Ice age-driven range shifts of diploids and expanding autotetraploids of Biscutella laevigata within a conserved niche.

Abstract

Early studies of the textbook mixed-ploidy system Biscutella laevigata highlighted diploids restricted to never-glaciated lowlands and tetraploids at high elevations across the European Alps, promoting the hypothesis that whole-genome duplication (WGD) is advantageous under environmental changes. Here we addressed long-held hypotheses on the role of hybridisation at the origin of the tetraploids, their single vs multiple origins, and whether a shift in climatic niche accompanied WGD. Climatic niche modelling together with spatial genetics and coalescent modelling based on ddRAD-seq genotyping of 17 diploid and 19 tetraploid populations was used to revisit the evolution of this species complex in space and time. Diploids differentiated into four genetic lineages corresponding to allopatric glacial refugia at the onset of the last ice age, whereas tetraploids displaying tetrasomic inheritance formed a uniform group that originated from southern diploids before the last glacial maximum. Derived from diploids occurring at high elevation, autotetraploids likely inherited their adaptation to high elevation rather than having evolved it through or after WGD. They further presented considerable postglacial expansion across the Alps and underwent admixture with diploids. Although the underpinnings of the successful expansion of autotetraploids remain elusive, differentiation in B. laevigata was chiefly driven by the glacial history of the Alps.