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Summary: C4 photosynthesis is a complex trait requiring multiple developmental and metabolic alterations. Despite this complexity, it has independently evolved over 60 times. However, our understanding of the transition to C4 is complicated by the fact that variation in photosynthetic type is usually segregated between species that diverged a long time ago.Here, we perform a genome‐wide association study (GWAS) using the grass Alloteropsis semialata, the only known species to have C3, intermediate, and C4 accessions that recently diverged. We aimed to identify genomic regions associated with the strength of the C4 cycle (measured using δ13C), and the development of C4 leaf anatomy.Genomic regions correlated with δ13C include regulators of C4 decarboxylation enzymes (RIPK), nonphotochemical quenching (SOQ1), and the development of Kranz anatomy (SCARECROW‐LIKE). Regions associated with the development of C4 leaf anatomy in the intermediate individuals contain additional leaf anatomy regulators, including those responsible for vein patterning (GSL8) and meristem determinacy (GIF1).The parallel recruitment of paralogous leaf anatomy regulators between A. semialata and other C4 lineages implies the co‐option of these genes is context‐dependent, which likely has implications for the engineering of the C4 trait into C3 species. [ABSTRACT FROM AUTHOR]

Summary: C4 photosynthesis is a key innovation in land plant evolution, but its immediate effects on population demography are unclear. We explore the early impact of the C4 trait on the trajectories of C4 and non‐C4 populations of the grass Alloteropsis semialata.We combine niche models projected into paleoclimate layers for the last 5 million years with demographic models based on genomic data.The initial split between C4 and non‐C4 populations was followed by a larger expansion of the ancestral C4 population, and further diversification led to the unparalleled expansion of descendant C4 populations. Overall, C4 populations spread over three continents and achieved the highest population growth, in agreement with a broader climatic niche that rendered a large potential range over time. The C4 populations that remained in the region of origin, however, experienced lower population growth, rather consistent with local geographic constraints. Moreover, the posterior transfer of some C4‐related characters to non‐C4 counterparts might have facilitated the recent expansion of non‐C4 populations in the region of origin.Altogether, our findings support that C4 photosynthesis provided an immediate demographic advantage to A. semialata populations, but its effect might be masked by geographic contingencies. [ABSTRACT FROM AUTHOR]