Asymmetric Micro-Evolutionary Responses in a Warming World: Heat-Driven Adaptation Enhances Metal Tolerance in a Planktonic Rotifer, but Not Vice Versa

Abstract

The resilience of natural populations in the face of global environmental change is determined by their ability to adapt to multiple, often interacting, stressors. Microevolutionary adaptation to one stressor can either enhance or reduce tolerance to other stressors. In the context of climate change, it is crucial to understand the effect of warming on the tolerance of organisms to additional environmental challenges. Conversely, adaptation to localized stressors, such as pollution, may also affect an organism's capacity to withstand climate change. Here, we investigate how prior adaptation to either high temperature or copper (Cu) contamination influences subsequent tolerance to the other stressor in populations of the freshwater zooplanktonic rotifer Brachionus calyciflorus (Pallas, 1766). Using an experimental evolution approach, we subjected populations to either gradually increasing Cu levels, elevated temperature, or control conditions over multiple generations. Subsequently, we conducted a common garden experiment to assess the effect of selection history on population performance. We found that heat-adapted populations exhibited increased tolerance to Cu, whereas Cu-adapted populations showed no enhanced tolerance to high temperatures. This form of "asymmetric cross-adaptation" is likely driven by selection for generalized stress responses associated with heat adaptation, while Cu adaptation selected for more specialized detoxification mechanisms with limited cross-protection. These findings suggest that the legacy of warming may enhance population tolerance to other stressors, whereas the benefits of adaptation to local pollution may be more constrained. Our study highlights the need to assess the generality of such patterns across taxa and stressor combinations, as this knowledge could inform environmental management strategies in multi-stressor contexts.

Keywords: climate change; copper toxicity; cross‐adaptation; cross‐tolerance; heat stress; micro‐evolutionary adaptation; pollution.

FIGURE 1

Experimental design. (a) Design of the selection experiment. Using 50 randomly selected genotypes from an ancestral population, we created nine genetically identical populations, three of which subsequently received stepwise increases in Cu concentrations at room temperature (starting at 30 μg·L⁻¹ Cu and finishing at 65 μg·L⁻¹ Cu at 22°C; “Cu‐selected populations”), three received increasing temperature levels (starting at 24°C and finishing at 35.5°C; “Heat‐selected populations”), whereas the remaining three received no Cu and were kept at room temperature (“Control populations”; 22°C). At each stress level, populations went through a cycle consisting of a period of population growth followed by sexual reproduction (See Figure S1); (b) design of the common garden experiment. For each of the nine populations obtained from the selection experiment, we established four clonal lines from dormant propagules produced after the final cycle in the evolution experiment. In addition, we used six clonal lines from propagules from the ancestral population (“Ancestral”). Experimental populations of all of these lines were individually exposed to control conditions (Control), a high Cu concentration (62.5 μg·L⁻¹ Cu; “Cu”), heat (34°C) and the combination of high Cu concentrations and heat (62.5 μg·L⁻¹ Cu and 34°C; “Cu+Heat”), resulting in a total of 168 experimental units.

FIGURE 2

(a) Population growth rate (r), (b) mortality, and (c) fecundity of Ancestral, Control, Cu‐, and Heat‐selected populations in response to the Control, Cu, and Heat treatments of the common garden experiment. Symbols and error bars represent means and 95% confidence intervals across population replicates of the selection experiment. Letters denote differences according to post hoc Tuckey pairwise comparisons (alpha = 0.05). Note that, because Ancestral populations did not align with the experimental design, they were not included in this post hoc comparison. Small symbols represent individual clones where different symbol types identify clones that originated from the same population in the selection experiment.

FIGURE 3

Population growth rate (r) of Ancestral, Control, Cu‐ and Heat‐selected populations in response to the Control, Cu, Heat, and Cu+Heat treatments of the common garden experiment, based on the dataset from which we omitted the data of the clones of the Control and Cu‐selected populations that failed to survive the Cu+Heat treatment (see Section 2). Symbols and error bars represent means and 95% confidence intervals across population replicates of the selection experiment. Letters denote differences according to post hoc Tuckey pairwise comparisons (alpha = 0.05).