title: Introgression and repeated co-option facilitated the recurrent emergence of C4photosynthesis among close relatives.
abstract: 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 C4photosynthesis, an adaptation to warm and dry conditions, in the grass Alloteropsis. We dissect the C4trait into its components, and show two independent origins of the C4phenotype 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 C4state from a common ancestor with an intermediate phenotype that had some C4anatomical and biochemical components. Molecular dating of C4genes confirms the introgression of two key C4components between species, while the inheritance of all others matches the species tree. The number of origins consequently varies among C4components, 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.
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, United Kingdom.
authors.forename: Luke T
authors.initials: LT
authors.lastname: Dunning
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, United Kingdom.
authors.forename: Marjorie R
authors.initials: MR
authors.lastname: Lundgren
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, United Kingdom.
authors.forename: Jose J
authors.initials: JJ
authors.lastname: Moreno-Villena
authors.affiliation: Makerere University, Kampala, Uganda.
authors.forename: Mary
authors.initials: M
authors.lastname: Namaganda
authors.affiliation: Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island, 02912.
authors.forename: Erika J
authors.initials: EJ
authors.lastname: Edwards
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, United Kingdom.
authors.forename: Patrik
authors.initials: P
authors.lastname: Nosil
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, United Kingdom.
authors.forename: Colin P
authors.initials: CP
authors.lastname: Osborne
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, United Kingdom.
authors.forename: Pascal-Antoine
authors.initials: PA
authors.lastname: Christin
mesh_terms: D000222:Adaptation, Physiological; D005075:Biological Evolution; D010641:Phenotype; D010788:Photosynthesis; D010802:Phylogeny; D006109:Poaceae / Q000235:genetics / Q000502:physiology
keywords: Ancestral state; co-option; complex trait; reticulate evolution; species tree