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

Abstract

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.

Gomphrena (Amaranthaceae, Gomphrenoideae) diversified as a C4 lineage in the New World tropics with specializations in floral and inflorescence morphology, and an escape to Australia

“…(2007) only included five Gomphrena species to map the evolution of C 4 photosynthesis on the tree of Amaranthaceae and revealed a common origin of C 4 in species of Gomphrena belonging to "clade a" alongside with Philoxerus, Guilleminea and Froelichia. This result was confirmed by Bena & al. (2017) who tested if the evolution of the C 4 pathway correlated with changes in macroclimatic niches and found that C 4 Gomphrenoideae specialized to dryer regions compared to their C 3 relatives and then expanded into colder environments.…”

“…(2009), Sage & al. (2007) and Bena & al. (2017) show that the gomphrenoid clade contains species of Gomphrena in two different lineages: The first lineage comprises Lithophila, Gossypianthus and Philoxerus (= Blutaparon) along with most species of Gomphrena (= Gomphrena s.str.…”

“…6, Appendix S9), the section Chnoanthus appears as a natural group. Recently, Bena & al. (2017) generated trnL-F sequences of an individual of each G. umbellata, G. radiata, G. cladotrichoides and G. mendocina, the latter two of which are close relatives of G. tomentosa.…”

“…They found three lineages in a polytomy, among which one depicted Gossypianthus sister to Gomphrena boliviana, another Gomphrena flac cida sister to Blutaparon+Lithophila, and the third the remaining species of Gomphrena. Recently, Bena & al. (2017) added trnL-F sequences of a dozen further species from Argentina, but their trees remained statistically unsupported.…”

C4 photosynthesis evolved in warm climates but promoted migration to cooler ones

“…; Bena et al . ). However, our analysis is the first to show that C 4 photosynthesis also increased the rate of transitions among climate types, with frequent migration into temperate climates without freezing (Fig.…”