Using multilocus sequence data to assess population structure, natural selection, and linkage disequilibrium in wild tomatoes.

We employed a multilocus approach to examine the effects of population subdivision and natural selection on DNA polymorphism in 2 closely related wild tomato species (Solanum peruvianum and Solanum chilense), using sequence data for 8 nuclear loci from populations across much of the species' range. Both species exhibit substantial levels of nucleotide variation. The species-wide level of silent nucleotide diversity is 18% higher in S. peruvianum (pi(sil) approximately 2.50%) than in S. chilense (pi(sil) approximately 2.12%). One of the loci deviates from neutral expectations, showing a clinal pattern of nucleotide diversity and haplotype structure in S. chilense. This geographic pattern of variation is suggestive of an incomplete (ongoing) selective sweep, but neutral explanations cannot be entirely dismissed. Both wild tomato species exhibit moderate levels of population differentiation (average F(ST) approximately 0.20). Interestingly, the pooled samples (across different demes) exhibit more negative Tajima's D and Fu and Li's D values; this marked excess of low-frequency polymorphism can only be explained by population (or range) expansion and is unlikely to be due to population structure per se. We thus propose that population structure and population/range expansion are among the most important evolutionary forces shaping patterns of nucleotide diversity within and among demes in these wild tomatoes. Patterns of population differentiation may also be impacted by soil seed banks and historical associations mediated by climatic cycles. Intragenic linkage disequilibrium (LD) decays very rapidly with physical distance, suggesting high recombination rates and effective population sizes in both species. The rapid decline of LD seems very promising for future association studies with the purpose of mapping functional variation in wild tomatoes.

Genealogical footprints of speciation processes in wild tomatoes: demography and evidence for historical gene flow.

Multilocus studies assessing patterns of nucleotide polymorphism within and among closely related species provide access to genealogical information bearing on demographic and geographic aspects of their speciation history. However, the technical difficulties in obtaining sufficient sequence data have severely limited this approach thus far, especially in outbred plant taxa. We employ the analytical framework of divergence population genetics in testing the isolation model of speciation in three self-incompatible species of wild tomatoes (clade Lycopersicon), in particular the assumption of divergence without gene flow. Based on DNA sequence data for 13 nuclear loci, average levels of silent polymorphism vary more than three-fold among species. We estimate a large effective population size for the ancestral species, quite similar to that of the highly polymorphic L. peruvianum. The other two species, however, exhibit concordant signatures of population-size reduction. These demographic inferences are biologically plausible and consistent with results obtained from standard neutrality tests. While the isolation model cannot be rejected by goodness-of-fit criteria, patterns of intragenic linkage disequilibrium in L. peruvianum are indicative of historical introgression at least in some regions of the genome. Considered jointly with the geographic pattern of postzygotic reproductive isolation, our results suggest that speciation occurred under residual gene flow, implying natural selection as one of the evolutionary forces driving the diversification of tomato lineages.