Ecological selection pressures for C4 photosynthesis in the grasses

Grasses using the C-4 photosynthetic pathway dominate grasslands and savannahs of warm regions, and account for half of the species in this ecologically and economically important plant family. The C-4 pathway increases the potential for high rates of photosynthesis, particularly at high irradiance, and raises water-use efficiency compared with the C-3 type. It is therefore classically viewed as an adaptation to open, arid conditions. Here, we test this adaptive hypothesis using the comparative method, analysing habitat data for 117 genera of grasses, representing 15 C-4 lineages. The evidence from our three complementary analyses is consistent with the hypothesis that evolutionary selection for C-4 photosynthesis requires open environments, but we find an equal likelihood of C-4 evolutionary origins in mesic, arid and saline habitats. However, once the pathway has arisen, evolutionary transitions into arid habitats occur at higher rates in C-4 than C-3 clades. Extant C-4 genera therefore occupy a wider range of drier habitats than their C-3 counterparts because the C-4 pathway represents a pre-adaptation to arid conditions. Our analyses warn against evolutionary inferences based solely upon the high occurrence of extant C-4 species in dry habitats, and provide a novel interpretation of this classic ecological association.