C4 photosynthesis and climate through the lens of optimality

Abstract

CO2, temperature, water availability, and light intensity were all potential selective pressures that determined the competitive advantage and expansion of the C4 photosynthetic carbon-concentrating mechanism over the last ∼30 My. To tease apart how selective pressures varied along the ecological trajectory of C4 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 C4 dominance changed through the course of C4 evolution. The higher stomatal resistance and leaf-to-root ratios enabled by C4 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 CO2 concentration. Through paleoclimate model simulations, we find that water limitation was the primary driver for a C4 advantage, with atmospheric CO2 as high as 600 ppm, thus confirming molecular-based estimates for C4 evolution in the Oligocene. Under these high-CO2 conditions, nitrogen reallocation was necessary. Low CO2 and high light, but not nitrogen reallocation, were the primary drivers for the mid- to late-Miocene global expansion of C4. We also predicted the timing and spatial distribution for origins of C4 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.