The evolutionary ecology of C4 plants

C-4 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 C-4 plants now dominate many biomes, especially in the tropics and subtropics. The C-4 syndrome comes in many flavours, with numerous phenotypic realizations of C-4 physiology and diverse ecological strategies. In this work, we analyse the events that happened in a C-3 context and enabled C-4 physiology in the descendants, those that generated the C-4 physiology, and those that happened in a C-4 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 C-4 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 C-4 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.