Aim To assess the role of the Balkan Peninsula as a Pleistocene refugium for the smooth newt, Lissotriton vulgaris, and to test whether its genetic differentiation is temporally compatible with the southern refugia model. Location The Balkan Peninsula. Methods Phylogeographical analyses were conducted using mitochondrial DNA (mtDNA) sequences sampled from 49 populations of L. vulgaris. A fossil‐calibrated estimate of divergence times among major mtDNA clades was obtained. Results We detected seven parapatrically distributed mtDNA clades with very little admixture among populations. Whereas most clades diverged in the Pleistocene, the earliest splits between Caucasian, Anatolian and Balkan clades occurred in the Pliocene. Clades C, D, K and M have local distributions within the Balkans and have evolved in isolation from other groups. Clade L originated in the Pannonian Basin and northern margin of the Balkan Peninsula and recently expanded across central and western Europe. Clades H and E have recently arrived in the Balkans from source populations in the Apennine Peninsula and Anatolia, respectively. Main conclusions The history of L. vulgaris involves multiple, independent refugial populations in the Balkans. Only one of them, located at the northern periphery of the peninsula, showed evidence of post‐glacial expansion into western and northern Europe. The Balkans have therefore served as a reservoir of old diversity for L. vulgaris. By contrast, populations at the northern and eastern frontiers of the peninsula have experienced non‐equilibrium dynamics. Our dating revealed that very little, if any, pre‐Pliocene genetic diversity has survived in Europe, despite an extensive fossil record for this species in the Miocene and Pliocene. Differentiation of the European mtDNA clades thus seems to have been primarily moulded by Pleistocene climate change. None of the currently recognized subspecies present in the Balkans are reciprocally monophyletic in their mtDNA. We hypothesize that incomplete lineage sorting and mtDNA introgression account for the observed discrepancies.
Genomic heterogeneity of divergence between hybridizing species may reflect heterogeneity of introgression, but also processes unrelated to hybridization. Heterogeneous introgression and its repeatability can be directly tested in natural hybrid zones by examining multiple transects. Here, we studied hybrid zones between the European newts Lissotriton montandoni and two lineages of Lissotriton vulgaris, with replicate transects within each zone. Over 1,000 nuclear genes located on a linkage map and mitochondrial DNA were investigated using geographical and genomic clines. Overall, the five transects were all similar, showing hallmarks of strong reproductive isolation: bimodal distribution of genotypes in central populations and narrow allele frequency clines. However, the extent of introgression differed between the zones, possibly as a consequence of their different ages, as suggested by the analysis of heterozygosity runs in diagnostic markers. In three transects genomic signatures of small‐scale (~2 km) zone movements were detected. We found limited overlap of cline outliers between transects, and only weak evidence of stronger differentiation of introgression between zones than between transects within zones. Introgression was heterogeneous across linkage groups, with patterns of heterogeneity similar between transects and zones. Predefined candidates for increased or reduced introgression exhibited only a subtle tendency in the expected direction, suggesting that interspecific differentiation is not a reliable indicator for the strength of introgression. These hierarchically sampled hybrid zones of apparently different ages show how introgression unfolds with time and offer an excellent opportunity to dissect the dynamics of hybridization and architecture of reproductive isolation at advanced stages of speciation.
Genetic variation within species is commonly structured in a hierarchical manner which may result from superimposition of processes acting at different spatial and temporal scales. In organisms of limited dispersal ability, signatures of past subdivision are detectable for a long time. Studies of contemporary genetic structure in such taxa inform about the history of isolation, range changes and local admixture resulting from geographically restricted hybridization with related species. Here we use a set of 139 transcriptome-derived, unlinked nuclear single nucleotide polymorphisms (SNP) to assess the genetic structure of the Carpathian newt (Lissotriton montandoni, Lm) and introgression from its congener, the smooth newt (L. vulgaris, Lv). Two substantially differentiated groups of Lm populations likely originated from separate refugia, both located in the Eastern Carpathians. The colonization of the present range in north-western and south-western directions was accompanied by a modest loss of variation; admixture between the two groups has occurred in the middle of the Eastern Carpathians. Local, apparently recent introgression of Lv alleles into several Lm populations was detected, demonstrating increased power for admixture detection in comparison to a previous study based on a limited number of microsatellite markers. The level of introgression was higher in Lm populations classified as admixed than in syntopic populations. We discuss the possible causes and propose further tests to distinguish between alternatives. Several outlier loci were identified in tests of interspecific differentiation, suggesting genomic heterogeneity of gene flow between species.
The ‘smooth newt’, the taxon traditionally referred to asLissotriton vulgaris, consists of multiple morphologically distinct taxa. Given the uncertainty concerning the validity and rank of these taxa,L. vulgarissensu lato has often been treated as a single, polytypic species. A recent study, driven by genetic data, proposed to recognize five species,L. graecus,L. kosswigi,L. lantzi,L. schmidtleriand a more restrictedL. vulgaris. The Carpathian newtL. montandoniwas confirmed to be a closely related sister species. We propose to refer to this collective of sixLissotritonspecies as the smooth newt orLissotriton vulgarisspecies complex. Guided by comprehensive genomic data from throughout the range of the smooth newt species complex we 1) delineate the distribution ranges, 2) provide a distribution database, and 3) produce distribution maps according to the format of the New Atlas of Amphibians and Reptiles of Europe, for the six constituent species. This allows us to 4) highlight regions where more research is needed to determine the position of contact zones.
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