Rapid evolution of post-zygotic reproductive isolation is widespread in Arctic plant lineages

The Arctic tundra, with its extreme temperatures and short growing season, is evolutionarily young and harbours one of the most species-poor floras on Earth. Arctic species often show little phenotypic and genetic divergence across circumpolar ranges. However, strong intraspecific post-zygotic reproductive isolation (RI) in terms of hybrid sterility has frequently evolved within selfing Arctic species of the genus Draba. Here we assess whether incipient biological species are common in the Arctic flora.

We conducted an extensive crossing experiment including six species representing four phylogenetically distant families collected across the circumpolar Arctic. We crossed conspecific parental populations representing different spatial scales, raised 740 F1 hybrids to maturity and measured fertility under laboratory conditions. We examined genetic divergence between populations for two of these species (Cardamine bellidifolia and Ranunculus pygmaeus).

In five of the six species, we find extensive reduction in pollen fertility and seed set in F1 hybrids; 219 (46 %) of the 477 F1 hybrids generated between parents separated by ≥427 km had <20 % pollen fertility. Isolation with migration (IM) and *BEAST analyses of sequences of eight nuclear genes in C. bellidifolia suggests that reproductively isolated populations of this species diverged during, or even after, the last glaciation. Likewise, Arctic populations of R. pygmaeus were genetically very similar despite exhibiting strongly reduced fertility in crosses, suggesting that RI evolved recently also in this species.

We show that post-zygotic RI has developed multiple times within taxonomically recognized Arctic species belonging to several distantly related lineages, and that RI may have developed over just a few millennia. Rapid and widespread evolution of incipient biological species in the Arctic flora might be associated with frequent bottlenecks due to glacial cycles, and/or selfing mating systems, which are common in the harsh Arctic environment where pollinators are scarce.