Rapid functional and evolutionary changes follow gene duplication in yeast

Duplication of genes or genomes provides the raw material for evolutionary innovation. After duplication a gene may be lost, recombine with another gene, have its function modified or be retained in an unaltered state. The fate of duplication is usually studied by comparing extant genomes and reconstructing the most likely ancestral states. Valuable as this approach is, it may miss the most rapid evolutionary events. Here, we engineered strains of Saccharomyces cerevisiae carrying tandem and non-tandem duplications of the singleton gene IFA38 to monitor (i) the fate of the duplicates in different conditions, including time scale and asymmetry of gene loss, and (ii) the changes in fitness and transcriptome of the strains immediately after duplication and after experimental evolution. We found that the duplication brings widespread transcriptional changes, but a fitness advantage is only present in fermentable media. In respiratory conditions, the yeast strains consistently lose the non-tandem IFA38 gene copy in a surprisingly short time, within only a few generations. This gene loss appears to be asymmetric and dependent on genome location, since the original IFA38 copy and the tandem duplicate are retained. Overall, this work shows for the first time that gene loss can be extremely rapid and context dependent.