Phylogenetic analyses reveal the shady history of C4 grasses

Abstract

Grasslands cover more than 20% of the Earth's terrestrial surface, and their rise to dominance is one of the most dramatic events of biome evolution in Earth history. Grasses possess two main photosynthetic pathways: the C(3) pathway that is typical of most plants and a specialized C(4) pathway that minimizes photorespiration and thus increases photosynthetic performance in high-temperature and/or low-CO(2) environments. C(4) grasses dominate tropical and subtropical grasslands and savannas, and C(3) grasses dominate the world's cooler temperate grassland regions. This striking pattern has been attributed to C(4) physiology, with the implication that the evolution of the pathway enabled C(4) grasses to persist in warmer climates than their C(3) relatives. We combined geospatial and molecular sequence data from two public archives to produce a 1,230-taxon phylogeny of the grasses with accompanying climate data for all species, extracted from more than 1.1 million herbarium specimens. Here we show that grasses are ancestrally a warm-adapted clade and that C(4) evolution was not correlated with shifts between temperate and tropical biomes. Instead, 18 of 20 inferred C(4) origins were correlated with marked reductions in mean annual precipitation. These changes are consistent with a shift out of tropical forest environments and into tropical woodland/savanna systems. We conclude that C(4) evolution in grasses coincided largely with migration out of the understory and into open-canopy environments. Furthermore, we argue that the evolution of cold tolerance in certain C(3) lineages is an overlooked innovation that has profoundly influenced the patterning of grassland communities across the globe.

Fig. 1.

Species accumulation curves for mean annual temperature and precipitation, sorted by major grass lineage. These data represent 1,584,351 independent collection localities spread across 10,469 taxa. Each point in the curve is a species’ mean value.

Fig. 2.

The evolution of photosynthetic pathway and temperature niche in grasses. (A) Green lines indicate C₃ photosynthesis; black lines indicate C₄ photosynthesis. Maximum likelihood methods reconstructed 20 origins of C₄ photosynthesis and one reversal to C₃ photosynthesis. (B) Maximum likelihood reconstructions of mean annual temperature (MAT), using species’ mean values that were generated from 1,146,612 geo-referenced herbarium specimens.

Fig. 3.

Maximum likelihood reconstructions of ancestral C₃ and C₄ precipitation niches for 21 C₃/C₄ evolutionary divergences. White dots indicate C₃ value; black dots indicate C₄ value. Background shading indicates gross climate delineations between a closed-canopy tropical forest (white) and open woodland/savanna system (gray); transition occurs around MAP ˜1500 mm year⁻¹, coefficient of variation of precipitation ˜0.75. Gray bars highlight C₃/C₄ transitions that are consistent with a movement of the C₄ lineage from tropical forest into open woodland/savanna.