Phylogeographic pattern of range expansion provides evidence for cryptic species lineages in Silene nutans in Western Europe

Abstract

As a result of recent or past evolutionary processes, a single species might consist of distinct Evolutionary Significant Units (ESUs), even corresponding to cryptic species. Determining the underlying mechanisms of range shifts and the processes at work in the build-up of divergent ESUs requires elucidating the factors that contribute to population genetic divergence across a species' range. We investigated the large-scale patterns of genetic structure in the perennial herbaceous plant species Silene nutans (Caryophyllaceae) in Western Europe. We sampled and genotyped 111 populations using 13 nuclear microsatellite loci and 6 plastid single-nucleotide polymorphisms. Broad-scale spatial population genetic structure was examined using Bayesian clustering, spatial multivariate analyses and measures of hierarchical genetic differentiation. The genotypic structure of S. nutans was typical of a predominantly allogamous mating system. We also identified plastid lineages with no intra-population polymorphism, mirroring two genetically differentiated nuclear lineages. No evidence of admixture was found. Spatial trends in genetic diversity further suggested independent leading-edge expansion associated with founding events and subsequent genetic erosion. Overall, our findings suggested speciation processes in S. nutans and highlighted striking patterns of distinct stepwise recolonisation of Western Europe shaped by Quaternary climate oscillations. Two main potential ESUs can be defined in Western Europe, corresponding to Eastern and Western nuclear-plastid lineages. In situ preservation of populations and genetic rescue implying ex situ conservation techniques should take the lineage identity into account. This is particularly true in Great Britain, northern France and Belgium, where S. nutans is rare and where distinct lineages co-occur in close contact.

Lineages ofSilene nutansdeveloped rapid, strong, asymmetric postzygotic reproductive isolation in allopatry

“…An individual's assignment to W1 or E1 plastid groups was based on a combination of six plastid SNPs developed from the intergenic spacer sequences psbA-trnH and the matK gene fragment of S. nutans representative samples (Lahiani et al 2013) and described in Martin et al (2016). An individual's assignment to W1 or E1 plastid groups was based on a combination of six plastid SNPs developed from the intergenic spacer sequences psbA-trnH and the matK gene fragment of S. nutans representative samples (Lahiani et al 2013) and described in Martin et al (2016).…”

“…An individual's assignment to W1 or E1 plastid groups was based on a combination of six plastid SNPs developed from the intergenic spacer sequences psbA-trnH and the matK gene fragment of S. nutans representative samples (Lahiani et al 2013) and described in Martin et al (2016). Amplification procedures, multiplexing, and genotyping were carried out following the standard protocols described in Godé et al (2014) and Martin et al (2016). Amplification procedures, multiplexing, and genotyping were carried out following the standard protocols described in Godé et al (2014) and Martin et al (2016).…”

“…To investigate the possibility of hybridization events in the regions of focus, we used a set of 24 nuclear microsatellites (Table S3). The populations of England, eastern France, and four Belgian populations (HAM, LEFF, OLL, and HER) were previously genotyped using six plastid SNPs and 13 nuclear microsatellites (B09, E08, G01, H07, D10, Sil16, Sil19, Sil24, Sil31, Sil35, Sil36, Sil37, and Sil42) in Martin et al (2016). The populations of England, eastern France, and four Belgian populations (HAM, LEFF, OLL, and HER) were previously genotyped using six plastid SNPs and 13 nuclear microsatellites (B09, E08, G01, H07, D10, Sil16, Sil19, Sil24, Sil31, Sil35, Sil36, Sil37, and Sil42) in Martin et al (2016).…”

Congruent population genetic structures and divergence histories in anther‐smut fungi and their host plants Silene italica and the Silene nutans species complex

“…Within S. nutans , we identified four distinct haplotypes based on the six plastid SNPs, retrieving in our sample the four major genetic lineages of S. nutans previously identified in Western Europe (Figure 1a; Martin et al, 2016, 2017; Van Rossum et al, 2018). The blue, yellow, orange and red haplotypes were found, as in previous studies, in the northeastern, southeastern, western and southwestern parts of Europe, respectively.…”

“…To further genotype the plant individuals for studying the population genetic structure, we used a combination of plastid (chloroplast) SNPs and nuclear microsatellite markers as previously described (Godé et al, 2014; Martin et al, 2016, 2017). For plastid markers, using the KASPAR protocol we genotyped six SNPs, named Cp42, Cp397, Cp540, Cp656, Cp730 and Cp804, and polymorphic for [T/G], [A/C], [C/T], [G/T], [C/T] and [T/G], respectively.…”