Exposure of nontarget populations to agricultural chemicals is an important aspect of global change. We quantified the capacity of natural Daphnia magna populations to locally adapt to insecticide exposure through a selection experiment involving carbaryl exposure and a control. Carbaryl tolerance after selection under carbaryl exposure did not increase significantly compared to the tolerance of the original field populations. However, there was evolution of a decreased tolerance in the control experimental populations compared to the original field populations. The magnitude of this decrease was positively correlated with land use intensity in the neighbourhood of the ponds from which the original populations were sampled. The genetic change in carbaryl tolerance in the control rather than in the carbaryl treatment suggests widespread selection for insecticide tolerance in the field associated with land use intensity and suggests that this evolution comes at a cost. Our data suggest a strong impact of current agricultural land use on nontarget natural Daphnia populations.

Anthropogenic global warming has become a major geological and environmental force driving drastic changes in natural ecosystems. Due to the high thermal conductivity of water and the effects of temperature on metabolic processes, freshwater ecosystems are among the most impacted by these changes. The ability to tolerate changes in temperature may determine species long-term survival and fitness. Therefore, it is critical to identify coping mechanisms to thermal and hyper-thermal stress in aquatic organisms. A central regulatory element compensating for changes in oxygen supply and ambient temperature is the respiratory protein haemoglobin (Hb). Here, we quantify Hb plastic and evolutionary response in Daphnia magna subpopulations resurrected from the sedimentary archive of a lake with known history of increase in average temperature and recurrence of heat waves. By measuring constitutive changes in crude Hb protein content among subpopulations, we assessed evolution of the Hb gene family in response to temperature increase. To quantify the contribution of plasticity in the response of this gene family to hyper-thermal stress, we quantified changes in Hb content in all subpopulations under hyper-thermal stress as compared to nonstressful temperature. Further, we tested competitive abilities of genotypes as a function of their Hb content, constitutive and induced. We found that Hb-rich genotypes have superior competitive abilities as compared to Hb-poor genotypes under hyper-thermal stress after a period of acclimation. These findings suggest that whereas long-term adjustment to higher occurrence of heat waves may require a combination of plasticity and genetic adaptation, plasticity is most likely the coping mechanism to hyper-thermal stress in the short term. Our study suggests that with higher occurrence of heat waves, Hb-rich genotypes may be favoured with potential long-term impact on population genetic diversity.

There is growing evidence of rapid genetic adaptation of natural populations to environmental change, opening the perspective that evolutionary trait change may subsequently impact ecological processes such as population dynamics, community composition, and ecosystem functioning. To study such eco-evolutionary feedbacks in natural populations, however, requires samples across time. Here, we capitalize on a resurrection ecology study that documented rapid and adaptive evolution in a natural population of the water flea Daphnia magna in response to strong changes in predation pressure by fish, and carry out a follow-up mesocosm experiment to test whether the observed genetic changes influence population dynamics and top-down control of phytoplankton. We inoculated populations of the water flea D. magna derived from three time periods of the same natural population known to have genetically adapted to changes in predation pressure in replicate mesocosms and monitored both Daphnia population densities and phytoplankton biomass in the presence and absence of fish. Our results revealed differences in population dynamics and top-down control of algae between mesocosms harboring populations from the time period before, during, and after a peak in fish predation pressure caused by human fish stocking. The differences, however, deviated from our a priori expectations. An S-map approach on time series revealed that the interactions between adults and juveniles strongly impacted the dynamics of populations and their top-down control on algae in the mesocosms, and that the strength of these interactions was modulated by rapid evolution as it occurred in nature. Our study provides an example of an evolutionary response that fundamentally alters the processes structuring population dynamics and impacts ecosystem features.

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.

