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Hybridogenesis in the P. kl. hispanicus complex. Pelophylax kl. hispanicus originates from hybridization between P. bergeri (B genome) and a new lineage P. n. t. 1 (E genome, as a reference to “Extinct”). It eliminates its P. bergeri germline and thus only contributes P. n. t. 1 gametes. This klepton requires P. bergeri to reproduce and their crosses yield klepton offspring only. These natural mechanisms allow to preserve the P. n. t. 1 germline in the wild.
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Hybridogenesis is a special mode of hybrid reproduction where one parental genome is eliminated and the other is transmitted clonally. We propose that this mechanism can perpetuate the genome of extinct species, based on new genetic data from Pelophylax water frogs. We characterized the genetic makeup of Italian hybridogenetic hybrids (P. kl. hispa...
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Citations
... As in other regions of central and southern Italy, green frogs are represented in the Matese Massif by a sinklepton, that is, by two closely related taxa from the genetic point of view, one of which is the parent species, Pelophylax bergeri, and the other is the hybridogenetic hybrid or klepton hybrid, Pelophylax kl. hispanicus (Dubois & Ohler, 1994;Günther & Plötner, 1994;Dubey & Dufresnes, 2017). The genetic makeup of the Italian hybridogenetic hybrids has recently been analysed and a new endemic lineage of eastern-Mediterranean origin as one parental ancestor of P. kl. hispanicus identified. ...
... kl. hispanicus), which can thus be considered as a semi living fossil" (Dubey & Dufresnes, 2017). Pelophylax bergeri and P. kl. hispanicus are morphologically and chromatically very similar and in Molise and Campania, as in the rest of central and southern Italy, they usually coexist in the same habitat Di Nicola et al., 2019). ...
... cf. bedriagae) was widely introduced to Italy, Belgium, France, Switzerland, Germany and some regions of Russia [43][44][45][46][47][48][49][50][51][52][53]. Introgression of mt-nuclear DNA genes of this species was found in eastern European populations of P. ridibundus and P. esculentus [54][55][56], while the native range of the species is located in western Iran, Turkey, southern Bulgaria, eastern Greece, the Caucasus and Crimea [8,9,17,[57][58][59][60][61]. ...
... The time shown next to node in italic (for the study lineages P. cf. bedriagae, Syrdarya and Balkhash of P. sp. novum in bold italic), Table S1: sampling information of mtDNA datasets; Table S2: sampling information of nDNA dataset; Table S3: molecular diversity indices and neutrality tests. References [8,9,39,43] are cited in the Tables S1 and S2. ...
In order to study the diversity, phylogenetic relationships and distribution of marsh frogs of
the Pelophylax ridibundus complex in Kazakhstan and northwest China, we conducted phylogeographic
analyses of 125 samples from53 localities using themtDNAND2 and COI genes and the SAI nuclear gene
sequences. Phylogenetic inference of mtDNA revealed three main lineages—sister lineages Balkhash
and Syrdarya (as the Central Asian P. sp. novum), and the Anatolian P. cf. bedriagae, while from nDNA
data, we additionally detected the western form, P. ridibundus. According to mtDNA data, the mean
genetic distances between P. sp. novum and two other forms of marsh frogs was more than 5%. Genetic
homogeneity within populations of the Syrdarya lineage and P. cf. bedriagae is characterized by low
nucleotide diversity and high haplotype diversity. Demographic analyses of the lineages showed past
population expansions of the Balkhash and the Syrdarya forms. Divergence from the most recent
ancestor had occurred in the Early Pleistocene period (2.46 Mya) for the Balkhash and the Syrdarya
lineages, and 1.27Mya for the P. cf. bedriagae. Our findings provide a first investigation of the lineage
diversification and population dynamics of the Central Asian marsh frogs and will be useful for further
taxonomic implications and conservational actions.
... The SAI-1 amplicon lengths obtained on agarose gel in this study were compared with species-unique SAI-1 length and assigned to specific Pelophylax species (P. ridibundus, P. kurtmuelleri, P. lessonae or P. shqipericus) as described in Hauswaldt et al. (2012), Dubey and Dufresnes (2017) and Vucić et al. (2018). ...
