A Novel Hypothesis for the Role of Photosynthetic Physiology in Shaping Macroevolutionary Patterns

The fossil record and models of atmospheric concentrations of O-2 and CO2 suggest that past shifts in plant ecological dominance often coincided with dramatic changes in Earth's atmospheric composition. This study tested the effects of past changes in atmospheric composition on the photosynthetic physiology of a limited range of early-diverging angiosperms (eight), gymnosperms (three), and ferns (two). We performed physiological measurements on all species and used the results to parameterize simulations of their photosynthetic paleophysiology using three independent modeling approaches. Unique physiological attributes were identified for the three evolutionary groups: angiosperm taxa displayed significantly higher mesophyll conductance (g(m)), yet their stomatal conductance (g(s)) was lower than that of ferns. Gymnosperm taxa displayed low g(s) and g(m), but they partially offset their significant diffusional limitations on photosynthesis through their higher maximum Rubisco carboxylation rate. Despite their high total conductance to CO2, fern taxa lacked an optimized control of g(s), which was reflected in their low intrinsic water use efficiency. Simulations of the photosynthetic physiology of ferns, angiosperms, and gymnosperms through Earth's history demonstrated that past fluctuations in O-2 and CO2 concentrations may have resulted in significant shifts in the relative competitiveness of the three evolutionary groups. Although preliminary because of limited species sampling, these findings hint at a potential mechanistic basis for the observed broad temporal correlation between atmospheric change and shifts in plant evolutionary group-level richness observed in the fossil record and are presented as a framework to be tested with paleophotosynthetic proxies and through increased species sampling.