Saccharomyces cerevisiae is one of the most important model organisms and has been a valuable asset to human civilization. However, despite its extensive use in the last 9,000 y, the existence of a seasonal cycle outside human-made environments has not yet been described. We demonstrate the role of social wasps as vector and natural reservoir of S. cerevisiae during all seasons. We provide experimental evidence that queens of social wasps overwintering as adults (Vespa crabro and Polistes spp.) can harbor yeast cells from autumn to spring and transmit them to their progeny. This result is mirrored by field surveys of the genetic variability of natural strains of yeast. Microsatellites and sequences of a selected set of loci able to recapitulate the yeast strain's evolutionary history were used to compare 17 environmental wasp isolates with a collection of strains from grapes from the same region and more than 230 strains representing worldwide yeast variation. The wasp isolates fall into subclusters representing the overall ecological and industrial yeast diversity of their geographic origin. Our findings indicate that wasps are a key environmental niche for the evolution of natural S. cerevisiae populations, the dispersion of yeast cells in the environment, and the maintenance of their diversity. The close relatedness of several wasp isolates with grape and wine isolates reflects the crucial role of human activities on yeast population structure, through clonal expansion and selection of specific strains during the biotransformation of fermented foods, followed by dispersal mediated by insects and other animals. evolutionary biology | genomics

Understanding the dynamics of biodiversity, including the spatial distribution of genetic diversity, is critical for predicting responses to environmental changes, as well as for effective conservation measures. This task requires tracking changes in biodiversity at large spatial scales and correlating with species functional traits. We provide three comprehensive resources to understand the determinants for mitochondrial DNA differentiation represented by (a) 15,609 COI sequences and (b) 14 traits belonging to 307 butterfly species occurring in Western‐Central Europe and (c) the first multi‐locus phylogenetic tree of all European butterfly species. By applying phylogenetic regressions we show that mitochondrial DNA spatial differentiation (as measured with GST, G′ST, D and DST) is negatively correlated with species traits determining dispersal capability and colonization ability. Thanks to the high spatial resolution of the COI data, we also provide the first zoogeographic regionalization maps based on intraspecific genetic variation. The overall pattern obtained by averaging the spatial differentiation of all Western‐Central European butterflies shows that the paradigm of long‐term glacial isolation followed by rapid pulses of post‐glacial expansion has been a pervasive phenomenon in European butterflies. The results and the extensive data sets we provide here constitute the basis for genetically‐informed conservation plans for a charismatic group in a continent where flying insects are under alarming decline.

The reproductive ecology of Saccharomyces cerevisiae is still largely unknown. Recent evidence of interspecific hybridization, high levels of strain heterozygosity, and prion transmission suggest that outbreeding occurs frequently in yeasts. Nevertheless, the place where yeasts mate and recombine in the wild has not been identified. We found that the intestine of social wasps hosts highly outbred S. cerevisiae strains as well as a rare S. cerevisiae×S. paradoxus hybrid. We show that the intestine of Polistes dominula social wasps favors the mating of S. cerevisiae strains among themselves and with S. paradoxus cells by providing a succession of environmental conditions prompting cell sporulation and spores germination. In addition, we prove that heterospecific mating is the only option for European S. paradoxus strains to survive in the gut. Taken together, these findings unveil the best hidden secret of yeast ecology, introducing the insect gut as an environmental alcove in which crosses occur, maintaining and generating the diversity of the ascomycetes.yeasts | Saccharomyces cerevisiae | Saccharomyces paradoxus | hybrids | social wasps S ince the birth of agriculture, the budding yeast Saccharomyces cerevisiae has flourished in human-made fermented products (1). However, insects such as social wasps have been recently shown to host S. cerevisiae in their intestine and spread them in the wild (2). For a long time it was agreed that the mating of S. cerevisiae spores mostly occurs between spores belonging to the same ascus (self-fertilization/inbreeding) and that outbreeding (mating of spores belonging to different asci) is a very uncommon event (3). However, several recent findings have called this hypothesis into question. Evidence of interspecific hybridization (4-6), a high level of strain heterozygosity (7,8), and prion transmission (9) have suggested that outbreeding could occur more frequently than previously estimated (9).We calculated the outbreeding rate from the heterozygosity level at polymorphic sites in three genes selected as able to reproduce the topology generated with the genomes of S. cerevisiae (10). Calculation of the outbreeding rate was carried out only on diploid strains for which the sequences of the three genes were available (n = 34; SI Appendix, Table S1), and was based on a modified model, accounting for the possibility of diploid individuals to derive either from intra-ascus mating or from outcrossing (11). Isolates from wasp gut were more likely to have originated from outbreeding compared with strains isolated from other sources (Fig. 1A). There are two possible reasons that could have led to this situation: either wasps prefer to feed on mated yeasts or the insect intestine makes yeast mating more likely.If wasps prefer to feed on mated yeasts, a possibility suggested by the evidence that fruit flies are differentially attracted by S. cerevisiae strains (12), we should have inferred almost the same outbreeding rate for strains isolated from wasp intestines and grapes, although th...