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Was Fermentation Key to Yeast Diversification?

By Claire Asher, on 17 February 2015

From bread to beer, yeast has shaped our diets and our recreation for centuries. Recent research in GEE shows how humans have shaped the evolution of this important microorganism. As well as revealing the evolutionary origins of modern fission yeast, the new study published in Nature Genetics this month shows how techniques developed for detecting genetic causes of disease in humans can be usefully applied to better understand the ecology, biochemistry and evolution of commercially and scientifically important microorganisms like yeast.

Fission yeast, Schizosaccharomyces pombe, is one of the principal ‘model’ species that cell biologists use to try and understand the inner workings of cells. Most famously, Paul Nurse used this yeast to discover the genes that control cell division. The laboratory strain was first isolated from French wine in 1924, and has been used ever since by an increasingly large community of fission yeast researchers. However, serendipitous collection of new strains has continued slowly since that time, and many of these are associated with human fermentation processes – different strains have been isolated from Sicilian vineyards, from the Brazilian sugarcane spirit Cachaça and from the fermented tea Kombucha. Despite it’s enormous scientific importance, little is known about the ecology and evolution of fission yeast.

Research published this month by Professor Jürg Bähler, Dr Daniel Jeffares and colleagues from UCL’s department of Genetics, Evolution and Environment, along with researchers from 10 other institutions across five countries, reveals an intimate link between historic dispersal and diversification in yeast and our love of fermented food and drinks. The project sequenced the genomes of 161 strains of fission yeast, isolated in 20 countries over the last 100 years, enabling the researchers to reconstruct the evolutionary history of S. pombe, as well as investigating genetic and phenotypic variation within and between strains.

Beer, Wine and Colonialism

Bähler and Jeffares were able to date the diversification and dispersal of S. pombe to around 2,300 years ago, coinciding with the early distribution of fermented drinks such as beer and wine. Strains from the Americas were most similar to each other, and dated to around 1600 years ago, most likely carried across the Atlantic in fermented products by European colonists. This is reminiscent of findings for the common bread and beer yeast species, Saccharomyces cerevisae, whose global dispersal is thought to date to around 10,000 years ago, coinciding with Neolithic population expansions. This research therefore reveals the intimate link between human use of yeast for fermentation and it’s evolutionary diversification, and highlights the power of humans to shape the lives of the organisms with which they interact.

From Genotype to Phenotype

Fission Yeast, Schizosaccharomyces pombe

The researchers also used genome-wide association techniques to investigate the relationship between genotype and phenotype in the different strains. They began by carefully measuring 74 different traits in representatives of each strain. Some traits were simple, such as cell size and shape, but the researchers also measured environment-genotype interactions, for example by investigating growth rates and population sizes with different nutrient availabilities, drug treatments and other environment variables. In total, they identified 223 different phenotypes, most of which were heritable to some extent. Further, relatively few of the phenotypes were strongly linked to a particular population or region, making yeast ideal for genome-wide association studies (GWAS), unlike Saccharomyces cerevisae, for which it has not been possible to use GWAS successfully.

GWAS was developed to identify genes that are linked to specific diseases in humans, however this study highlights how the technique can usefully be applied to understanding evolution and genotype-phenotype relationships in other organisms. Tightly controlled experimental conditions that can be achieved with microorganisms in the laboratory make GWAS possible and informative for organisms such as yeast. The researchers found 89 traits that were significantly associated with at least one gene; the strongest association explained about a quarter of variation between individuals.

Hallmarks of Selection

Looking at variation in genomic sequence between strains also allowed the researchers to investigate which parts of the genome have undergone more evolutionary change than others, and which regions are likely to be particularly important for function. Genes and genomic regions that are crucial to survival (such as those involved in basic cellular function, for example), tend to change relatively little over evolutionary time, because most mutations in their sequence would be severely detrimental to survival. A process known as purifying selection tends to keep these genetic sequences the same over long stretches of evolutionary time. Less crucial genetic sequences have more freedom to change without having serious consequences; they are not subject to strong purifying selection and tend to show more variation between individuals and populations.

The authors found that genetic variation between strains was lowest for protein-coding gene sequences (those that produce protein products such as hormones and enzymes), which is to be expected. However, they found variation was also low in non-coding regions near genes. These regions are thought to be important in gene regulation, echoing an increasing appreciation that the evolution of the regulation of gene expression may be as important, if not more so, than the evolution of the gene sequences themselves.

