Abstract

Understanding the mechanisms of local adaptation of wild species is a central issue in evolutionary biology. DNA sequence data allows investigating the recent demographic history of organisms. Knowledge of this history makes it possible to quantify adaptive and deleterious mutations and to analyze local adaptation at candidate genes taking the demographic context into account. As modulation of gene expression is crucial for an organism’s survival during stress conditions, a next step to investigate adaptation is to study the expression profile of candidate genes. Wild species are more valuable systems to investigate local adaptation than model organisms as key issues in ecology and evolution of the later cannot be addressed properly in some cases. Wild tomato species provide several advantages when studying adaptation to abiotic stress: they grow in diverse environments – ranging from mesic to extremely arid conditions – and its genomic information is available from the cultivated relative. First, we investigated the potential for adaptation and the strength of purifying selection acting at eight housekeeping genes in four closely related wild tomato species (Solanum arcanum, S. chilense, S. habrochaites, S. peruvianum) occupying different habitats by analyzing the distribution of fitness effects of a new mutation. There is no evidence for adaptation at these loci, but we detect strong purifying selection acting on the coding regions in all four species. Additionally, we find evidence for negative selection acting on non-coding regions. However, the strength of selection varies among species. Our results suggest that the variance of the distribution of fitness effects differ between closely related species which inhabit different environments. Second, using a candidate gene approach, we studied the evolution the Asr (ABA /water stress/ripening induced) gene family in populations from contrasting environments of S. chilense and S. peruvianum. Asr genes have been reported to help the plant cope with waterdeficit in many ways and are therefore useful candidates to study adaptation to drought stress. The molecular variation in the Asr gene family indicates that Asr1 has evolved under strong purifying selection. Prior reports described evidence for positive election at Asr2 – we cannot confirm this hypothesis and argue that patterns of selection discovered previously were caused by demography. Asr4 shows patterns consistent with local adaptation in a S. chilense population that inhabits an extremely dry environment. A new member of the Asr family (Asr5) was also discovered and seems to exchange genetic material with Asr3 by gene conversion. Our results provide a good example for the dynamic nature of gene families in plants, especially of tandemly arrayed genes that are of importance in adaptation. Third, we investigated the expression profile following cold and drought stress as well as the regulatory regions of Asr genes and the dehydrin pLC30-15. The latter has been reported to be involved in water and chilling stress response. Populations from different habitats of S. chilense and S. peruvianum were analyzed. The gene expression of Asr4 seems to be adaptive to drought conditions. Analysis of the regulatory regions shows a conserved promoter region of Asr2 and positive selection acting on the downstream region of pLC30-15. We provide an example for expression variation in natural populations but also observe plasticity in gene expression. As noise in expression is common in stress responsive genes, we describe this expression plasticity to be advantageous in these stress-responsive genes. In conclusion, taking the potential distribution of the species into account, it appears that S. peruvianum (and S. habrochaites) can cope with a great variety of environmental conditions without undergoing local adaptation, whereas S. chilense (and S. arcanum) seem to undergo local adaptation more frequently. With Asr4 we identify a gene to be of potential interest for further functional studies and describe wild Solanum species to be of great interest as a genetic resource for its cultivated relatives.