Polygenic evolution of a sugar specialization trade-off in yeast

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The evolution of novel traits can involve many mutations scattered throughout the genome1,2. Detecting and validating such a suite of alleles, particularly if they arose long ago, remains a key challenge in evolutionary genetics1,2,3. Here we dissect an evolutionary trade-off of unprecedented genetic complexity between long-diverged species. When cultured in 1% glucose medium supplemented with galactose,Saccharomyces cerevisiae, but notS. bayanusor otherSaccharomycesspecies, delayed commitment to galactose metabolism until glucose was exhausted. Promoters of seven galactose (GAL) metabolic genes fromS. cerevisiae, when introduced together intoS. bayanus, largely recapitulated the delay phenotype in 1% glucose-galactose medium, and most had partial effects when tested in isolation. Variation inGALcoding regions also contributed to the delay when tested individually in 1% glucose-galactose medium. When combined,S. cerevisiae GALcoding regions gave rise to profound growth defects in theS. bayanusbackground. In medium containing 2.5% glucose supplemented with galactose, wild-typeS. cerevisiaerepressedGALgene expression and had a robust growth advantage relative toS. bayanus; transgenesis ofS. cerevisiae GALpromoter alleles orGALcoding regions was sufficient for partial reconstruction of these phenotypes.S. cerevisiae GALgenes thus encode a regulatory program of slow induction and avid repression, and a fitness detriment during the glucose-galactose transition but a benefit when glucose is in excess. Together, these results make clear that genetic mapping of complex phenotypes is within reach, even in deeply diverged species.

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