Divergent evolutionary histories of C4 grasses shape global grassland ecology

Abstract:

C₄ photosynthesis has evolved in more than 23 independent lineages of grasses as an adaptation to hot, sunny conditions. Geological records demonstrate that C₄ grasses abruptly became ecologically dominant during the late Cenozoic across the tropical and temperate regions, transforming the Earth System and facilitating major faunal and floral radiations. However, although each C₄ grass lineage originated and specialised in different environments, the importance of these divergent evolutionary histories for global ecology remains largely unknown. Here, we address this problem by compiling the first global map of grassy biomes based entirely upon ground-based vegetation surveys of dominant species. Our analysis shows that grasses dominate the ground layer across 40% of the vegetated land surface, with C₄ grasses accounting for 60% of this area, and grassy biomes occurring under almost all climatic conditions. More than 98% of C₃ grassy vegetation is dominated by the cold tolerant Pooideae lineage, which is replaced by C₄ lineages at mean annual temperatures exceeding 15^oC. The world’s C₄ grassy vegetation is largely dominated by only four of the 23 independent C₄ grass lineages, and these segregate strongly along global environmental gradients and across continents. The Chloridoideae lineage is globally important in dominating semi-arid environments with a long fire return interval. In contrast, although the Andropogoneae lineage dominates extremely wet regions with frequent fire in the Paleotropics and North America, the same niche space is dominated by Paspaleae in South America. Sorting of lineages along precipitation and fire gradients is strongly predicted by plant height. Our results demonstrate that the divergent histories of independent C₄ grass lineages have constrained the assembly and functional traits of grassy biomes, with important implications for understanding how biome boundaries may shift in past and future environments.