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Geographical isolation facilitates the emergence of distinct phenotypes within a single species, but reproductive barriers or selection is needed to maintain the polymorphism after secondary contact. Here, we explore the processes that maintain intraspecific variation of C4 photosynthesis, a complex trait that results from the combined action of multiple genes. The grass Alloteropsis semialata includes C4 and non‐C4 populations, which have co‐existed as a polyploid series for more than one million years in the miombo woodlands of Africa. Using population genomics, we show that there is genome‐wide divergence for the photosynthetic types, but the current distribution does not reflect a simple habitat displacement scenario as the genetic clusters overlap, being occasionally mixed within a given habitat. Despite evidence of recurrent introgression between non‐C4 and C4, in both diploids and polyploids, the distinct genetic lineages retain their identity, potentially because of selection against hybrids. Coupled with strong isolation by distance within each genetic group, this selection created a geographical mosaic of photosynthetic types. Diploid C4 and non‐C4 types never grew together, and the C4 type from mixed populations constantly belonged to the hexaploid lineage. By limiting reproductive interactions between photosynthetic types, the ploidy difference likely allows their co‐occurrence, reinforcing the functional diversity within this species. Together, these factors enabled the persistence of divergent physiological traits of ecological importance within a single species despite gene flow and habitat overlap.

C4 photosynthesis evolved multiple times independently in angiosperms, but most origins are relatively old so that the early events linked to photosynthetic diversification are blurred. The grass Alloteropsis semialata is an exception, as this species encompasses C4 and non-C4 populations. Using phylogenomics and population genomics, we infer the history of dispersal and secondary gene flow before, during and after photosynthetic divergence in A. semialata. We further analyse the genome composition of individuals with varied ploidy levels to establish the origins of polyploids in this species. Detailed organelle phylogenies indicate limited seed dispersal within the mountainous region of origin and the emergence of a C4 lineage after dispersal to warmer areas of lower elevation. Nuclear genome analyses highlight repeated secondary gene flow. In particular, the nuclear genome associated with the C4 phenotype was swept into a distantly related maternal lineage probably via unidirectional pollen flow. Multiple intraspecific allopolyploidy events mediated additional secondary genetic exchanges between photosynthetic types. Overall, our results show that limited dispersal and isolation allowed lineage divergence, with photosynthetic innovation happening after migration to new environments, and pollen-mediated gene flow led to the rapid spread of the derived C4 physiology away from its region of origin.

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 C4 photosynthesis as a study system, a derived physiology that increases plant productivity in warm, dry conditions. The grass Alloteropsis semialata includes C4 and non-C4 genotypes, 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 C4 and non-C4 A. 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 C4 components were acquired. However, rare but recurrent subsequent gene flow allowed the spread of adaptive loci across genetic pools. Indeed, laterally-acquired genes for key C4 functions were rapidly passed between populations with otherwise distinct gene pools. 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. This article is protected by copyright. All rights reserved.

Several chapters in this volume demonstrate how epigenetic work at the molecular level over the last few decades has revolutionized our understanding of genome function and developmental biology. However, epigenetic processes not only further our understanding of variation and regulation at the genomic and cellular levels, they also challenge our understanding of heritable phenotypic variation at the level of whole organisms and even the process of evolution by natural selection (Jablonka and Lamb 1989, 1995; Danchin et al. 2011). Although many of the epigenetic mechanisms involved in differential gene expression are reset each generation, some epigenetic marks are faithfully transmitted across generations (Jablonka and Raz 2009; Verhoeven et al. 2010a). In addition, we now know that natural variation exists not only at the DNA sequence level but also the epigenetic level (e.g., Vaughn et al. 2007; Herrera and Bazaga 2010). This may be particularly common in plants, and several studies suggest that epigenetic variation alone can cause significant heritable variation in phenotypic traits (e.g., Cubas et al. 1999; Johannes et al. 2009; Scoville et al. 2011). Because of these observations, there is currently increasing interest in understanding the role of epigenetic processes in ecology and evolution (e.g., Richards 2006, 2011; Bossdorf et al. 2008; Johannes et al. 2008; Richards et al. 2010a).