The spatial scale of genetic differentiation in a model organism: the wild yeast Saccharomyces paradoxus

Abstract

Little information is presently available on the factors promoting genetic divergence in eukaryotic microbes. We studied the spatial distribution of genetic variation in Saccharomyces paradoxus, the wild relative of Saccharomyces cerevisiae, from the scale of a few centimetres on individual oak trees to thousands of kilometers across different continents. Genealogical analysis of six loci shows that isolates from Europe form a single recombining population, and within this population genetic differentiation increases with physical distance. Between different continents, strains are more divergent and genealogically independent, indicating well-differentiated lineages that may be in the process of speciation. Such replicated populations will be useful for studies in population genomics.

Figure 1

(a) The distribution of genotypes on two trees: 56 strains, 13 different genotypes, different letters indicating a different genotype (see electronic supplementary material). Each line represents a vertical transect, with dots indicating the sites of first sampling. Squares show the positions of the second set of samples collected around the sites found to have S. paradoxus in the first sample. (b) The probability of uncovering a different genotype as a function of physical distance on the tree trunk (logistic regression, p=0.02). For every pair of strains, whether they have the same or different genotype is plotted as a function of the distance between them. The data for tree 1002/Y only; points have been displaced to make them more obvious.

Figure 2

Genealogies for the six gene fragments. A total of 84 strains are shown, 65 from the UK and 19 from other locations in Europe (number of strains followed by location: RU (Russia), LA (Latvia), SW (Sweden), DE (Denmark) and SP (Spain)). Dark-grey shading highlights strains from the UK and light grey from Northeastern Europe. All the trees are perfect, containing no homoplasy, and rooted with strains from Far East Asia; numbers indicate the number of changes on that branch and non-synonymous changes are in bold. Strains from Johnson et al. (2004) for which we have only restriction digest data are not included, and for MFalpha1, polymorphic sites in the repeat region are also not included.

Figure 3

Species tree showing three distinct lineages within S. paradoxus; only branches compatible in all six gene genealogies are drawn. Branch lengths are proportional to the average number of changes for the six genes, numbers indicating lengths for SAG1, AGA2, STE2, STE3, MFA1 and MFalpha1, respectively. Numbers on the terminal taxa are lengths for the deepest node within the taxon (averages shown in black).