes and/or other environmental variables in their microhabitats. Secondly, we assessed underlying metabolomic fingerprints using GC-MS metabolomics in a subset of individuals collected during days with either low or high temperature variation. Concentrations of metabolites, including sugars, polyols, and free amino acids varied significantly with time of collection. For instance, we detected elevated sugar levels in animals caught at the lowest daily field temperatures. Polyol concentrations were lower in individuals collected in the morning and evening and higher at midday and afternoon, possibly reflecting changes in temperature. Additionally, changes in concentrations of metabolites associated with energetic metabolism were observed across collection times. Our findings suggest that in these extreme polar environments hardening responses are marked and likely play a crucial role for coping with microhabitat temperature variation on a daily scale, and that metabolite levels are actively altered on a daily basis.

Highlights

We examined the effects of daily variation in the microhabitat temperatures on plastic adjustments of heat and cold tolerance of the Greenlandic seed bug Nysius groenlandicus (Zetterstedt) during summer in Southern Greenland
Day 5 was characterized by a high temperature variation with an amplitude of 25◦C; the average temperatures at the four collection times differed by 21◦C (Figure 1 and Supplementary Table 1)
We showed that thermal tolerance was correlated with ambient microhabitat temperature in the Greenlandic seed bug, N. groenlandicus

Summary

Introduction

Terrestrial ectotherms are subject to large spatial and temporal variability in their thermal environment (Kearney and Porter, 2009). Organisms, including insects, living in these environments must be able to survive and reproduce over a wide range of temperatures (Deere et al, 2006; Bahrndorff et al, 2021a). This can be achieved by evolutionary adaptation to the local thermal conditions across generations, or by fast adjustments of the physiology within the lifetime of an organism via phenotypic plasticity (Scheiner, 1993; Fusco and Minelli, 2010; Kristensen et al, 2020). Rapid plastic adaptive changes can rescue individuals exposed to biotic and abiotic challenges at a shorter timescale, including daily environmental fluctuations (Colinet and Hoffmann, 2012; Noer et al, 2022). Plastic changes might be relevant for arctic species exposed to unpredictable and rapid changes in the environment

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Discussion

Conclusion