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Böndel, Katharina (2014): Evolution of the wild tomato species Solanum chilense: demography and natural selection. Dissertation, LMU München: Faculty of Biology



Demography and adaptation are important factors determining the evolution of plant species. Many plant species are substructured into populations or demes connected by migration (metapopulations). The spatial distribution of populations and migration patterns depend on the means of dispersal. Since plants are sessile organisms, they also have to cope with both biotic and abiotic stresses. Therefore adaptations to local environmental conditions are essential to ensure survival and duration of the species. Wild tomato species (Solanum section Lycopersicon) are native to western South America. They occur in diverse and often extreme habitats including rain forests, coastal regions, high altitude habitats in the Andean Mountains and also hyperarid deserts in the Atacama Desert. Therefore, wild tomatoes are a good model system to study plant evolution and genomic bases for plant adaptation. This study focuses on the wild tomato species Solanum chilense, which exhibits a metapopulation structure with populations distributed from southern Peru to northern Chile. In its native range, S. chilense is confronted with different abiotic stresses including drought, cold and salinity. I sequenced 30 unlinked nuclear genes from 23 populations using next generation sequencing. 16 genes are involved in the abiotic stress response and serve as candidates for selection and adaptation. The remaining 14 genes are used as references to study the genomic average and species past demography. In the first part of this study, I investigated the demographic history of the wild tomato species Solanum chilense. Genetic data analyses revealed a north-south cline. This cline includes 1) a decrease of genetic variation from north to south, 2) an increase in the strength of population expansion along the cline, and 3) an increase in genetic differentiation from other wild tomato species towards the south of the range. Results further revealed that the populations form four groups: a central group and three peripheral groups. Altogether the results suggest that S. chilense originated in the northern part of its current distribution and migrated to the south, via two routes, along the coast and higher up in the Andes. During this north-south colonization, at least three bottlenecks occurred. In the second part of this study, I investigated natural selection and local adaptation in S. chilense. Signatures of selection and local adaptation were detected in the abiotic stress-related genes, for example signatures of positive selection in high altitude populations were found possibly indicating adaptation to low temperatures. Interestingly, signatures of balancing selection were detected as well in high altitude populations reflecting probable adaptation to different types of abiotic stresses. The coastal populations showed a distinct pattern. Several genes involved in the salt stress response exhibited signatures of local adaptation. Performing a salt stress experiment, I revealed that low altitude populations cope better with such stress than populations from intermediate or high altitudes. The coastal populations also showed an accumulation of nonsynonymous and possibly deleterious genetic variation, which can be explained by extreme bottlenecks and potential occurrence of selfing in some populations. Signatures of selection and local adaptation in S. chilense were mainly detected in populations from the peripheral groups and not in the central region, in agreement with the hypothesis that local adaptation is associated with the colonization of new territories. In summary, this study showed that demography plays an important role in the evolutionary history of S. chilense and that local adaptation for key abiotic stresses occurs more frequently in the marginal ranges of the species distribution.