This ground-breaking research from GEE reveals fascinating insights into the ecology and evolution of fission yeast, a microorganism that directly or indirectly influences our lives on a daily basis. It highlights how important humans have been in shaping the genomes of commercially and scientifically important organisms, whilst also expanding our knowledge of genes, genomes and phenotypes more generally. Applying techniques such as this to a wider range of organisms has the potential to vastly increase our understanding of the genomic dynamics of evolutionary change.

Original Article:

() Nature Genetics

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This research was made possible by funding from the Wellcome Trust, the European Research Council (ERC), the (BBSRC), the UK Medical Research Council (MRC), Cancer Research UK, the Czech Science Foundation and Charles University.

Function Over Form:
Phenotypic Integration and the Evolution of the Mammalian Skull

By Claire Asher, on 8 December 2014

Our bodies are more than just a collection of independent parts – they are complex, integrated systems that rely upon precise coordination in order to function properly. In order for a leg to function as a leg, the bones, muscles, ligaments, nerves and blood vessels must all work together as an integrated whole. This concept, known as phenotypic integration, is a pervasive characteristic of living organisms, and recent research in GEE suggests that it may have a profound influence on the direction and magnitude of evolutionary change.

Phenotypic integration explains how multiple traits, encoded by hundreds of different genes, can evolve and develop together such that the functional unit (a leg, an eye, the circulatory system) fulfils its desired role. Phenotypic integration could be complete – every trait is interrelated and could show correlated evolution. However, theoretical and empirical data suggest that it is more commonly modular, with strong phenotypic integration within functional modules. This modularity represents a compromise between a total lack of trait coordination (which would allow evolution to breakdown functional phenotypic units) and the evolutionary inflexibility of complete integration. Understanding phenotypic integration and its consequences is therefore important if we are to understand how complex phenotypes respond to natural selection.

Functional modules in mammals, Goswami et al (2014)

Functional modules in mammals, Goswami et al (2014)

It is thought that phenotypic integration is likely to constrain evolution and render certain phenotypes impossible if their evolution would require even temporary disintegration of a functional module. However, integration may also facilitate evolution by coordinating the responses of traits within a functional unit. Recent research by GEE academic Dr Anjali Goswami and colleagues sought to understand the evolutionary implications of phenotypic integration in mammals.

Expanding on existing mathematical models, and applying these to data from 1635 skulls from nearly 100 different mammal species including placental mammals, marsupials and monotremes, Dr Goswami investigated the effect of phenotypic integration on evolvability and respondability to natural selection. Comparing between a model with two functional modules in the mammalian skull and a model with six, the authors found greater support for a larger number of functional modules. Monotremes, whose skulls may be subject to different selection pressures due to their unusual life history, did not fit this pattern and may have undergone changes in cranial modularity during the early evolution of mammals. Compared with random simulations, real mammal skulls tend to be either more or less disparate from each other, suggesting that phenotypic integration may both constrain and facilitate evolution under different circumstances. The authors report a strong influence of phenotypic integration on both the magnitude and trajectory of evolutionary responses to selection, although they found no evidence that it influences the speed of evolution.

Thus, phenotypic integration between functional modules appears to have a profound impact on the direction and extent of evolutionary change, and may tend to favour convergent evolution of modules that perform the same function (e.g bird and bat wings for powered flight), by forcing individuals down certain evolutionary trajectories. The influence of phenotypic integration on the speed, direction and magnitude of evolution has important implications for the study of evolution, particularly when analysing fossil remains, since it can make estimates of the timing of evolutionary events more difficult. Failing to incorporate functional modules into models of evolution will likely reduce their accuracy and could produce erroneous results.

Phenotypic integration is what holds together functional units within an organism as a whole, in the face of natural selection. Modularity enables traits to evolve independently when their functions are not strongly interdependent, and prevents evolution from disintegrating functional units. Through these actions, phenotypic integration can constrain or direct evolution in ways that might not be predicted based on analyses of traits individually. This can have important impacts upon the speed, magnitude and direction of evolution, and may tend to favour convergence.

Original Article:

() Global Environmental Change

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This research was made possible by support from the Natural Environment Research Council (NERC), and the National Science Foundation (NSF).