Adaptation to elevated CO2 in different biodiversity contexts

Introduction

Species do not evolve in isolation but within a community of interacting species. While some evidence exists for the impact of predator–prey1,2,3or host–parasite interactions4 on adaptive evolution, we lack experimental data on the impact of competition on adaptation in natural systems. Laboratory and mesocosm studies have found contrasting results for how competition influences adaptation. Competition can inhibit adaptation, as found in algal cultures (Chlamydomonas reinhardtii) evolving to elevated CO2 (ref. 5). Similarly, adaptive diversification to habitat heterogeneity in Pseudomonas flourescens was prevented in the presence of interspecific competitors, as these competitors exclude intraspecific variants6. Competition can also alter the nature of selection2,7,8. For instance, increased water temperature caused the zooplankton Daphnia magna and D. pulex to evolve faster growth in the absence of competition but to evolve a larger size at maturity in the presence of competitors and predators2. Similarly, bacterial species adapted differently to a novel environment when grown alone or with other bacteria species7. In plants, the presence, composition, and diversity of competing species shows tremendous spatial variation9, can have a major impact on individual performance10,11, and thus might have an important influence on species’ adaptation to environmental change. Yet, how biotic community context alters how species adapt to environmental change in natural field settings remains entirely unknown.

To address this knowledge gap, herein we report on an investigation of the impact of prairie grassland communities on the evolutionary response to elevated CO2 over 14 years in the Biodiversity Carbon dioxide and Nitrogen experiment (BioCON) at the Cedar Creek Ecosystem Sciences Reserve (Minnesota, USA)12. To determine how the surrounding biological community influences a species’ ability to evolve in response to abiotic change, we focused on very different community structures: monoculture versus high diversity. By focusing on the presence or absence of interspecific competitors, we increased our power to detect the impacts of the surrounding species diversity on evolution. We tested four possible scenarios by which species diversity might affect the evolutionary responses of a focal species to abiotic environmental change.

The first scenario is that species diversity has no effect on adaptation to abiotic environmental change (Fig. 1a,b). If selective pressures exerted by changing abiotic conditions overwhelm those from the biotic community, species diversity should have no impact on local adaptation to abiotic change. Statistically, the response to selection (fitness of plants evolved under elevated CO2 (eCO2) minus fitness of plants evolved under ambient CO2 (aCO2)) should be predicted only by the change in CO2 environment (ΔCO2), regardless of species diversity (Fig. 1a,b).

Figure 1: The hypothetical influence of species richness on adaptation of plants to elevated CO2.

The response of a focal species to selection in a given context can be quantified as the difference in performance (for example, biomass or fitness) between plants originating from elevated CO2 (eCO2) plots and those from ambient CO2 (aCO2) plots (y axis). (a,b) If species diversity has no effect on adaptation, local adaptation to eCO2 should be similar in species-poor and species-rich communities regardless of the species richness of the assay environment. (c,d) If species diversity constrains adaptation, an evolutionary response to eCO2 should be more evident for plants that experienced selection in a species-poor community than in a species-rich community, regardless of the species richness of the assay environment. (e,f) If species diversity promotes adaptation to eCO2, then plants that experienced selection within a species-rich community may show greater fitness in eCO2regardless of assay species richness. (g,h) If species diversity alters the fitness landscape in response to CO2, then plants may only show improved fitness in eCO2 when planted back into a community of similar richness to the one in which they experienced selection. Each scenario can be represented by a particular statistical term, shown on the right.