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

Abstract

Background and Aims The Arctic tundra, with its extreme temperatures and short growing season, is evolutionarily young and harbors one of the most species-poor floras on Earth. Arctic species often show little phenotypic and genetic divergence across circumpolar ranges. However, strong intraspecific postzygotic 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. Methods 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). Key Results 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. Conclusion We show that postzygotic 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.

Mating system and speciation I: Accumulation of genetic incompatibilities in allopatry

“…Empirical results are so far limited but tend to support our predictions, in particular the accumulation of numerous incompatibilities between recently diverged populations of several selfing Arctic plant species [18,19], and the phylogeny-based analyses suggesting self-compatible lineages in the Solanaceae have higher speciation rates than self-incompatible [12,16]. However, the process of speciation in these cases remains poorly known.…”

Mating system and speciation I: accumulation of genetic incompatibilities in allopatry

“…So far, empirical results are still limited but tend to support these predictions, for example with the accumulation of numerous incompatibilities between recently diverged population of selfing arctic species [18, 19] or with macro-analyses suggesting higher speciation rates in selfing lineages in Solanaceae [12, 16] as mentioned in the introduction. However, the underlying process of speciation remains unknown.…”

“…A more explicit analysis remains to be done but our basic model (where selection linearly decreases with the selfing rate) confirms this prediction as soon as antagonistic selection is strong enough (say of the order of N e s > 5). So far, empirical results are still limited but tend to support these predictions, for example with the accumulation of numerous incompatibilities between recently diverged population of selfing arctic species [18,19] or with macro-analyses suggesting higher speciation rates in selfing lineages in Solanaceae [12,16] as mentioned in the introduction. However, the underlying process of speciation remains unknown.…”

“…To our knowledge however, there are only a few of such studies. For instance, in the Arctic flora, intraspecific crosses between geographically isolated populations of eight predominantly selfing species resulted in F1 hybrids with low pollen fertility and seed set, whereas no reduced fertility was observed in the single outcrossing species for which successful crosses could be made [18, 19]. In the selfing species, it was estimated that RI may have developed over just a few millennia.…”

Indirect Effects of Parental Conflict on Conspecific Offspring Development

“…Yet, Hybrid Seed Inviability (HSI) is also common in diploid plant systems and largely results from parent-of-origin specific growth defects in the endosperm (Brandvain and Haig 2005;Lowry et al 2008;Briscoe Runquist et al 2014;Rebernig et al 2015;Garner et al 2016;Lafon-Placette and Köhler 2016;Oneal et al 2016;Lafon-Placette et al 2017Roth et al 2018bRoth et al , 2019Coughlan et al 2020b;Sandstedt et al 2020;Gustafsson et al 2021;İltaş et al 2021). These patterns, while strikingly similar to the defects exemplified in interploidy crosses (Lafon-Placette and Köhler 2016;Lafon-Placette et al 2017;Städler et al 2021), cannot be explained by genome-wide imbalances of maternal:paternal gene expression in the endosperm, and must involve the evolution of paternal-excessive and maternal-repressive alleles.…”