The budding yeast, Saccharomyces cerevisiae, is a leading system in genetics, genomics and molecular biology and is becoming a powerful tool to illuminate ecological and evolutionary principles. However, little is known of the ecology and population structure of this species in nature. Here, we present a field survey of this yeast at an unprecedented scale and have performed population genetics analysis of Chinese wild isolates with different ecological and geographical origins. We also included a set of worldwide isolates that represent the maximum genetic variation of S. cerevisiae documented so far. We clearly show that S. cerevisiae is a ubiquitous species in nature, occurring in highly diversified substrates from human-associated environments as well as habitats remote from human activity. Chinese isolates of S. cerevisiae exhibited strong population structure with nearly double the combined genetic variation of isolates from the rest of the world. We identified eight new distinct wild lineages (CHN I-VIII) from a set of 99 characterized Chinese isolates. Isolates from primeval forests occur in ancient and significantly diverged basal lineages, while those from human-associated environments generally cluster in less differentiated domestic or mosaic groups. Basal lineages from primeval forests are usually inbred, exhibit lineage-specific karyotypes and are partially reproductively isolated. Our results suggest that greatly diverged populations of wild S. cerevisiae exist independently of and predate domesticated isolates. We find that China harbours a reservoir of natural genetic variation of S. cerevisiae and perhaps gives an indication of the origin of the species.

The yeast Saccharomyces cerevisiae has been an essential component of human civilization because of its long global history of use in food and beverage fermentation. However, the diversity and evolutionary history of the domesticated populations of the yeast remain elusive. We show here that China/Far East Asia is likely the center of origin of the domesticated populations of the species. The domesticated populations form two major groups associated with solid- and liquid-state fermentation and appear to have originated from heterozygous ancestors, which were likely formed by outcrossing between diverse wild isolates primitively for adaptation to maltose-rich niches. We found consistent gene expansion and contraction in the whole domesticated population, as well as lineage-specific genome variations leading to adaptation to different environments. We show a nearly panoramic view of the diversity and life history of S. cerevisiae and provide new insights into the origin and evolution of the species.

Lager-brewing arose in 15th century Bavaria [1] and is nowadays the most popular technique for alcoholic beverage production in the world. The technique is characterized by low temperature fermentation using the domesticated yeast Saccharomyces pastorianus (synonym S. carlsbergensis). It has been clear that the lager yeast is a hybrid with one portion of its genome having originated from S. cerevisiae ale yeast [2]. However, the source of the non-ale subgenome, which endows lager yeast with cold tolerance, had been a matter of debate [3]. Recently, a Patagonian origin hypothesis of lager yeast has been proposed based on the discovery of a new cryotolerant Saccharomyces species from Patagonian native forests of Argentina [4]. This yeast, named S. eubayanus, exhibited the closest known match (99.56%) to the non-ale portion of lager yeast and, thus, was believed to be its progenitor. However, we now show that this yeast species is likely native to the Tibetan Plateau. One of the Tibetan populations of the species exhibits closer affinity with lager yeast than the Patagonian population as inferred from population genetics and genome sequence analyses. We thus provide strong evidence for a Far East Asian origin hypothesis of lager yeast, which apparently corresponds better with geography and world trade history.