Phenotypic landscape inference reveals multiple evolutionary paths to C${}_4$ photosynthesis

Abstract

C${}_4$ photosynthesis has independently evolved from the ancestral C${}_3$ 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 C${}_4$ 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 C${}_3$, C${}_4$, or intermediate C${}_3$-C${}_4$ 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 C${}_4$ phenotype evolved. The alternative evolutionary histories underlying the appearance of C${}_4$ photosynthesis were determined by ancestral lineage and initial phenotypic alterations unrelated to photosynthesis. We conclude that the order of C${}_4$ trait acquisition is flexible and driven by non-photosynthetic drivers. This flexibility will have facilitated the convergent evolution of this complex trait.

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