Genomic differentiation and SNP variation reveal local adaptations to eastern Mediterranean environmental conditions in wild radishes

Background and Aims: Morphological differences between the two genetically close wild radishes, Raphanus raphanistrum and R. pugioniformis, include differences in fruit structure that influence their dispersal ability and within-population spatial structure. Here we tested within- and among-population genetic variation, hypothesizing that (1) short-distance dispersal of heavy fruits in R. pugioniformis provide opportunities for local adaptions, while (2) long distances of single-seeded diaspores increase migration rates in R. raphanistrum, resulting in closer genetic distances among populations. Methods: Populations were mapped along a geographical gradient in the eastern Mediterranean, and genotyping by sequencing was employed to assess population genetic structure. Population genetic variation was analysed using genetic diversity parameters, pairwise genetic differentiation coefficients, Mantel tests, migration rates and ADMIXTURE analyses. Furthermore, SNP detection was utilized to identify loci associated with local adaptations. Key Results: The average values of migration rates were similar in the two species, and non-synonymous SNP loci in coding region sequences of R. raphanistrum (n = 12) and R. pugioniformis (n = 7) were well associated with directional selection. However, the genetic diversity parameters, isolation-by-distance Mantel tests, principal coordinates analysis and ADMIXTURE analyses indicated higher genetic differentiation among populations of R. pugioniformis than among populations of R. raphanistrum. Furthermore, a higher number of loci in R. pugioniformis than in R. raphanistrum (12 vs 3 SNP outlier loci, respectively) were associated with average annual rainfall, the most prominent environmental parameter in the east Mediterranean. Conclusions: The results support the hypothesis that long-distance dispersal contributes to lower genetic diversity in populations of R. raphanistrum compared with R. pugioniformis. Considering that the distribution range of R. raphanistrum is relatively homogeneous, whereas R. pugioniformis is scattered across varying topographical and climatic gradients, the results of this genome scan highlight the significant role of the environment in adaptive inter- and intra-species genetic variation in these two genetically close species.