Introgression and repeated co-option facilitated the recurrent emergence of C₄ photosynthesis among close relatives

• Published in: Evolution 2017-06, Vol.71 (6), p.1541-1555
• Main Authors: Dunning, Luke T., Lundgren, Marjorie R., Moreno-Villena, Jose J., Namaganda, Mary, Edwards, Erika J., Nosil, Patrik, Osborne, Colin P., Christin, Pascal-Antoine
• Format: Article
• Language: English
• Subjects: Adaptation; Ancestral state; Biochemistry; Chronology; complex trait; co‐option; Dating; Drying; Emergence; Genes; Grasses; Heredity; Inference; Modelling; Original; ORIGINAL ARTICLE; Origins; Photosynthesis; reticulate evolution; species tree; Trajectories; Transcription; Trees
• ISSN: 0014-3820; 1558-5646
• DOI: 10.1111/evo.13250

The origins of novel traits are often studied using species trees and modeling phenotypes as different states of the same character, an approach that cannot always distinguish multiple origins from fewer origins followed by reversals. We address this issue by studying the origins of C₄ photosynthesis, an adaptation to warm and dry conditions, in the grass Alloteropsis. We dissect the C₄ trait into its components, and show two independent origins of the C₄ phenotype via different anatomical modifications, and the use of distinct sets of genes. Further, inference of enzyme adaptation suggests that one of the two groups encompasses two transitions to a full C₄ state from a common ancestor with an intermediate phenotype that had some C₄ anatomical and biochemical components. Molecular dating of C₄ genes confirms the introgression of two key C₄ components between species, while the inheritance of all others matches the species tree. The number of origins consequently varies among C₄ components, a scenario that could not have been inferred from analyses of the species tree alone. Our results highlight the power of studying individual components of complex traits to reconstruct trajectories toward novel adaptations.