Genetic origin, developmental mechanism, and evolutionary process of a novel phenotype in Mimulus (monkeyflowers)

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Project Summary The emergence of qualitatively distinct new structures or patterns (e.g., turtle shells, beetle horns, butterfly color patterns, plant flowers) is one of the most fascinating aspects of organismal evolution. How such novel, complex traits have originated and evolved remains one of the most important yet challenging problems of evolutionary biology. It is widely assumed that novel structures or patterns arise by co-option or rewiring of pre-existing developmental programs, but we know very little about the specific genetic changes that trigger such co-option or developmental rewiring, how the genetic changes translate to novel phenotypes, what kind of developmental pre-settings or cryptic pre-patterns are required for the the trigger gene(s) to produce the novel phenotype and how these cryptic pre-patterns come about, and how the novel phenotypes rise in frequency in natural habitats (i.e., the evolutionary process). This project is to address these fundamental questions by studying a novel, qualitatively distinct, pigmentation pattern that evolved very recently in a wild population of Mimulus verbenaceus (crimson monkeyflower), a species amenable to genetic and developmental manipulations as well as evolutionary analyses or/and ecological interrogations. We propose to: (i) Identify the causal gene and mutation(s) underlying the novel pigmentation pattern by genetic mapping and transgenic experiments; (ii) Characterize the developmental pre-settings (cryptic pre- patterns) required for the formation of the novel pigmentation pattern by identifying multiple upstream activators and repressors, through analysis of chemically induced mutants with altered pigmentation patterns; (iii) Elucidate the evolutionary process through which the novel phenotype rose in frequency in the natural habitat by population genomics analyses and field experiments. We anticipate that these studies will, for the first time, provide a detailed view of the genetic and developmental mechanisms as well as the evolutionary process driving the emergence of a novel phenotype in nature. The successful completion of this project is also expected to help move the field forward by shifting the focus from correlational studies and just-so stories of morphological innovations that happened in the distant past, to rigorous genetic, developmental, and evolutionary analyses of novel phenotypes that are still in the initial stage of emergence.