Polyploidization is a rare yet sometimes successful way for animals to rapidly create geno- and phenotypes that may colonize new habitats and quickly adapt to environmental changes. In this study, we use water frogs of the Pelophylax esculentus complex, comprising two species (Pelophylax lessonae, genotype LL; Pelophylax ridibundus, RR) and various diploid (LR) and triploid (LLR, LRR) hybrid forms, summarized as P. esculentus, as a model for studying recent hybridization and polyploidization in the context of speciation. Specifically, we compared the geographic distribution and genetic diversity of diploid and triploid hybrids across Europe to understand their origin, maintenance and potential role in hybrid speciation. We found that different hybrid and parental genotypes are not evenly distributed across Europe. Rather, their genetic diversity is structured by latitude and longitude and the presence/absence of parental species but not of triploids. Highest genetic diversity was observed in central and eastern Europe, the lowest in the northwestern parts of Europe. This gradient can be explained by the decrease in genetic diversity during postglacial expansion from southeastern glacial refuge areas. Genealogical relationships calculated on the basis of microsatellite data clearly indicate that hybrids are of multiple origin and include a huge variety of parental genomes. Water frogs in mixed-ploidy populations without any parental species (i.e. all-hybrid populations) can be viewed as evolutionary units that may be on their way towards hybrid speciation. Maintenance of such all-hybrid populations requires a continuous exchange of genomes between diploids and triploids, but scenarios for alternative evolutionary trajectories are discussed.
BackgroundGenetic architecture of a species is a result of historical changes in population size and extent of distribution related to climatic and environmental factors and contemporary processes of dispersal and gene flow. Population-size and range contractions, expansions and shifts have a substantial effect on genetic diversity and intraspecific divergence, which is further shaped by gene-flow limiting barriers. The Balkans, as one of the most important sources of European biodiversity, is a region where many temperate species persisted during the Pleistocene glaciations and where high topographic heterogeneity offers suitable conditions for local adaptations of populations. In this study, we investigated the phylogeographical patterns and demographic histories of four species of semifossorial slow-worm lizards (genus Anguis) present in the Balkan Peninsula, and tested the relationship between genetic diversity and topographic heterogeneity of the inhabited ranges.ResultsWe inferred phylogenetic relationships, compared genetic structure and historical demography of slow worms using nucleotide sequence variation of mitochondrial DNA. Four Anguis species with mostly parapatric distributions occur in the Balkan Peninsula. They show different levels of genetic diversity. A signature of population growth was detected in all four species but with various courses in particular populations. We found a strong correlation between genetic diversity of slow-worm populations and topographic ruggedness of the ranges (mountain systems) they inhabit. Areas with more rugged terrain harbour higher genetic diversity.ConclusionsPhylogeographical pattern of the genus Anguis in the Balkans is concordant with the refugia-within-refugia model previously proposed for both several other taxa in the region and other main European Peninsulas. While slow-worm populations from the southern refugia mostly have restricted distributions and have not dispersed much from their refugial areas, populations from the extra-Mediterranean refugia in northern parts of the Balkans have colonized vast areas of eastern, central, and western Europe. Besides climatic historical events, the heterogeneous topography of the Balkans has also played an important role in shaping genetic diversity of slow worms.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0669-1) contains supplementary material, which is available to authorized users.
We investigated the recent evolutionary history of the Danube crested newt, Triturus dobrogicus through reconstructions of: (1) the number and position of refugia at the last glacial maximum, (2) the role of major central European rivers in pattern of post‐glacial dispersal, and (3) the present‐day distribution pattern. We analysed sequences of mitochondrial DNA (ND2, 1065 bp) and six microsatellite loci in 363 T. dobrogicus individuals from 58 populations covering the range of the species. Our analyses suggested that T. dobrogicus survived the last glacial maximum in two separate refugia positioned in northwestern Pannonia and in Southern Pannonia from where its range expanded along the Danube and Tisza Rivers. Our findings also confirmed that rivers played an important role in shaping the evolutionary history of amphibian species in Central Europe. We compared the T. dobrogicus range with another lowland amphibian, the fire‐bellied toad Bombina bombina, using species distribution modelling. In line with these models, the isolated mountains inside Pannonia are occupied not by B. bombina, but by its mountain‐dwelling sister‐species B. variegata. However, in contrast to the model, crested newts (including T. dobrogicus) are absent from these mountains. We attribute this biogeographical discrepancy to the positioning of the species’ refugia at the last glacial maximum.
