Comparing the ECOS and EVOL responses to warming
The evolutionary ecosystem response of SOC equilibrium to warming combines the non-evolutionary response of the ecosystem and the evolutionary adaptive response of exoenzyme production (Fig. 1c). In all three scenarios of temperature dependence, the SOC non-evolutionary equilibrium generally decreases as temperature or resource allocation to exoenzymes increases (Fig. 1b, Supplementary Figs. 3 and 4, Supplementary Note 3). The negative effect of temperature results from the SOC equilibrium being mostly sensitive to the maximum decomposition rate (\(v_{\max}^{D}\)) (Supplementary Note 3). As the maximum decomposition rate increases with warming, the SOC equilibrium decreases. The SOC equilibrium is always lower in systems where microbes invest more resources in exoenzymes because, all other parameters being fixed, a larger exoenzyme allocation fraction entails that more exoenzymes are produced per unit time, which leads to more SOC decomposed per unit time (Supplementary Note 1).
We therefore predict that, without evolution, the equilibrium soil carbon stock shrinks as the climate warms, in all scenarios of temperature dependence (Fig. 3). The strongest losses occur in initially cold systems due to the non-linear response of the maximum decomposition rate (\(v_{\max}^{D}\)), hence of the SOC equilibrium, to temperature (Fig. 3, Supplementary Figure 4). We expect microbial evolutionary adaptation to alter the non-evolutionary response according to the scenario, from aggravating soil carbon loss in systems where microbes adapt to warming with higher exoenzyme production, to buffering carbon loss from soils where microbes adaptively respond to warming with a lower exoenzyme allocation fraction (Fig. 1c).
As expected, the simulated ecosystem-evolutionary change in SOC equilibrium in response to warming (Figs. 2, 3) mirrors the evolutionary adaptive response of the exoenzyme allocation fraction to warming in all scenarios of temperature dependence (Supplementary Figs. 5a-d). In the baseline scenario, microbes always evolve a higher enzyme allocation fraction in response to rising temperature; as a consequence, evolutionary adaptation amplifies the non-evolutionary soil carbon loss due to warming (Fig. 3a). The effect of evolution is strongest in ecosystems characterized by conditions that are hostile to microbial growth (low initial temperature, T 0; high mortality, \(d_{M}\); low MGE, \(\gamma_{M}\); low maximum uptake rate,\(v_{0}^{U}\)) (Fig. 2, Fig. 3a, Supplementary Fig. 6), where the adaptive response of the exoenzyme allocation fraction is most pronounced (Supplementary Fig. 5a). Strong evolutionary effects are robust to the other model parameters – enzyme parameters (efficiency, production) and environmental parameters (litter input, leaching) (Supplementary Figs. 6 and 7, Supplementary Note 5), which have no influence on the relationship between φ * and temperature (equation (8)). The model also predicts stronger evolutionary effects when the differential access to resources between microbial strains is small (low c 0) (equation (8), Fig. 2c, d). Small competition asymmetry selects for microbes allocating little to exoenzymes (low φ *); due to the non-linear response of SOC equilibrium to φ , this causes the SOC equilibrium to be more sensitive to variation in the exoenzyme allocation fraction (Supplementary Note 1, Supplementary Fig. 3).
In the temperature-dependent mortality scenario, the strength of the effect of temperature on mortality is an important determinant of the evolutionary adaptive response to warming. When mortality is moderately sensitive to temperature, the positive response of φ * to warming is attenuated. As a result, the evolutionary aggravation of soil carbon loss is less severe (Fig. 3b). When mortality is strongly sensitive to temperature, warming creates more hostile conditions for microbial growth, therefore φ * decreases with warming. Evolutionary adaptation then buffers the loss of soil carbon (negative EVO effect, Fig. 3c).
In the temperature-dependent MGE scenario, the direction (positive or negative) of the response of φ * to warming is determined by the initial temperature T 0. The evolutionary effect parallels the response of φ *. At low T 0,φ * increases strongly with temperature, causing an aggravation of soil carbon loss (positive evolutionary effect). In contrast, at highT 0, φ * decreases strongly with warming, thus opposing the non-evolutionary response (negative evolutionary effect) and promoting carbon sequestration instead (Fig. 3d). At intermediate T 0, φ * is weakly sensitive to temperature, and the effect of evolutionary adaptation to warming is negligible.