Evolutionary trajectories, accessibility and other metaphors: the case of C₄ and CAM photosynthesis

Are evolutionary outcomes predictable? Adaptations that show repeated evolutionary convergence across the Tree of Life provide a special opportunity to dissect the context surrounding their origins, and identify any commonalities that may predict why certain traits evolved many times in particular clades and yet never evolved in others. The remarkable convergence of C₄ and Crassulacean Acid Metabolism (CAM) photosynthesis in vascular plants makes them exceptional model systems for understanding the repeated evolution of complex phenotypes. This review highlights what we have learned about the recurring assembly of C₄ and CAM, focusing on the increasingly predictable stepwise evolutionary integration of anatomy and biochemistry. With the caveat that we currently understand C₄ evolution better than we do CAM, I propose a general model that explains and unites C₄ and CAM evolutionary trajectories. Available data suggest that anatomical modifications are the 'rate-limiting step' in each trajectory, which in large part determines the evolutionary accessibility of both syndromes. The idea that organismal structure exerts a primary influence on innovation is discussed in the context of other systems. Whether the rate-limiting step occurs early or late in the evolutionary assembly of a new phenotype may have profound implications for its distribution across the Tree of Life.