Search

The domestication of plants, animals and microbes by humans are the longest artificial evolution experiments ever performed. The study of these long-term experiments can teach us about the genomics of adaptation through the identification of the genetic bases underlying the traits favoured by humans. In laboratory evolution, the characterization of the molecular changes that evolved specifically in some lineages is straightforward because the ancestors are readily available, for instance in the freezer. However, in the case of domesticated species, the ancestor is often missing, which leads to the necessity of going back to nature in order to infer the most likely ancestral state. Significant and relatively recent examples of this approach include wolves as the closest wild relative to domestic dogs (Axelsson et al. 2013) and teosinte as the closest relative to maize (reviewed in Hake & Ross-Ibarra 2015). In both cases, the joint analysis of domesticated lineages and their wild cousins has been key in reconstructing the molecular history of their domestication. While the identification of closest wild relatives has been done for many plants and animals, these comparisons represent challenges for micro-organisms. This has been the case for the budding yeast Saccharomyces cerevisiae, whose natural ecological niche is particularly challenging to define. For centuries, this unicellular fungus has been the cellular factory for wine, beer and bread crafting, and currently for bioethanol and drug production. While the recent development of genomics has lead to the identification of many genetic elements associated with important wine characteristics, the historical origin of some of the domesticated wine strains has remained elusive due to the lack of knowledge of their close wild relatives. In this issue of Molecular Ecology, Almeida et al. (2015) identified what is to date the closest known wild population of the wine yeast. This population is found associated with oak trees in Europe, presumably its natural host. Using population genomics analyses, Almeida and colleagues discovered that the initial divergence between natural and domesticated wine yeasts in the Mediterranean region took place around the early days of wine production. Surprisingly, genomic regions that are key to wine production today appeared not to be derived from these natural populations but from genes gained from other yeast species.

Genetic variation in gene expression traits contributes to phenotypic diversity and may facilitate adaptation following environmental change. This is especially important in long-lived organisms where adaptation to rapid changes in the environment must rely on standing variation within populations. However, the extent of expression variation in most wild species remains to be investigated. We address this question by measuring the segregation of expression levels in white spruce [Picea glauca (Moench), Voss] in a transcriptome-wide manner and examining the underlying evolutionary and biological processes. We applied a novel approach for the genetic analysis of expression variation by measuring its segregation in haploid meiotic seed tissue. We identified over 800 transcripts whose abundances are most likely controlled by variants in single loci. Cosegregation analysis of allelic expression levels was used to construct regulatory associations between genes and define regulatory networks. The majority (67%) of segregating transcripts were under linkage. Regulatory associations were typically among small groups of genes (2-3 transcripts), indicating that most segregating expression levels can evolve independently from one another. One notable exception was a large putative trans effect that altered the expression of 180 genes that includes key regulators of protein metabolism, highlighting a regulatory cascade affected by variation in a single locus in this conserved metabolic pathway. Overall, segregating expression variation was associated with stress response- and duplicated genes, whose evolution may be linked to functional innovations. These observations indicate that expression variation might be important in facilitating diversity of molecular responses to environmental stresses in wild trees.

Genetic diversity in experimental, domesticated and wild populations of the related yeasts, Saccharomyces cerevisiae and Saccharomyces paradoxus, has been well described at the global scale. We investigated the population genomics of a local population on a small spatial scale to address two main questions. First, is there genomic variation in a S. paradoxus population at a spatial scale spanning centimetres (microsites) to tens of metres? Second, does the distribution of genomic variants persist over time? Our sample consisted of 42 S. paradoxus strains from 2014 and 43 strains from 2015 collected from the same 72 microsites around four host trees (Quercus rubra and Quercus alba) within 1 km2 in a mixed hardwood forest in southern Ontario. Six additional S. paradoxus strains recovered from adjacent maple and beech trees in 2015 are also included in the sample. Whole-genome sequencing and genomic SNP analysis revealed five differentiated groups (clades) within the sampled area. The signal of persistence of genotypes in their microsites from 2014 to 2015 was highly significant. Isolates from the same tree tended to be more related than strains from different trees, with limited evidence of dispersal between trees. In growth assays, one genotype had a significantly longer lag phase than the other strains. Our results indicate that different clades coexist at fine spatial scale and that population structure persists over at least a one-year interval in these wild yeasts, suggesting the efficacy of yearly sampling to follow longer term genetic dynamics in future studies.

