Genomic origins of novel metabolic pathways: the case of C4 photosynthesis in grasses

The existence of traits of impressive complexity has always puzzled evolutionary biologists. Traits such as camera eyes, bacteria flagella and plant carnivory result from intricate interactions between multiple structural and metabolic components. Understanding how each of these components originated and evolved to lead to the emergence of such a network of interactions and the associated function is therefore a major scientific challenge. Darwin and Wallace provided probably the major contribution to the problem; natural selection operating over successive generations via slight modifications can produce complexity. Nonetheless, there is still a large gap between the macroevolutionary patterns that are observed and the genetic changes underlying them. Here I address the problem of complex trait origins using the C4 photosynthetic metabolism as a study system. My comparative analyses of whole genome sequencing data of selected grass lineages showed that (1) enzymes of the C4 cycle can evolve via a burst of amino acid substitutions concentrated in a relatively short period of time, followed by continued adaptive evolution and anatomical specializations, showing that a single C4 origin can give rise to a variety of C4 phenotypes; (2) gene duplication via dosage effects can be a mechanism to suddenly increase the expression levels of genes involved in the C4 cycle; (3) adaptive mutations in components of the C4 trait can evolve in isolation in distinct genetic pools, and later be combined in admixture events; and (4) in some cases such adaptive mutations might be swept across populations by means other than recursive recombination. Overall, the findings presented in this dissertation suggest that (i) the components required for a rudimentary C4 cycle might be acquired in a relatively short period of time via large effect mutations on key genes, and (ii) genetic exchanges between divergent lineages can facilitate the assembly and optimization of a C4 metabolism. In addition, the methods developed here to analyse the genomic origins of C4 photosynthesis using low-coverage sequence data can be applied to other groups and other traits, potentially contributing to the advent of large-scale comparative genomic analyses to understand the evolutionary origins of complex adaptive traits.