Macroclimatic niche limits and the evolution of C4 photosynthesis in Gomphrenoideae (Amaranthaceae)

During the evolution of vascular plants, C-4 photosynthesis has developed > 60 times, but most studies concerning the evolution and the ecophysiological advantages of the C-4 syndrome have been carried out in grasses. Among eudicots, C-4 photosynthesis has developed in lineages that are morphologically more diverse than the relatively homogeneous grasses, and conclusions about C-4 evolution based on grasses may or may not apply to eudicots. Little is known about the origin of C-4 photosynthesis in Amaranthaceae s.s., one of the most C-4 species-rich lineages of eudicots. Among subfamily Gomphrenoideae, C-3 and C-4 species are found in arid regions, but high Andean species display the C-4 pathway. In this study, we aimed to compare the climatic extremes between C-3 and C-4 species in Gomphrenoideae. In particular, we evaluated the upper and lower extremes of three climatic variables among closely related C-3 and C-4 lineages, using phylogenetic generalized least squares (PGLS), applied on four topologies: maximum parsimony, Bayesian and maximum likelihood (ML) topologies including species with available DNA sequences and a ML topology that included unsequenced species with available climate data. We tested whether the evolution of C-4 photosynthesis correlates with a niche specialization where both the upper and the lower extremes change position or a niche expansion where only a single extreme changes position. PGLS results showed that C-4 species of Gomphrenoideae have specialized to dryer regions and expanded into colder ones than their C-3 relatives. However, the niche expansion into colder climates only includes areas with low temperatures during winter, not during the growing period. Finally, we found no evidence for a niche change into warmer climates. Therefore, the model for the evolution of C-4 photosynthesis in Gomphrenoideae may differ from the one supported in Chenopodioideae and seems to be more similar to that found in grasses, where the C-4 pathway appears to have evolved in humid habitats, but facilitated an expansion into arid ones. However, we found no support for the common expectation that C-4 species reach warmer climates than their C-3 relatives, contrasting with previous results on grasses.