Abstract
Reconstructing the phylogenetic relationships within Caryophyllaceae tribe Sileneae has been obscured by hybridization and incomplete lineage sorting. Silene is the largest genus in the Caryophyllaceae, and unraveling its evolutionary history has been particularly challenging. In order to infer the phylogenetic relationships among the five species in Silene section Psammophilae, we have performed a genome skimming approach to acquire the complete plastid genome (cpDNA), nuclear ribosomal cistron (nrDNA), and partial mitochondrial genome (mtDNA). We have included 26 populations, representing the range of each species' distribution. This section includes five morphologically similar species endemic to the Iberian Peninsula and Balearic Islands (Ibiza and Formentera), yet some of them occupy distinct edaphic habitats (e.g. maritime sands, calcareous sandstones). In addition to phylogeographic analyses, genetic structuring using the chloroplast data set was inferred with Discriminant Analysis of Principal Components (DAPC), analyses of molecular variance (AMOVA), and a partial Mantel test. Reference-guided assembly of 50 bp single-end and 250 bp paired-end Illumina reads produced the nearly complete cpDNA genome (154 kbp), partial mtDNA genome (from 81 to 114 kbp), and the nrDNA cistron (6.4 kbp). Selected variable regions of the cpDNA and mtDNA assemblies were confirmed by Sanger sequencing. Phylogenetic analyses of the mainland populations reveal incongruence among the three genomes. None of the three data sets produced relationships consistent with taxonomy or geography. In contrast, Silene cambessedesii, present in the Balearic Islands, is the only species that forms a strongly supported monophyletic clade in the cpDNA genome and is strongly differentiated with respect to the remaining taxa of the Iberian Peninsula. These results contrast with those obtained for mainland populations. Across the entire analysis, only one well-supported mainland clade of Silene littorea and Silene stockenii emerges from the southern region of the Iberian Peninsula. DAPC and AMOVA results suggest the absence of genetic structure among mainland populations of Silene section Psammophilae, whereas partial Mantel test discarded spatial correlation of genetic differentiation. The widespread incongruence between morphology-based taxonomic boundaries and phylogeography suggests a history of interspecific hybridization, in which only a substantial geographic barrier, like isolation by the Mediterranean Sea, was sufficient to create and maintain species boundaries in Silene section Psammophilae.
Highlights
The Mediterranean Basin is commonly described as one of the most important biodiversity hotspots in the world (Médail and Quézel, 1997; Médail and Quézel, 1999; Myers et al, 2000)
The Balearic archipelago was separated from the mainland in the Oligocene [30–25 million years ago (Ma)], yet ephemeral land bridges connecting the mainland to the islands formed during the Messinian Salinity Crisis in the Late Miocene (Hsü et al, 1973; Krijgsman et al, 1999; Duggen et al, 2003)
In the Aegean islands, for instance, glaciations during the Late Pleistocene (~0.8–0.01 Ma) decreased sea levels and created land bridges that allowed the colonization of many mainland taxa (e.g. Nigella arvensis and Silene gigantea complexes, dwarf elephants, or pigmy hippopotami, among others) (Reyment, 1983; Bittkau and Comes, 2009; Du Pasquier et al, 2017), whereas Balearic Islands remained isolated because no land bridges connected them to the mainland during this time (Van der Geer et al, 2010)
Summary
The Mediterranean Basin is commonly described as one of the most important biodiversity hotspots in the world (Médail and Quézel, 1997; Médail and Quézel, 1999; Myers et al, 2000). The scarcity of new taxa coming to the Balearic Islands after their isolation contrasts with the colonization events in other Mediterranean islands. In the Aegean islands, for instance, glaciations during the Late Pleistocene (~0.8–0.01 Ma) decreased sea levels and created land bridges that allowed the colonization of many mainland taxa (e.g. Nigella arvensis and Silene gigantea complexes, dwarf elephants, or pigmy hippopotami, among others) (Reyment, 1983; Bittkau and Comes, 2009; Du Pasquier et al, 2017), whereas Balearic Islands remained isolated because no land bridges connected them to the mainland during this time (Van der Geer et al, 2010)
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