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

TL;DR

This study uncovers multiple evolutionary routes to C$_4$ photosynthesis, demonstrating that its development is flexible and driven by non-photosynthetic factors, which explains its convergent evolution across diverse plant lineages.

Contribution

The paper introduces a novel Bayesian hidden Markov model approach to infer the phenotypic landscape and evolutionary trajectories leading to C$_4$ photosynthesis.

Findings

C$_4$ photosynthesis evolved via four major trajectories.

Evolutionary paths are influenced by ancestral lineage and initial phenotypic changes.

The order of trait acquisition in C$_4$ evolution is highly flexible.

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.