Phenotypic landscape inference reveals multiple evolutionary paths to C₄ photosynthesis

Original · EN

C₄ photosynthesis has independently evolved from the ancestral C₃ pathway in at least 60 plant lineages, but, as with other complex traits, how it evolved is unclear. Here we show that the polyphyletic appearance of C₄ photosynthesis is associated with diverse and flexible evolutionary paths that group into four major trajectories. We conducted a meta-analysis of 18 lineages containing species that use C₃, C₄, or intermediate C₃-C₄ forms of photosynthesis to parameterise a 16-dimensional phenotypic landscape. We then developed and experimentally verified a novel Bayesian approach based on a hidden Markov model that predicts how the C₄ phenotype evolved. The alternative evolutionary histories underlying the appearance of C₄ photosynthesis were determined by ancestral lineage and initial phenotypic alterations unrelated to photosynthesis. We conclude that the order of C₄ trait acquisition is flexible and driven by non-photosynthetic drivers. This flexibility will have facilitated the convergent evolution of this complex trait.