Photosynthetic innovation broadens the niche within a single species

Abstract

Adaptation to changing environments often requires novel traits, but how such traits directly affect the ecological niche remains poorly understood. Multiple plant lineages have evolved C4 photosynthesis, a combination of anatomical and biochemical novelties predicted to increase productivity in warm and arid conditions. Here, we infer the dispersal history across geographical and environmental space in the only known species with both C4 and non-C4 genotypes, the grass Alloteropsis semialata. While non-C4 individuals remained confined to a limited geographic area and restricted ecological conditions, C4 individuals dispersed across three continents and into an expanded range of environments, encompassing the ancestral one. This first intraspecific investigation of C4 evolutionary ecology shows that, in otherwise similar plants, C4 photosynthesis does not shift the ecological niche, but broadens it, allowing dispersal into diverse conditions and over long distances. Over macroevolutionary timescales, this immediate effect can be blurred by subsequent specialisation towards more extreme niches.

Introgression and repeated co-option facilitated the recurrent emergence of C4photosynthesis among close relatives

“…Other populations, potentially under pressures linked to the colonization of colder environments (Lundgren et al. 2015), might have lost the weak C 4 cycle by downregulating the genes (Fig. 2).…”

“…The over representation of C 4 A. semialata accessions mirrors their natural abundance, with C 4 accessions spread throughout Africa, Asia, and Australia, C 3 accessions only reported in Southern Africa, and C 3 +C 4 individuals restricted to central East Africa (Lundgren et al. 2015). We also make use of species representing the C 3 sister group to Alloteropsis ( Panicum pygmaeum and Entolasia marginata ), previously identified using plastid markers (GPWGII 2012).…”

“…In addition, plastid genomes for the same species were retrieved from Lundgren et al. (2015), and reanalyzed with the same parameters. For each of these datasets, the median, 95% CI, and 0.25 and 0.75 quantiles were extracted from the posterior distribution, using the R package APE (Paradis et al.…”

Genome biogeography reveals the intraspecific spread of adaptive mutations for a complex trait

“…The photosynthetic type of these samples has been determined previously, and they encompass non‐C 4 individuals with and without a weak C 4 cycle, as well as multiple C 4 accessions (Table S1, Supporting information; Lundgren et al . , ). An additional eight Alloteropsis accessions were sampled here to increase the resolution of genome biogeography for the group (Table S1, Supporting information).…”

Grass diversification in Madagascar: In situ radiation of two large C3 shade clades and support for a Miocene to Pliocene origin of C4 grassy biomes

“…The cosmopolitan distribution of grasses must therefore be the result of recurrent dispersal between continents. Bio‐ and phylogeographic work has shown that the availability of suitable climatic conditions played a major role in allowing grasses to successfully colonize new continents (Linder, Antonelli, Humphreys, Pirie, & Wüest, ; Lundgren et al., ; Visser, Clayton, Simpson, Freckleton, & Osborne, ). The multiple evolution of C 4 photosynthesis in grasses, first occurring in the Oligocene (Christin et al., ; Vicentini, Barber, Aliscioni, Giussani, & Kellogg, ), and the expansion of grasslands in the Miocene were major drivers of grass diversification (Spriggs, Christin, & Edwards, ).…”