There is growing evidence that urbanization drives adaptive evolution in response to thermal gradients. One such example is documented in the water flea Daphnia magna. However, organisms residing in urban lentic ecosystems are increasingly exposed to chemical pollutants such as pesticides through run-off and aerial transportation. The extent to which urbanization drives the evolution of pesticide resistance in aquatic organisms and whether this is impacted by warming and thermal adaptation remains limitedly studied. We performed a common garden rearing experiment using multiple clonal lineages originating from five replicated urban and rural D. magna populations, in which we implemented an acute toxicity test exposing neonates (<24h) to either a solvent control or the organophosphate pesticide chlorpyrifos. Pesticide exposures were performed at two temperatures (20°C vs. 24°C) to test for temperature-associated differences in urbanization-driven evolved pesticide resistance. We identified a strong overall effect of pesticide exposure on Daphnia survival probability (-72.8 percentage points). However, urban Daphnia genotypes showed higher survival probabilities compared to rural ones in the presence of chlorpyrifos (+29.7 percentage points). Our experiment did not reveal strong temperature x pesticide or temperature x pesticide x urbanization background effects on survival probability. The here observed evolution of resistance to an organophosphate pesticide is a first indication Daphnia likely also adapts to pesticide pollution in urban areas. Increased pesticide resistance could facilitate their population persistence in urban ponds, and feed back to ecosystem functions, such as top-down control of algae. In addition, adaptive evolution of nontarget organisms to pest control strategies and occupational pesticide use may modulate how pesticide applications affect genetic and species diversity in urban areas.

Understanding whether populations and communities can evolve fast enough to keep up with ongoing climate change is one of the most pressing issues in biology today. A growing number of studies have documented rapid evolutionary responses to warming, suggesting that populations may be able to persist despite temperature increases. The challenge now is to better understand how species interactions, which are ubiquitous in nature, mediate these population responses to warming. Here, we use laboratory natural selection experiments in a freshwater community to test hypotheses related to how thermal evolution of Daphnia pulex to two selection temperatures (12 and 18°C) is mediated by rapid thermal evolution of its algal resource (Scenedesmus obliquus) or by the presence of the zooplankton predator Chaoborus americanus. We found that cold-evolved algae (a high-quality resource) facilitated the evolution of increased thermal plasticity in Daphnia populations selected at 12°C, for both body size and per capita growth rates (r). Conversely, warm-evolved algae facilitated the evolution of increased r thermal plasticity for Daphnia selected at 18°C. Lastly, we found that the effect of selection temperature on evolved Daphnia body size was more pronounced when Daphnia were also reared with predators. These data demonstrate that trait evolution of a focal population to the thermal environment can be affected by both bottom-up and top-down species interactions and that rapid temperature evolution of a resource can have cascading effects on consumer thermal evolution. Our study highlights the importance of incorporating species interactions when estimating ecological and evolutionary responses of populations and communities to ongoing temperature warming.

While human-induced stressors such as warming and pollutants may co-occur and interact, evolutionary studies typically focus on single stressors. Rapid thermal evolution may help organisms better deal with warming, yet it remains an open question whether thermal evolution changes the toxicity of pollutants under warming. We investigated the effects of exposure to a novel pollutant (zinc oxide nanoparticles, nZnO) and 4°C warming (20°C vs. 24°C) on key life history and physiological traits of the water flea Daphnia magna, a keystone species in aquatic ecosystems. To address the role of thermal evolution, we compared these effects between clones from an experimental evolution trial where animals were kept for two years in outdoor mesocosms at ambient temperatures or ambient +4°C. The nZnO was more toxic at 20°C than at 24°C: only at 20°C, it caused reductions in early fecundity, intrinsic growth rate and metabolic activity. This was due to a higher accumulated zinc burden at 20°C than at 24°C, which was associated with an upregulation of a metallothionein gene at 20°C but not at 24°C. Clones from the heated mesocosms better dealt with warming than clones from the ambient mesocosms, indicating rapid thermal evolution. Notably, rapid thermal evolution did not change the toxicity of nZnO, neither at 20°C nor at 24°C, suggesting no pleiotropy or metabolic trade-offs were at work under the current experimental design. Evaluating whether thermal evolution influences the toxicity of pollutants is important for ecological risk assessment. It provides key information to extrapolate laboratory-derived toxicity estimates of pollutants both in space to warmer regions and in time under future global warming scenarios. In general, studying how the evolution of tolerance to one anthropogenic stressor influence tolerance to other anthropogenic stressors should get more attention in a rapidly changing world where animals increasingly face combinations of stressors.