Ecological selection pressures for C4 photosynthesis in the grasses

Abstract

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.

Figure 1

Species number and habitat water requirements in extant C₃ and C₄ genera. The plots show mean ±95% C.I. for (a) species number, (b) range of water requirements tolerated and (c) mean water requirements for each photosynthetic type.

Figure 2

Models of the coevolution of photosynthetic pathway and habitat preference. Reversals from C₄ to C₃ photosynthesis are allowed in models (a,b), but prohibited in (c,d). Models (a,c) show preference for habitat openness, and (b,d) tolerance of habitat aridity. Grey-shaded boxes indicate the most likely ancestral condition, and arrow size is proportional to the rate/likelihood of transitions between character states.

Figure 3

Likelihood of alternative ancestral states for nodes in the phylogenetic tree, showing (a) photosynthetic pathway (yellow circles, C₄; blue circles, C₃) and (b) preference for habitat openness (yellow circles, shade; blue circles, open habitat). See figure S1 in the electronic supplementary material for key to genera. Ancestral values were computed for individual traits using the likelihood method of Pagel (1994) and phylogenies drawn using the ace and plot.phylo functions in APE (Paradis et al. 2004).

Figure 4

Likelihood of alternative ancestral states for nodes in the phylogenetic tree, showing (a) photosynthetic pathway (yellow circles, C₄; blue circles, C₃) and (b) preference for habitat aridity (yellow circles, xeric; blue circles, mesic). See figure S1 in the electronic supplementary material for key to genera. Ancestral values were computed for individual traits using the likelihood method of Pagel (1994) and phylogenies drawn using the ace and plot.phylo functions in APE (Paradis et al. 2004).