Rapid evolution of pigmentation in D. melanogaster: from cis regulation to phenotype

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PROJECT SUMMARY Rapid evolutionary adaptation is a foundational process in biology and at the core of many issues facing humanity including cancer, bacterial and viral diseases, evolution of drug and pesticide resistance, and biological response to global change. Many traits that evolve rapidly are complex and polygenic, and we lack a comprehensive understanding of the genetic and evolutionary dynamics of rapid evolution in natural populations. Pigmentation is a complex phenotype determined by many loci. From the peppered moth to the pocket mouse, adaptive coloration is widely observed and, in many cases, a few large effect loci have been identified and then shown mechanistically to be responsible. Patterns of pigmentation in Drosophila melanogaster are also thought to be adaptive, exhibiting clines at multiple scales, yet the genetic architecture and evolutionary dynamics are substantially more complex: body segments exhibit a variety of colors and patterns, dozens of loci affecting pigmentation have been verified, and patterns among different segments are not always highly correlated. Our preliminary data demonstrate that pigmentation can evolve very rapidly and cyclically in natural populations, fluctuating seasonally between dark coloration post-winter and light coloration post-summer. Hundreds of alleles change in frequency and are associated with the rapid evolution of pigmentation phenotype. Rapid seasonal evolution of pigmentation in D. melanogaster is not an example of a few loci of large effect, but represents a different paradigm underpinning the rapid evolution of complex traits. The need for rapid change is associated with a plastic response in which temperature causes an immediate change in pigmentation during development, but thermal plasticity does not explain the seasonal pigmentation response. We observe both durable shifts in midpoints as well as an increase in the distribution of the extremes. Shifts in population midpoint may not be due to the same set of loci as those that drive the phenotypic extremes. There are more than 20 known pigmentation loci controlled by cis regulation and associated with a diverse set of transcription factors. Pigmentation changes could be a result of shifting frequencies in trans factors that trigger cis regulation among a large number of loci, or it could be changes in cis effects directly. The targets of selection may be small in number or may represent a larger mutational target, and testing parallelism will enable us to determine the mutational target size. In this proposal we survey the genetics of rapid evolution in pigmentation with the goal of answering the following questions: Are the loci responsible for the average shift in pigmentation the same as loci in phenotypic extremes? Are the targets of rapid directional selection the same among populations? Are pigmentation traits directly responsible for rapid adaptation? Are cis regulatory changes occurring in the same set of loci at different spatial and temporal scales? To accomplish these goals we have planned a comprehensive set of experiments, using an innovative approach and novel experimental material, that will provide fundamental insight into the genetics of rapid evolution in natural populations.