Social wasps are a Saccharomyces mating nest

Abstract

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...

Sensory input attenuation allows predictive sexual response in yeast

“…This assumption is likely to hold under ecological conditions relevant for yeast mating outside of the ascus, which includes mating of haploids from different linages (outcrossing) or from the same lineage (inbreeding). While the frequency of yeast outcrossing, and of mating outside of the ascus in general, is significantly lower than that of inbreeding361, the genomic structure of natural and domesticated isolates of S. cerevisiae as well as observations in the wasp gut niche provide clear evidence for outcrossing in nature662. The selective importance of sexual aggregation in yeast is further emphasized by an apparently accelerated evolution of sexual agglutinins compared with other surface proteins, which suggests that agglutinins may play a major function in yeast speciation63.…”

The ecology of insect–yeast relationships and its relevance to human industry

“…While yeasts typically reproduce asexually, the gut environment of both wasps and fruit flies stimulates yeast outbreeding [84,85]. In fruit flies, the harsh conditions of the gut break up S. cerevisiae spore tetrads, allowing for 10Â greater hybridization rates than those that were not ingested by flies.…”

Yeast Hybrids in Winemaking

“…Although normally digested in the wasp intestine, viable strains of Saccharomyces can be isolated from wasps, and these wasps are thought to play an important role in dispersal of Saccharomyces in the wild 9 . Wasps were fed five genetically different strains of S. cerevisiae, each of which carried different genetic mutations, and the wasps were allowed to hibernate in isolation 10 . Yeasts were harvested from the wasp intestinal tract and evaluated for the evidence of mating.…”

“…Hybrids of S. cerevisiae × S. uvarum and S. cerevisiae × S. paradoxus were found 10 . This observation could mean either that the wasps prefer feeding on substances that naturally contain yeast hybrids, or that inter-as well as intraspecific mating occurs in the wasp intestinal tract.…”

“…Over one-third of the wasps developed interspecific hybrids of S. paradoxus and S. cerevisiae, indicating that illicit as well as licit mating occurs within the insect. Interestingly, both the pure S. cerevisiae strains and the pure S. paradoxus strains could no longer be isolated from the wasp intestine at the end of the hibernation period, and only the hybrid strains survived 10 . Thus, hybrids are better able to adapt to the intestine Regions that have a greater diversity of wasp food sources may show, in turn, a greater diversity of interspecific hybrids on grapes at the point of harvest, and this would be an interesting study to conduct.…”