We investigated the genomic constitution and the reproduction mode of Rana esculenta from two pure hybrid populations found in western Slovakia, using cytomorphological, karyological and allozyme electrophoretic methods. Both populations were composed of diploid R. esciilenta females and diploid and triploid R. esculenta males. A single subadult R. ridibitnda female was caught at one of the localities. The females significantly outnumbered the males in both populations. All electrophoretically investigated triploid R. esciilenta males possessed the allopolyploid genomic constitution RLL (one "ridihirnrki" and two "lessonae" genomes). In the ovariesitestes of diploid femalesimales, exclusively allelic products characteristic of R. ridihundu were detected, suggesting that they hybridogenetically produced gametes carrying a "ridihunrfu " genome. On the contrary, the electrophoresis revealed only allelic products characteristic of Rana lessonae in the testes of triploid RLL males from one of the populations. Thus, these males apparently substitutc genetically the host species R. lessonae and play the important role in perpetuation of the investigated population.
Coexistence of sperm‐dependent asexual hybrids with their sexual progenitors depends on genetic and ecological interactions between sexual and asexual forms. In this study, we investigate genotypic composition, modes of hybridogenetic gametogenesis and habitat preferences of European water frogs (Pelophylax esculentus complex) in a region of sympatric occurrence. Pelophylax esculentus complex comprises parental species P. ridibundus and P. lessonae, whose primary hybridization leads to hybridogenetic lineages of P. esculentus. Hybrids clonally transmit one parental genome and mate with the other parental species, forming a new generation of hybrids. In the region of western Slovakia, we found syntopic occurrence of diploid and triploid hybrids with P. lessonae, syntopic occurrence of all three taxa as well as the existence of pure P. ridibundus populations. All triploid hybrids were exclusively male possessing one ridibundus and two different lessonae genomes (RLL). Sex ratio in diploid hybrids was substantially female‐biased. Irrespective of the population composition, diploid hybrids excluded the lessonae genome from their germ line and produced ridibundus gametes. Contrarily, RLL males unequivocally eliminated the ridibundus genome and produced diploid lessonae sperms. Perpetuation of RLL males in studied populations is most likely achieved by their mating with diploid hybrid females. The composition of water frog populations is also shaped by taxon‐specific habitat preferences. While P. ridibundus preferred larger water bodies (gravelpits, fishery ponds, dead river arms), P. lessonae was most frequently found in marshes and smaller sandpits. Pelophylax esculentus occupied predominately similar habitats as its sexual host P. lessonae.
In temperate regions of the Earth Pleistocene, climatic fluctuations significantly influenced distribution of species. However, little is known on how glacial and interglacial cycles affected range dynamics of the species occupying lower latitudes. In this study, we investigated mitochondrial DNA (mtDNA) variation and reconstructed the potential current and past (during the mid‐Holocene, 6 ka BP, and the Last Glacial Maximum, LGM, 21 ka BP) distribution of Neurergus derjugini, an endangered amphibian species endemic to the mid‐Zagros Mountains in Iran and Iraq. Six haplotypes identified in the control region (D‐loop) form a well‐supported monophyletic clade, distinct from other Neurergus species and revealing a sister relationship to Neurergus kaiseri. Nucleotide diversity quantifying mean divergence between the sequences is low and does not support the recognition of distinct evolutionary lineages in Neurergus derjugini. The landscape connectivity analysis and the haplotype parsimony network reveal higher gene flow rate between the breeding streams in the southern part of the range, while the northern populations are more isolated. The potential distribution of Neurergus derjugini is restricted to valleys close to mountain tops, wherein very high elevations and dry habitats appear to be unsuitable. During the mid‐Holocene and LGM conditions, the range of the species may have been more extended and shifted to lower elevations. These findings show retraction of the Neurergus derjugini range during the Quaternary and indicate that range dynamics of the species occupying lower latitudes may not follow a scenario of glacial retraction and postglacial expansion.
The scarcity of parthenogenetic vertebrates is often attributed to their 'inferior' mode of clonal reproduction, which restricts them to self-reproduce their own genotype lineage and leaves little evolutionary potential with regard to speciation and evolution of sexual reproduction. Here, we show that for some taxa, such uniformity does not hold. Using hybridogenetic water frogs (Pelophylax esculentus) as a model system, we demonstrate that triploid hybrid males from two geographic regions exhibit very different reproductive modes. With an integrative data set combining field studies, crossing experiments, flow cytometry and microsatellite analyses, we found that triploid hybrids from Central Europe are rare, occur in male sex only and form diploid gametes of a single clonal lineage. In contrast, triploid hybrids from north-western Europe are widespread, occur in both sexes and produce recombined haploid gametes. These differences translate into contrasting reproductive roles between regions. In Central Europe, triploid hybrid males sexually parasitize diploid hybrids and just perpetuate their own genotype -which is the usual pattern in parthenogens. In north-western Europe, on the other hand, the triploid males are gamete donors for diploid hybrids, thereby stabilizing the mixed 2n-3n hybrid populations. By demonstrating these contrasting roles in male reproduction, we draw attention to a new significant evolutionary potential for animals with nonsexual reproduction, namely reproductive plasticity.
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