A polygenic architecture with habitat-dependent effects underlies ecological differentiation in Silene.

Ecological differentiation can drive speciation but it is unclear how the genetic architecture of habitat-dependent fitness contributes to lineage divergence. We investigated the genetic architecture of cumulative flowering, a fitness component, in second-generation hybrids between Silene dioica and Silene latifolia transplanted into the natural habitat of each species. We used reduced-representation sequencing and Bayesian sparse linear mixed models (BSLMMs) to analyze the genetic control of cumulative flowering in each habitat. Our results point to a polygenic architecture of cumulative flowering. Allelic effects were mostly beneficial or deleterious in one habitat and neutral in the other. Positive-effect alleles often were derived from the native species, whereas negative-effect alleles, at other loci, tended to originate from the non-native species. We conclude that ecological differentiation is governed and maintained by many loci with small, habitat-dependent effects consistent with conditional neutrality. This pattern may result from differences in selection targets in the two habitats and from environmentally dependent deleterious load. Our results further suggest that selection for native alleles and against non-native alleles acts as a barrier to gene flow between species.

RAD-seq reveals genetic structure of the F2-generation of natural willow hybrids (Salix L.) and a great potential for interspecific introgression.

BACKGROUND: Hybridization of species with porous genomes can eventually lead to introgression via repeated backcrossing. The potential for introgression between species is reflected by the extent of segregation distortion in later generation hybrids. Here we studied a population of hybrids between Salix purpurea and S. helvetica that has emerged within the last 30 years on a glacier forefield in the European Alps due to secondary contact of the parental species. We used 5758 biallelic SNPs produced by RAD sequencing with the aim to ascertain the predominance of backcrosses (F1 hybrid x parent) or F2 hybrids (F1 hybrid x F1 hybrid) among hybrid offspring. Further, the SNPs were used to study segregation distortion in the second hybrid generation. RESULTS: The analyses in STRUCTURE and NewHybrids revealed that the population consisted of parents and F1 hybrids, whereas hybrid offspring consisted mainly of backcrosses to either parental species, but also some F2 hybrids. Although there was a clear genetic differentiation between S. purpurea and S. helvetica (FST = 0.24), there was no significant segregation distortion in the backcrosses or the F2 hybrids. Plant height of the backcrosses resembled the respective parental species, whereas F2 hybrids were more similar to the subalpine S. helvetica. CONCLUSIONS: The co-occurrence of the parental species and the hybrids on the glacier forefield, the high frequency of backcrossing, and the low resistance to gene flow via backcrossing make a scenario of introgression in this young hybrid population highly likely, potentially leading to the transfer of adaptive traits. We further suggest that this willow hybrid population may serve as a model for the evolutionary processes initiated by recent global warming.

RAD sequencing resolved phylogenetic relationships in European shrub willows (Salix L. subg. Chamaetia and subg. Vetrix) and revealed multiple evolution of dwarf shrubs.

The large and diverse genus Salix L. is of particular interest for decades of biological research. However, despite the morphological plasticity, the reconstruction of phylogenetic relationships was so far hampered by the lack of informative molecular markers. Infrageneric classification based on morphology separates dwarf shrubs (subg. Chamaetia) and taller shrubs (subg. Vetrix), while previous phylogenetic studies placed species of these two subgenera just in one largely unresolved clade. Here we want to test the utility of genomic RAD sequencing markers for resolving relationships at different levels of divergence in Salix. Based on a sampling of 15 European species representing 13 sections of the two subgenera, we used five different RAD sequencing datasets generated by ipyrad to conduct phylogenetic analyses. Additionally we reconstructed the evolution of growth form and analyzed the genetic composition of the whole clade. The results showed fully resolved trees in both ML and BI analysis with high statistical support. The two subgenera Chamaetia and Vetrix were recognized as nonmonophyletic, which suggests that they should be merged. Within the Vetrix/Chamaetia clade, a division into three major subclades could be observed. All species were confirmed to be monophyletic. Based on our data, arctic-alpine dwarf shrubs evolved four times independently. The structure analysis showed five mainly uniform genetic clusters which are congruent in sister relationships observed in the phylogenies. Our study confirmed RAD sequencing as a useful genomic tool for the reconstruction of relationships on different taxonomic levels in the genus Salix.

Fitness of natural willow hybrids in a pioneer mosaic hybrid zone.

Hybrid fitness is an important parameter to predict the evolutionary consequences of a hybridization event and to characterize hybrid zones. We studied fitness parameters of F1 and later-generation hybrids between the lowland species Salix purpurea and the alpine S. helvetica that have recently emerged during colonization of an alpine glacier forefield. Fruit production (number of capsules per catkin and fruit set) did not differ between hybrids and parents, but the number of seeds per capsule of F1 hybrids was slightly lower than that of later-generation hybrids and of the parents. Germination rates and seedling growth were tested on three substrates (pH 4.5, 7.0, and 8.0). Germination rates of seeds collected from F1 hybrids were lower on acid and neutral substrates, but equal at pH 8.0 compared to all other groups, while the seeds from later-generation hybrids performed as well as the parents on all three substrates. In seedling growth, the colonizer S. purpurea performed better than all other taxa on all three substrates, while hybrids resembled the subalpine species S. helvetica. Results suggest that endogenous selection acts against F1 hybrids, but favors fitter genotypes in later-generation hybrids. Exogenous selection via soil pH appears to be weak during seedling establishment. The pioneer vegetation on the glacier forefield may offer sufficient niche space for hybrid seedlings. Owing to the relatively high fitness of the hybrids and the scattered distribution of hybrids and parental individuals on the glacier forefield, this hybrid zone can be assigned to a mosaic model, probably facilitating gene flow and introgression between the parental species. As establishment of the hybrid zone appears to be linked to a colonization process, we propose to call it a pioneer mosaic hybrid zone.