The evolutionary ecology of C4 plants

C4 photosynthesis is a physiological syndrome resulting from multiple anatomical and biochemical components, which function together to increase the CO2 concentration around Rubisco and reduce photorespiration. It evolved independently multiple times and C4 plants now dominate many biomes, especially in the tropics and subtropics. The C4 syndrome comes in many flavours, with numerous phenotypic realizations of C4 physiology and diverse ecological strategies. In this work, we analyse the events that happened in a C3 context and enabled C4 physiology in the descendants, those that generated the C4 physiology, and those that happened in a C4 background and opened novel ecological niches. Throughout the manuscript, we evaluate the biochemical and physiological evidence in a phylogenetic context, which demonstrates the importance of contingency in evolutionary trajectories and shows how these constrained the realized phenotype. We then discuss the physiological innovations that allowed C4 plants to escape these constraints for two important dimensions of the ecological niche--growth rates and distribution along climatic gradients. This review shows that a comprehensive understanding of C4 plant ecology can be achieved by accounting for evolutionary processes spread over millions of years, including the ancestral condition, functional convergence via independent evolutionary trajectories, and physiological diversification.