Grasses are ancestrally tropical understory species whose current dominance in warm open habitats is linked to the evolution of C4 photosynthesis. C4 grasses maintain high rates of photosynthesis in warm and water stressed environments, and the syndrome is considered to induce niche shifts into these habitats while adaptation to cold ones may be compromised. Global biogeographic analyses of C4 grasses have, however, concentrated on diversity patterns, while paying little attention to distributional limits. Using phylogenetic contrast analyses, we compared macro-climatic distribution limits among ~1300 grasses from the subfamily Panicoideae, which includes 4/5 of the known photosynthetic transitions in grasses. We explored whether evolution of C4 photosynthesis correlates with niche expansions, niche changes, or stasis at subfamily level and within the two tribes Paniceae and Paspaleae. We compared the climatic extremes of growing season temperatures, aridity, and mean temperatures of the coldest months. We found support for all the known biogeographic distribution patterns of C4 species, these patterns were, however, formed both by niche expansion and niche changes. The only ubiquitous response to a change in the photosynthetic pathway within Panicoideae was a niche expansion of the C4 species into regions with higher growing season temperatures, but without a withdrawal from the inherited climate niche. Other patterns varied among the tribes, as macro-climatic niche evolution in the American tribe Paspaleae differed from the pattern supported in the globally distributed tribe Paniceae and at family level.
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.
Abstract—Gomphrena meyeniana is an extremely variable species from the Andean highlands, which has attracted the attention of many botanists because it is the world’s highest-elevation C4 eudicot and because of its wide morphological variability. It has the typical high-Andean plant morphology, with small leaves tightly clustered on a thick rootstock. The large range of morphological variation within this species coupled with the varying opinions on the existence of several species or infra-specific taxa and the lack of molecular information has made the clarification of the G. meyeniana complex a challenge. Our approach was to perform broad molecular sampling to identify the phylogenetic position of G. meyeniana within Gomphrena and to perform a multivariate analysis to objectively differentiate taxa based on morphological characters. The ITS and trnL-F regions were analyzed individually and in combination using Bayesian inference and maximum parsimony methods. To analyze the morphological characters we performed a clustering method (partitioning around medoids with the Gower’s dissimilarity algorithm). The molecular analyses supported the monophyly of the G. meyeniana complex, but did not support segregation into varieties. The morphological analyses supported recognition of three varieties that can be easily distinguished by three simple characters: the presence of leaves on the flowering shoot, the habit of the flowering shoot, and the pilosity of the sepals. The varieties of G. meyeniana accepted here are G. meyeniana var. meyeniana, G. meyeniana var. caulescens, and G. meyeniana var. flaccida. A dichotomous key to identify the infra-specific taxa is here presented and illustrated. Gomphrena meyeniana var. tucumanensis and G. meyeniana var. conwayi are synonymized with G. meyeniana var. caulescens and G. meyeniana var. meyeniana, respectively.
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