Thermal evolution offsets the elevated toxicity of a contaminant under warming: A resurrection study in Daphnia magna

Abstract

Synergistic interactions between temperature and contaminants are a major challenge for ecological risk assessment, especially under global warming. While thermal evolution may increase the ability to deal with warming, it is unknown whether it may also affect the ability to deal with the many contaminants that are more toxic at higher temperatures. We investigated how evolution of genetic adaptation to warming affected the interactions between warming and a novel stressor: zinc oxide nanoparticles (nZnO) in a natural population of Daphnia magna using resurrection ecology. We hatched resting eggs from two D. magna subpopulations (old: 1955–1965, recent: 1995–2005) from the sediment of a lake that experienced an increase in average temperature and in recurrence of heat waves but was never exposed to industrial waste. In the old “ancestral” subpopulation, exposure to a sublethal concentration of nZnO decreased the intrinsic growth rate, metabolic activity, and energy reserves at 24°C but not at 20°C, indicating a synergism between warming and nZnO. In contrast, these synergistic effects disappeared in the recent “derived” subpopulation that evolved a lower sensitivity to nZnO at 24°C, which indicates that thermal evolution could offset the elevated toxicity of nZnO under warming. This evolution of reduced sensitivity to nZnO under warming could not be explained by changes in the total internal zinc accumulation but was partially associated with the evolution of the expression of a key metal detoxification gene under warming. Our results suggest that the increased sensitivity to the sublethal concentration of nZnO under the predicted 4°C warming by the end of this century may be counteracted by thermal evolution in this D. magna population. Our results illustrate the importance of evolution to warming in shaping the responses to another anthropogenic stressor, here a contaminant. More general, genetic adaptation to an environmental stressor may ensure that synergistic effects between contaminants and this environmental stressor will not be present anymore.

Stoichiometric responses to nano ZnO under warming are modified by thermal evolution in Daphnia magna

“…This was because nZnO only increased the body P content but did not change body C and N contents under warming. This increase in P content was not related to increases in P-rich RNA, which instead decreased under nZnO exposure at 24°C (Zhang et al, 2018). Moreover, we could not detect a relationship at the individual level between the P content and the RNA content in current study.…”

“…These deviations were explained by reductions in both C-rich fat and sugars and in N-rich proteins (Janssens et al, 2017), and a higher incorporation of carbon relative to nitrogen (Ek et al, 2015), respectively. In current study, this marginal decrease could be only partly explained by the associated decrease of the C-rich sugar content, as this decrease in sugar content was only observed at 24°C (Zhang et al, 2018). Furthermore, while we detected the expected positive relationship at the individual level between the sugar content and the C content in this subpopulation, this relationship was of moderate strength (R² = 0.28).…”

“…We compared the effects of nZnO and warming on Daphnia body stoichiometry (C, N and P contents and their ratios) in these two subpopulations. In a companion study (Zhang et al, 2018), we found that nZnO changed the macromolecules assumed to be important for body stoichiometry by the GSP (C-rich sugar and fat, N-rich proteins, and Prich RNA) and also found that these changes differed between the two subpopulations. Specifically, nZnO exposure reduced the sugar content at 24°C in both subpopulations, but the reduction was doubled in the recent subpopulation compare to the old subpopulation.…”

“…To test for relationships between body stoichiometry and the assumed associated macromolecules, we regressed the three elements against the associated macromolecule: carbon against sugars and fat, nitrogen against proteins, and phosphorus against RNA (contents of sugars, fat and proteins see Zhang et al (2018), RNA content see supporting information). We did so for each subpopulation separately.…”

Effects of Pollution on Fish Behavior, Personality, and Cognition: Some Research Perspectives

“…For instance, some families of Atlantic salmon Salmo salar that are tolerant to high-temperature are also more tolerant to hypoxia, because of increased heart ventricle size and myoglobin levels, although the evolutionary implications are still unclear (e.g., Anttila et al, 2013). In another study, some Daphnia magna populations are co-adapted to warming and increased toxicity (Zhang et al, 2018). However, most previous studies focused on physiological and life-history traits, so that the evolution of behavioral traits in a multiple stress framework remains unclear.…”