Tracking alternative versions of the galactose gene network in the genus Saccharomyces and their expansion after domestication

In nature microorganisms frequently face fluctuating environmental conditions, which can favour adaptive phenotypic plasticity. When Saccharomyces cerevisiae grows on mixtures of glucose and galactose, galactose utilization is repressed by glucose and induction of the GAL gene network only occurs when glucose is exhausted. In this yeast, the study of trait variation at the population level led to the detection of distinct sets of GAL structural genes. Besides the reference version, present in most strains, alternative highly divergent alleles supporting faster growth on galactose were recently uncovered in strains associated with dairy products and also in some wild strains. The reference and alternative alleles highlight distinct galactose utilization strategies and are maintained by balancing selection. Here, we report on the discovery, using phylogenetic inference, of new wild populations of S. cerevisiae harbouring the alternative GAL version and, for the first time, of S. paradoxus alternative alleles. In addition, we show that the non-functional GAL version found earlier in S. kudriavzevii is phylogenetically related to the alternative versions, which constitutes case of trans-specific maintenance of highly divergent alleles that encompasses the entire genus. We characterized glucose and galactose utilization in strains harboring the different GAL network variants and exposed different levels of alleviation of glucose repression and growth proficiency on galactose. We propose that domestication of S. cerevisiae in the dairy environment co-opted the alternative GAL version present in wild strains. This involved a specialization towards thriving in milk from a generalist ancestor partially adapted to galactose consumption in the plant niche.