Differences in gene expression are thought to be an important source of phenotypic diversity, so dissecting the genetic components of natural variation in gene expression is important for understanding the evolutionary mechanisms that lead to adaptation. Gene expression is a complex trait that, in diploid organisms, results from transcription of both maternal and paternal alleles. Directly measuring allelic expression rather than total gene expression offers greater insight into regulatory variation. The recent emergence of high-throughput sequencing offers an unprecedented opportunity to study allelic transcription at a genomic scale for virtually any species. By sequencing transcript pools derived from heterozygous individuals, estimates of allelic expression can be directly obtained. The statistical power of this approach is influenced by the number of transcripts sequenced and the ability to unambiguously assign individual sequence fragments to specific alleles on the basis of transcribed nucleotide polymorphisms. Here, using mathematical modelling and computer simulations, we determine the minimum sequencing depth required to accurately measure relative allelic expression and detect allelic imbalance via high-throughput sequencing under a variety of conditions. We conclude that, within a species, a minimum of 500-1000 sequencing reads per gene are needed to test for allelic imbalance, and consequently, at least five to 10 millions reads are required for studying a genome expressing 10 000 genes. Finally, using 454 sequencing, we illustrate an application of allelic expression by testing for cis-regulatory divergence between closely related Drosophila species.

Gene-expression variation in natural populations is widespread, and its phenotypic effects can be acted upon by natural selection. Only a few naturally segregating genetic differences associated with expression variation have been identified at the molecular level. We have identified a single nucleotide insertion in a vineyard isolate of Saccharomyces cerevisiae that has cascading effects through the gene-expression network. This allele is responsible for about 45% (103/230) of the genes that show differential gene expression among the homozygous diploid progeny produced by a vineyard isolate. Using isogenic laboratory strains, we confirm that this allele causes dramatic differences in gene-expression levels of key genes involved in amino acid biosynthesis. The mutation is a frameshift mutation in a mononucleotide run of eight consecutive T's in the coding region of the gene SSY1, which encodes a key component of a plasma-membrane sensor of extracellular amino acids. The potentially high rate of replication slippage of this mononucleotide repeat, combined with its relatively mild effects on growth rate in heterozygous genotypes, is sufficient to account for the persistence of this phenotype at low frequencies in natural populations.

Saccharomyces cerevisiae, the budding yeast, is the most thoroughly studied eukaryote at the cellular, molecular, and genetic levels. Yet, until recently, we knew very little about its ecology or population and evolutionary genetics. In recent years, it has been recognized that S. cerevisiae occupies numerous habitats and that populations harbour important genetic variation. There is therefore an increasing interest in understanding the evolutionary forces acting on the yeast genome. Several researchers have used the tools of functional genomics to study natural isolates of this unicellular fungus. Here, we review some of these studies, and show not only that budding yeast is a prime model system to address fundamental molecular and cellular biology questions, but also that it is becoming a powerful model species for ecological and evolutionary genomics studies as well.

Evidence of selection acting on major histocompatibility complex (MHC) genes has been illustrated with the analysis of their nucleotide sequences and allele frequency distribution. Comparing the patterns of population differentiation at neutral markers and MHC genes in the wild may provide further insights about the relative role of selection and neutrality in shaping their diversity. In this study, we combine both methods to assess the role of selection on a MHC gene in Atlantic salmon. We compare variation at a MHC class II B locus and microsatellites among 14 samples from seven different rivers and seven subpopulations within a single river system covering a variety of habitats and different geographical scales. We show that diversifying selection is acting on the sites involved in antigen presentation and that balancing selection maintains a high level of polymorphism within populations. Despite important differences in habitat type, the comparison of the population structure at MHC and microsatellites on large geographical scales reveals a correlation between patterns of differentiation, indicating that drift and migration have been more important than selection in shaping population differentiation at the MHC locus. In contrast, strong discrepancies between patterns of population differentiation at the two types of markers provides support for the role of selection in shaping population structure within rivers. Together, these results confirm that natural selection is influencing MHC gene diversity in wild Atlantic salmon although neutral forces may also be important in their evolution.

