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

A Lovisa S Gustafsson,Lucas Marie-Orleach,Galina Gussarova,Christian Brochmann,Hajime Ikeda,Liv Borgen,Alexandre Antonelli,Loren H Rieseberg

doi:10.1093/aob/mcab128

Abstract

Background and AimsThe 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.MethodsWe 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).Key ResultsIn 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.ConclusionWe 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.

Highlights

The plants inhabiting the Arctic tundra must cope with extreme temperatures and variable and short growing seasons
We found that strong hybrid incompatibilities have developed within five Arctic species belonging to other genera of the Brassicaceae (Cardamine bellidifolia and Cochlearia groenlandica) as well as to other, distantly related plant families: Saxifragaceae (Saxifraga hyperborea), Ranunculaceae (Ranunculus pygmaeus) and Caryophyllaceae (Silene uralensis; Fig. 1)
While the parental plants as well as the F1 hybrids from intrapopulation crosses were highly fertile, we found that the F1 hybrids from within- and across-region crosses in these species showed significant reductions in pollen fertility and seed set

Summary

Introduction

The plants inhabiting the Arctic tundra must cope with extreme temperatures and variable and short growing seasons. The Arctic tundra is young in evolutionary terms; it formed about 2–3 million years ago in response to climate cooling, mainly by immigration of plant lineages pre-adapted to cold climates (Murray, 1995; Brochmann et al, 2013; Hoffmann et al, 2017). Many of these species seem to have rapidly spread across the entire circumpolar region (Hultén, 1937; Brochmann et al, 2013), and today the majority of Arctic species have vast, circumpolar ranges (Elven et al, 2011). The current genetic structure in many circumpolar species appears to be mainly shaped by the last glacial cycle due to extensive regional extinction and recolonization, and the species often exhibit little phenotypic and genetic variation (Eidesen et al, 2007; Skrede et al, 2009; Ikeda et al, 2017; unpubl. res.)

Methods

Results

Discussion

Conclusion