Phylogenomics unravels speciation patterns in temperate-montane plant species: a case study on the recently radiating Ranunculus auricomus species complex

Abstract

The time frame and geographical patterns of diversification processes in European temperate-montane herbs are still not well understood. We used the sexual species of the Ranunculus auricomus complex as a model system to understand how vicariance vs. dispersal processes in the context of Pleistocene climatic fluctuations have triggered speciation in temperate-montane plant species. We employed Target Enrichment sequence data from about 600 nuclear genes and coalescent-based species tree inference methods to resolve phylogenetic relationships among the sexual taxa of the complex. We estimated absolute divergence times and, using ancestral range reconstruction, we tested if speciation was rather enhanced by vicariance or dispersal processes. Phylogenetic relationships among taxa were fully resolved. Incongruence among species trees mainly concerned the intraspecific relationships in R. notabilis s.l., R. cassubicifolius s.l., and the position of the tetraploid R. marsicus. Speciation events took place in a very short time at the end of the Mid-Pleistocene Transition (830-580 ka). A second wave of intraspecific geographical differentiation within and around the European mountain systems happened between 200-100 ka. Ancestral range reconstruction supports the existence of a widespread European ancestor of the R. auricomus complex. Vicariance processes have triggered allopatric speciation in temperate-montane plant species during the climatic deterioration occurred in the last phase of the Mid-Pleistocene Transition. Vegetation restructuring from forest into tundra could have confined these forest species into isolated glacial refugia. During subsequent warming periods, range expansions of these locally distributed species could have been hampered by congeneric competitors in the same habitat.