Natural variation in Drosophila shows weak pleiotropic effects.

BACKGROUND: Pleiotropy describes the phenomenon in which a gene affects multiple phenotypes. The extent of pleiotropy is still disputed, mainly because of issues of inadequate power of analyses. A further challenge is that empirical tests of pleiotropy are restricted to a small subset of all possible phenotypes. To overcome these limitations, we propose a new measurement of pleiotropy that integrates across many phenotypes and multiple generations to improve power. RESULTS: We infer pleiotropy from the fitness cost imposed by frequency changes of pleiotropic loci. Mixing Drosophila simulans populations, which adapted independently to the same new environment using different sets of genes, we show that the adaptive frequency changes have been accompanied by measurable fitness costs. CONCLUSIONS: Unlike previous studies characterizing the molecular basis of pleiotropy, we show that many loci, each of weak effect, contribute to genome-wide pleiotropy. We propose that the costs of pleiotropy are reduced by the modular architecture of gene expression, which facilitates adaptive gene expression changes with low impact on other functions.

Distinct Patterns of Selective Sweep and Polygenic Adaptation in Evolve and Resequence Studies.

In molecular population genetics, adaptation is typically thought to occur via selective sweeps, where targets of selection have independent effects on the phenotype and rise to fixation, whereas in quantitative genetics, many loci contribute to the phenotype and subtle frequency changes occur at many loci during polygenic adaptation. The sweep model makes specific predictions about frequency changes of beneficial alleles and many test statistics have been developed to detect such selection signatures. Despite polygenic adaptation is probably the prevalent mode of adaptation, because of the traditional focus on the phenotype, we are lacking a solid understanding of the similarities and differences of selection signatures under the two models. Recent theoretical and empirical studies have shown that both selective sweep and polygenic adaptation models could result in a sweep-like genomic signature; therefore, additional criteria are needed to distinguish the two models. With replicated populations and time series data, experimental evolution studies have the potential to identify the underlying model of adaptation. Using the framework of experimental evolution, we performed computer simulations to study the pattern of selected alleles for two models: 1) adaptation of a trait via independent beneficial mutations that are conditioned for fixation, that is, selective sweep model and 2) trait optimum model (polygenic adaptation), that is adaptation of a quantitative trait under stabilizing selection after a sudden shift in trait optimum. We identify several distinct patterns of selective sweep and trait optimum models in populations of different sizes. These features could provide the foundation for development of quantitative approaches to differentiate the two models.