Ecological selection pressures for C(4) 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.