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How gene duplication and divergence contribute to genetic novelty and adaptation has been of intense interest, but experimental evidence has been limited. The genetic switch controlling the yeast galactose use pathway includes two paralogous genes in Saccharomyces cerevisiae that encode a co-inducer (GAL3) and a galactokinase (GAL1). These paralogues arose from a single bifunctional ancestral gene as is still present in Kluyveromyces lactis. To determine which evolutionary processes shaped the evolution of the two paralogues, here we assess the effects of precise replacement of coding and non-coding sequences on organismal fitness. We suggest that duplication of the ancestral bifunctional gene allowed for the resolution of an adaptive conflict between the transcriptional regulation of the two gene functions. After duplication, previously disfavoured binding site configurations evolved that divided the regulation of the ancestral gene into two specialized genes, one of which ultimately became one of the most tightly regulated genes in the genome.

Understanding the evolutionary relationship between genome content and ecological niche is one of the fundamental challenges of biology. The distinct physiologies of yeast species provide a window into how genomes evolve in concert with niche. Although the enzymes of the well studied yeast galactose utilization pathway are present in all domains of life, we have found that multiple genes of the GAL pathway are absent from four yeast species that cannot use galactose. Whereas three species lack any trace of the pathway except a single gene, Saccharomyces kudriavzevii, a close relative of Saccharomyces cerevisiae, retains remnants of all seven dedicated GAL genes as syntenic pseudogenes, providing a rare glimpse of an entire pathway in the process of degeneration. An estimate of the timing of gene inactivation suggests that pathway degeneration began early in the lineage and proceeded rapidly. S. kudriavzevii exhibits several other divergent physiological properties that are associated with a shift in ecological niche. These results suggest that rapid and irreversible gene inactivation and pathway degeneration are associated with adaptation to new ecological niches in natural populations. Inactivated genes may generally serve as markers of specific functions made dispensable by recent adaptive shifts.

Crop species experienced strong selective pressure directed at genes controlling traits of agronomic importance during their domestication and subsequent episodes of selective breeding. Consequently, these genes are expected to exhibit the signature of selection. We screened 501 maize genes for the signature of selection using microsatellites or simple sequence repeats (SSRs). We applied the Ewens-Watterson test, which can reveal deviations from a neutral-equilibrium model, as well as two nonequilibrium tests that incorporate the domestication bottleneck. We investigated two classes of SSRs: those known to be polymorphic in maize (Class I) and those previously classified as monomorphic in maize (Class II). Fifteen SSRs exhibited some evidence for selection in maize and 10 showed evidence under stringent criteria. The genes containing nonneutral SSRs are candidates for agronomically important genes. Because demographic factors can bias our tests, further independent tests of these candidates are necessary. We applied such an additional test to one candidate, which encodes a MADS box transcriptional regulator, and confirmed that this gene experienced a selective sweep during maize domestication. Genomic scans for the signature of selection offer a means of identifying new genes of agronomic importance even when gene function and the phenotype of interest are unknown.