Most organisms belonging to the Saccharomycotina subphylum have high genetic diversity and a vast repertoire of metabolisms and lifestyles, which explains its ecological versatility. The yeast Lachancea cidri is an ideal model for exploring the interplay between genetics, ecological function and evolution. L. cidri is a species that diverged from the Saccharomyces lineage before the whole-genome duplication and exhibits a broad distribution across the South Hemisphere, thus displaying an important ecological success. Here, we applied phylogenomics to investigate the adaptive genetic variation of L. cidri isolates obtained from natural environments in Australia and South America. Our approach revealed the presence of two main lineages according to their geographic distribution (Aus and SoAm). Estimation of the divergence time suggest that South American and Australian lineages diverged near the last glacial maximum event during the Pleistocene (64-8 KYA), consistent with the presence of multiple glacial refugia. Interestingly, we found that the French reference strain belongs to the Australian lineage, with a recent divergence (405-51 YA), likely associated to human movements. Additionally, species delimitation analysis identified different evolutionary units within the South American lineage and, together with parameters like Pi (π) and FST, revealed that Patagonia contains most of the genetic diversity of this species. These results agree with phenotypic characterizations, demonstrating a greater phenotypic diversity in the South American lineage. These findings support the idea of a Pleistocene-dated divergence between South Hemisphere lineages, where the Nothofagus and Araucaria ecological niches likely favored the extensive distribution of L. cidri in Patagonia.
The capacity of some yeasts to extract energy from single sugars, generating CO2 and ethanol (=fermentation), even in the presence of oxygen is known as the Crabtree effect. This phenomenon represents an important adaptation as it allowed the utilization of the ecological niche given by modern fruits, an abundant source of food that emerged in the terrestrial environment in the Cretaceous. However, identifying the evolutionary events that triggered fermentative capacity in Crabtree positive species is challenging, as microorganisms do not leave fossil evidence. Thus, key innovations should be inferred based only on traits measured under culture conditions. Here, we reanalyzed data form a common-garden experiment where several proxies of fermentative capacity were recorded in Crabtree positive and negative species, representing yeast’s phylogenetic diversity. In particular, we applied the “lasso-OU” algorithm which detects points of adaptive shifts, provided trait values representing a given performance measure. We tested whether multiple events or a single event explains the actual fermentative capacity of yeasts. According to the lasso-OU procedure, evolutionary changes in the three proxies of fermentative capacity that we considered (i.e., glycerol production, ethanol yield and respiratory quotient) are consistent with a single evolutionary episode (a whole-genomic duplication, WGD), instead of a series of small genomic rearrangements. Thus, the WGD appears as the key event behind the diversification of fermentative yeasts, which by increasing gene dosage and maximized their capacity of energy extraction for exploiting the new ecological niche provided by single sugars.