Abstract
CO(2), temperature, water availability, and light intensity were all potential selective pressures that determined the competitive advantage and expansion of the C(4) photosynthetic carbon-concentrating mechanism over the last ∼30 My. To tease apart how selective pressures varied along the ecological trajectory of C(4) expansion and dominance, we coupled hydraulics to photosynthesis models while optimizing photosynthesis over stomatal resistance and leaf/fine-root allocation. We further examined the importance of nitrogen reallocation from the dark to the light reactions. We show here that the primary selective pressures favoring C(4) dominance changed through the course of C(4) evolution. The higher stomatal resistance and leaf-to-root ratios enabled by C(4) led to an advantage without any initial difference in hydraulic properties. We further predict a reorganization of the hydraulic system leading to higher turgor-loss points and possibly lower hydraulic conductance. Selection on nitrogen reallocation varied with CO(2) concentration. Through paleoclimate model simulations, we find that water limitation was the primary driver for a C(4) advantage, with atmospheric CO(2) as high as 600 ppm, thus confirming molecular-based estimates for C(4) evolution in the Oligocene. Under these high-CO(2) conditions, nitrogen reallocation was necessary. Low CO(2) and high light, but not nitrogen reallocation, were the primary drivers for the mid- to late-Miocene global expansion of C(4) We also predicted the timing and spatial distribution for origins of C(4) ecological dominance. The predicted origins are broadly consistent with prior estimates, but expand upon them to include a center of origin in northwest Africa and a Miocene-long origin in Australia.