title: Genome biogeography reveals the intraspecific spread of adaptive mutations for a complex trait.
abstract: Physiological novelties are often studied at macro-evolutionary scales such that their micro-evolutionary origins remain poorly understood. Here, we test the hypothesis that key components of a complex trait can evolve in isolation and later be combined by gene flow. We use C4photosynthesis as a study system, a derived physiology that increases plant productivity in warm, dry conditions. The grass Alloteropsis semialata includes C4and non-C4genotypes, with some populations using laterally acquired C4-adaptive loci, providing an outstanding system to track the spread of novel adaptive mutations. Using genome data from C4and non-C4A. semialata individuals spanning the species' range, we infer and date past migrations of different parts of the genome. Our results show that photosynthetic types initially diverged in isolated populations, where key C4components were acquired. However, rare but recurrent subsequent gene flow allowed the spread of adaptive loci across genetic pools. Indeed, laterally acquired genes for key C4functions were rapidly passed between populations with otherwise distinct genomic backgrounds. Thus, our intraspecific study of C4-related genomic variation indicates that components of adaptive traits can evolve separately and later be combined through secondary gene flow, leading to the assembly and optimization of evolutionary innovations.
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
authors.forename: Jill K
authors.initials: JK
authors.lastname: Olofsson
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
authors.forename: Matheus
authors.initials: M
authors.lastname: Bianconi
authors.affiliation: Laboratoire Évolution & Diversité Biologique (EDB UMR5174), Université de Toulouse, CNRS, ENSFEA, UPS, 118 route de Narbonne, F-31062, Toulouse, France.
authors.forename: Guillaume
authors.initials: G
authors.lastname: Besnard
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
authors.forename: Luke T
authors.initials: LT
authors.lastname: Dunning
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
authors.forename: Marjorie R
authors.initials: MR
authors.lastname: Lundgren
authors.affiliation: Laboratoire Évolution & Diversité Biologique (EDB UMR5174), Université de Toulouse, CNRS, ENSFEA, UPS, 118 route de Narbonne, F-31062, Toulouse, France.
authors.forename: Helene
authors.initials: H
authors.lastname: Holota
authors.affiliation: Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK.
authors.forename: Maria S
authors.initials: MS
authors.lastname: Vorontsova
authors.affiliation: Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK.
authors.forename: Oriane
authors.initials: O
authors.lastname: Hidalgo
authors.affiliation: Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK.
authors.forename: Ilia J
authors.initials: IJ
authors.lastname: Leitch
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
authors.forename: Patrik
authors.initials: P
authors.lastname: Nosil
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
authors.forename: Colin P
authors.initials: CP
authors.lastname: Osborne
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
authors.forename: Pascal-Antoine
authors.initials: PA
authors.lastname: Christin
mesh_terms: D000220:Adaptation, Biological / Q000235:genetics*; D000349:Africa; D005075:Biological Evolution; D051456:Gene Flow; D009154:Mutation; D010788:Photosynthesis / Q000235:genetics*; D058974:Phylogeography; D006109:Poaceae / Q000235:genetics* / Q000502:physiology
keywords: C4 photosynthesis; adaptation; gene flow; lateral gene transfer; phylogeography