Spatial genetic structure in Beta vulgaris subsp. maritima and Beta macrocarpa reveals the effect of contrasting mating system, influence of marine currents, and footprints of postglacial recolonization routes

Understanding the factors that contribute to population genetic divergence across a species' range is a long-standing goal in evolutionary biology and ecological genetics. We examined the relative importance of historical and ecological features in shaping the present-day spatial patterns of genetic structure in two related plant species, Beta vulgaris subsp. maritima and Beta macrocarpa. Using nuclear and mitochondrial markers, we surveyed 93 populations from Brittany (France) to Morocco – the southern limit of their species' range distribution. Whereas B. macrocarpa showed a genotypic structure and a high level of genetic differentiation indicative of selfing, the population genetic structure of B. vulgaris subsp. maritima was consistent with an outcrossing mating system. We further showed (1) a strong geographic clustering in coastal B. vulgaris subsp. maritima populations that highlighted the influence of marine currents in shaping different lineages and (2) a peculiar genetic structure of inland B. vulgaris subsp. maritima populations that could indicate the admixture of distinct evolutionary lineages and recent expansions associated with anthropogenic disturbances. Spatial patterns of nuclear diversity and differentiation also supported a stepwise recolonization of Europe from Atlantic-Mediterranean refugia after the last glacial period, with leading-edge expansions. However, cytoplasmic diversity was not impacted by postglacial recolonization: stochastic long-distance seed dispersal mediated by major oceanic currents may mitigate the common patterns of reduced cytoplasmic diversity observed for edge populations. Overall, the patterns we documented here challenge the general view of reduced genetic diversity at the edge of a species' range distribution and provide clues for understanding how life-history and major geographic features interact to shape the distribution of genetic diversity.