An Invisible Domesticate: The Tangled History of Beer

Domestication is a co-evolutionary process where one species takes control of the reproduction of another in order to select for traits that benefit its own survival, leading to long-term genotypic and phenotypic changes in both partners. When I’ve traditionally thought about domesticated species, a wide range of organisms such as rice, maize, sheep, pigs, and horses would come to mind. Last year though, I realized that yeasts (mostly Saccharomyces cerevisiae, but also a few other Saccharomyces species) too are domesticated, largely through this study that was featured in an episode of my favorite podcast. I probably should have known, given humanity’s long history of drinking fermented foods and beverages such as bread, beer, and wine.

Archaeological evidence of fermented beverages dates all the way back to 7,000 B.C. in China. S. cerevisiae or its DNA has been recovered from Egyptian wine jars dating to more than 5000 years ago, and in containers from various excavated sites across the ancient Near East, all older than 2000 years old (among others). The graphic below, using information from a 2018 review on yeast domestication, shows some important archaeological dates in the history of fermented human products, but is by no means exhaustive.

Modern strains of broad varieties of yeast such as beer, wine, and baker’s yeast have complex evolutionary histories with distinct selection regimens for each kind of use, as well as hybridization with both wild and other domesticated strains. How do we know that? Population geneticists have developed tools that allow reconstruction of past evolutionary events based on the genome sequences of extant wild and domesticated species, and increasingly, ancient samples. As a window into this world, I want to briefly go through how the study I mentioned at the start came to conclude that modern beer strains contain ancestry related to European grape wine strains and Asian rice wine strains.

Beer is brewed using mainly two types of yeast, ale yeasts and lager yeasts, which produce the eponymous categories of beer. Ale yeasts are strains of S. cerevisiae, while lager yeast strains are hybrids of S. cerevisiae and Saccharomyces eubayanas called Saccharomyces pastorianus. The study started by grouping the genomes of ~400 yeast strains which included ale, lager, baking, wine, and wild strains from a variety of geographical locations into 13 distinct populations. How could they do this?

First, they extracted very specific information from all of the genome sequences: positions of the genome at which the different strains carried either one of two possible mutations, or put more generally, information on variation among the strains (see illustration below). They then modeled the observed variant positions in each strain based on possible ancestry proportions and other parameters, while changing the parameters to find the best possible model to explain the data. This led to estimates of ancestries for all the strains, which allowed their grouping based on population structure. Note here that for the lager strains, they were only looking at the S. cerevisiae part of the genomes.

The illustration shows four genomic sites for eight individuals; in our case, these could be eight individual yeast strains. The arrows represent sites at which there is variation. Based on the entire set of variants carried by each strain, one could estimate the ancestries of the strains, and use that to group them into distinct populations. Within each population, a particular allele may be fixed, like A in the first position in Population 1, or have a certain frequency; for instance, the allele frequency of C at the third position is 25% in Population 1, while the allele frequency of T at the first position is 75% in Population 2.

The authors next wanted to identify the possible founders of the four beer populations based on their grouping. For this, they took another model-based approach where they first constructed the best possible tree depicting the relationships between all the populations based on the frequencies of the variants in each population, assuming that each population could only have one immediate ancestral population; closely related populations should have more similar allele frequencies. They then asked if the tree becomes more likely or better supported if the model included the possibility of multiple ancestors and gene flow between populations. They saw that the beer populations were closely related to the European grape wine population, and found evidence for gene flow from a population closely related to the Asian rice wine (or saké) populations. This suggested that modern beer strains derived ancestry from populations related to European grape wine and Asian rice wine yeast strains.

To provide further support for this, the authors conducted what’s known as a four population test, in which two closely related populations are compared to two others that are more discordant. In this case, the two closely related populations were the European grape wine population and either one of the beer populations, and the two discordant populations were the Asian rice wine population and an even more divergent African population of strains. For all of the beer populations, they found that there were regions of the genome with variant frequencies more similar to the distant Asian rice wine population than to the closely related European grape wine population, again suggesting gene flow.

Until now, the authors had been looking at frequencies of mutations at variable sites across the strains. Now, these yeast strains were either diploid (having two copies of each chromosome, like humans) or polyploid (having more than two copies). They next constructed haplotypes, or maps of each chromosome, for two ale strains to see which variants occurred together in each chromosome across the strains. Sexual reproduction is accompanied by recombination or mixing and matching of homologous chromosomes. Using the haplotypes, the authors wanted to look for signs of recombination between the ancestral populations related to the European grape wine and Asian rice wine populations.

If, for instance, the variants that were shared by European grape wine and the ale strains had the same chromosomal organization in the two populations, it would indicate that there has not been much recombination to split up the variants into different chromosomes. The authors, however, found that variants from European grape wine and Asian rice wine populations were often switched around in the chromosomes of the ale strains. This suggested extensive recombination between genomes from the ancestral populations, which likely took place before the evolution of polyploidy in many ale strains, which restricts sexual reproduction and hence recombination.

This tangled history of modern beer strains invites us to ask where and when did the populations closely related to European grape wine and Asian rice wine yeasts actually come together. Since the site of domestication of European grape wine yeast is not known, the authors provide two possible hypotheses: 1) European grape wine yeast was first domesticated in Asia, where it mixed with Asian rice wine yeast before reaching Europe by trade or migration routes, or 2) European grape wine yeast was domesticated in Europe, and the mixing with Asian rice wine yeast occurred through subsequent East-West exchange along the Silk Route. Future studies, with more available yeast genome sequences including those of closely related wild, parental strains, could shed more light.

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