Abstract
Examples of phenotypic plasticity—the ability of organisms of identical genotypes to produce different phenotypes in response to the environment—are abundant, but often lack data on the causative physiology and biochemistry. Phenotypes associated with increased protection against or reduced damage from harmful environments may, in fact, be downstream effects of hidden adaptive responses that remain elusive to experimental measurement or be obscured by homeostatic or over-compensatory effects. The freshwater zooplankton crustacean Daphnia drastically increases its heat tolerance as the result of acclimation to high temperatures, an effect often assumed to be based on plastic responses allowing better protection against oxidative stress. Using several geographically distant Daphnia magna genotypes, we demonstrate that the more heat tolerant individuals have a higher total antioxidant capacity (TAC) both in the comparison of heat-acclimated vs. non heat-acclimated females and in the comparison of females to age- and body size-matched males, which show lower heat tolerance than females. However, experimental manipulations of hypothesized antioxidant pathways by either glutathione addition or glutathione synthesis inhibition had no effect on heat tolerance. Lipid peroxidation (LPO), contrary to expectations, did not appear to be a predictive measure of susceptibility to thermal damage: LPO was higher, not lower, in more heat tolerant heat-acclimated individuals after exposure to a lethally high temperature. We hypothesize that LPO may be maintained in Daphnia at a constant level in the absence of acute exposure to elevated temperature and increase as a by-product of a possible protective antioxidant mechanism during such exposure. This conclusion is corroborated by the observed short-term and long-term changes in phospholipid composition that included an increase in fatty acid saturation at 28 °C and up-regulation of certain long-chain polyunsaturated fatty acids. Phospholipid composition was more strongly affected by recently experienced temperature (4-day transfer) than by long-term (2 generations) temperature acclimation. This is consistent with partial loss of thermal tolerance after a short-term switch to a reciprocal temperature. As predicted under the homeoviscous adaptation hypothesis, the more heat tolerant Daphnia showed lower membrane fluidity than their less heat tolerant counterparts, in comparison both between acclimation temperatures and among different genotypes. We conclude that thermal tolerance in Daphnia is influenced by total antioxidant capacity and membrane fluidity at high temperatures, with both effects possibly reflecting changes in phospholipid composition.
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Abbreviations
- BSO:
-
Buthionine sulfoximine
- CumHO:
-
Cumene hydroperoxide
- DPH:
-
1,6-diphenyl-hexa-1,3,5-triene
- DTT:
-
Dithiotreitol
- FDR:
-
False discovery rate
- FI:
-
Fluorescence intensity
- FP:
-
Fluorescence polarization
- GH:
-
Glutathione (reduced)
- LPO:
-
Lipid peroxidation
- TAC:
-
Total antioxidant capacity
- PA:
-
Phosphatidic acids
- PC:
-
Phosphatiditcholines
- PC[n]:
-
Principal component #n
- PCA:
-
Principal component analysis
- PE:
-
Phosphatidylethanolamines
- PFI:
-
Phospholipid fluidity index
- PG:
-
Phosphatidylglycerols
- PI:
-
Phosphatidylinositols
- PS:
-
Phosphatidylserines
- PUFA:
-
Polyunsaturated fatty acid
- ROS:
-
Reactive oxygen species
- SM:
-
Sphingomyelins
- T imm :
-
Time until immobilization
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Acknowledgements
We are grateful to Dhirendra Kumar for equipment use, to Anthony C. Tharp and Irina Kaverina for assistance with fluorescence polarization measurements and to Joe Bidwell, Dieter Ebert, Karl Joplin, Aruna Kilaru, Dominik Martin-Creuzburg, and Roberto Arbore for many useful suggestions. This work was partly supported by NSF DEB-1136706 to LYY and ETSU Student-Faculty Collaboration grants to BLC and JWC.
Author contributions
LYY designed the study, participated in the experimental work, analyzed the data, and wrote the manuscript. BLC, JC, and KJH did the experimental work and participated in data analysis and writing the manuscript.
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Communicated by I. D. Hume.
B. L. Coggins, J. W. Collins, and K. J. Holbrook contributed equally to the work and are listed alphabetically.
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Coggins, B.L., Collins, J.W., Holbrook, K.J. et al. Antioxidant capacity, lipid peroxidation, and lipid composition changes during long-term and short-term thermal acclimation in Daphnia . J Comp Physiol B 187, 1091–1106 (2017). https://doi.org/10.1007/s00360-017-1090-9
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DOI: https://doi.org/10.1007/s00360-017-1090-9