Reproductive isolation is a critical step in the process of speciation. Among the most important factors driving reproductive isolation are genetic incompatibilities. Whether these incompatibilities are already present before extrinsic factors prevent gene flow between incipient species remains largely unresolved in natural systems. This question is particularly challenging because it requires that we catch speciating populations in the act before they reach the full-fledged species status. We measured the extent of intrinsic postzygotic isolation within and between phenotypically and genetically divergent lineages of the wild yeast Saccharomyces paradoxus that have partially overlapping geographical distributions. We find that hybrid viability between lineages progressively decreases with genetic divergence. A large proportion of postzygotic inviability within lineages is associated with chromosomal rearrangements, suggesting that chromosomal differences substantially contribute to the early steps of reproductive isolation within lineages before reaching fixation. Our observations show that polymorphic intrinsic factors may segregate within incipient species before they contribute to their full reproductive isolation and highlight the role of chromosomal rearrangements in speciation. We propose different hypotheses based on adaptation, biogeographical events and life history evolution that could explain these observations.

Ecological genomics is a research field that aims to determine how a genome or a population of genomes interacts with its environment across ecological and evolutionary timescales. This matter was the central theme of the symposium on Ecological Genomics that took place at the First meeting of the Canadian Society for Ecology and Evolution, held at the University of Toronto in May 2007. Through their research on a diverse array of organisms, the various speakers illustrated how ecology and evolution benefit from genomics, and indirectly how genomics can benefit from evolutionary ecology.

New technologies promise to revolutionize the field of molecular ecology. This technological progress comes with its own set of challenges. Among the most important ones is the analysis and interpretation of the data in a way that tells us about the molecular causes of the phenotype of interest and its consequences. In this issue, Whitehead et al. (2010) reveal part of the mechanistic basis of evolved pollution tolerance by studying the developmental and transcriptional response of tolerant and sensitive fish embryos to polychlorinated biphenyls (PCBs), a pollutant commonly found in coastal waters of the United States. By integrating their gene expression profiling data with phenotypic data on individuals along with what is known about pathways by which this pollutant acts in zebrafish and mammals, they are able to suggest detailed mechanisms that have evolved to allow a fish population to adapt to a very damaging pollutant and develop normally.

Saccharomyces cerevisiae, the budding yeast, is the most thoroughly studied eukaryote at the cellular, molecular, and genetic levels. Yet, until recently, we knew very little about its ecology or population and evolutionary genetics. In recent years, it has been recognized that S. cerevisiae occupies numerous habitats and that populations harbour important genetic variation. There is therefore an increasing interest in understanding the evolutionary forces acting on the yeast genome. Several researchers have used the tools of functional genomics to study natural isolates of this unicellular fungus. Here, we review some of these studies, and show not only that budding yeast is a prime model system to address fundamental molecular and cellular biology questions, but also that it is becoming a powerful model species for ecological and evolutionary genomics studies as well.

New technologies promise to revolutionize the field of molecular ecology. This technological progress comes with its own set of challenges. Among the most important ones is the analysis and interpretation of the data in a way that tells us about the molecular causes of the phenotype of interest and its consequences. In this issue, Whitehead et al. (2010) reveal part of the mechanistic basis of evolved pollution tolerance by studying the developmental and transcriptional response of tolerant and sensitive fish embryos to polychlorinated biphenyls (PCBs), a pollutant commonly found in coastal waters of the United States. By integrating their gene expression profiling data with phenotypic data on individuals along with what is known about pathways by which this pollutant acts in zebrafish and mammals, they are able to suggest detailed mechanisms that have evolved to allow a fish population to adapt to a very damaging pollutant and develop normally.