Spreading of alien water frog species (genus Pelophylax) has been reported across Europe, posing a severe risk for the replacement or genetic swamping of indigenous species. Crna Mlaka fishponds in Central Croatia were an experimental station for freshwater fish aquaculture during the first half of 20th century and hosted fish from different parts of Balkans. Crna Mlaka fishponds are thus estimated to be at higher risk of non-native frogs, likely introduced with the aquaculture industry, causing introgressive hybridization and genetic admixture of native Pelophylax species. We used nuclear and mitochondrial DNA sequences, in combination with microsatellite markers, to characterize water frogs of Crna Mlaka. We detected alleles of two native species, the Eurasian marsh frog Pelophylax ridibundus (Pallas, 1771) and the pool frog Pelophylax lessonae (Camerano, 1882), as well as non-native Albanian pool frog Pelophylax shqipericus (Hotz, Uzzell, Gunther, Tunner et Heppich, 1987) and Balkan pool frog Pelophylax kurtmuelleri (Gayda, 1940). Moreover, we found five hybrid forms: P. kurtmuelleri x P. ridibundus, P. kurtmuelleri x P. shqipericus, P. lessonae x P. kurtmuelleri, P. ridibundus x P. shqipericus, and P. lessonae x P. shqipericus indicating the existence of a hybrid swarm. The last three hybrids have never been reported in natural populations. Interestingly, although expected, no P. kl. esculentus (P. ridibundus x P. lessonae) was detected. Additionally, water frogs with introgressed mtDNA were detected, which results in cyto-nuclear discordance. The results of this study suggest that this is a unique case of species melting pot, a hybrid swarm emerging from two alien and two native frog species resulting in more than 50% of water frogs at this location being hybrids and/or having introgressed mtDNA and the loss of the hybridogenetic reproductive system of Pelophylax kl. esculentus.
... hispanicus (Fitzinger, 1826) should similarly reproduce via hybridogenesis with its parental taxon P. bergeri, although a recent molecular study has shown that the clonal genome transmitted by the hybridogen originated through the hybridisation with a species of the ridibundus group related to the Cyprian and Western Anatolian lineages, nowadays extinct in the wild (i.e. P. n.t. 1, Dubey & Dufresnes, 2017). According to this recent insight, a high conservation value should be conferred to this endemic hybridogenetic system (Dubey & Dufresnes, 2018). ...
... In Western Europe, introgression of P. bedriagae genes in P. ridibundus and P. kl. esculentus gene pools is recurrent (Holsbeek et al., 2008), thus the impact of this introduced taxon in Tuscany could be highly negative on the native hybridogenetic complex, potentially leading to genome replacement through hemiclonal exclusion or recombination processes. The recent discovery that Table 3. Haplotype diversity (hd), nucleotide diversity (pi) and average number of nucleotide differences (k) calculated for species (a) and localities (b P. kl. hispanicus retains the genome of an extinct species further poses important conservation implications for the safeguard of the parental P. bergeri and its klepton (Dubey & Dufresnes, 2017). In our analysis, 11 individuals were assigned to the native P. kl. hispanicus according to the observed length of polymorphism at the diagnostic SAI-1 marker (Hauswaldt et al., 2012), indeed bearing alleles associated to the native R-genome and P. bergeri mtDNA. ...
The introduction of alien water frogs is perhaps one of the most underestimated herpetological conservation issues in
Europe. The identification of distinct species is highly challenging at the phenotypic level, and artificial syntopy between
various taxa and lineages may lead to diverse outcomes, including hybridisation and local extinction. In central Italy the
native synklepton of Pelophylax bergeri (the parental taxon) and P. kl. (klepton) hispanicus (the hybridogenetic hybrid, which
clonally transmits the genome of an extinct ridibundus-like taxon) is present. Until recently, data regarding the presence of
alien water frogs in central Italy was scarce, and no alien taxa have been reported for Tuscany. In this study, four distinct
non-native Pelophylax lineages have been identified via molecular analysis in the Cecina and Arno river basins and ascribed to
the Marsh frog group (P. ridibundus sensu lato). Alien Pelophylax ridibundus, P. kurtmuelleri, and P. cf. bedriagae sensu stricto
currently appear to be widespread in the Cecina basin. Furthermore, evidence of hybridisation with autochthonous taxa
has been suggested by genetic analyses in four out of eight sampling localities. With a view to evaluate urgent conservation
strategies, a greater sampling effort is required to assess the actual distribution and ecology of the alien lineages, and further
research is necessary to measure their impact on the native hybridogenetic system of the central-southern Italian pool frogs.
... bergeri) replaced a native pool frog, P. lessonae ( Leuenberger et al., 2014;Dufresnes et al., 2016). New molecular data, apart of indication of exogenous green frog species, allowed also to reveal potential existing of new hybridogenetic complexes ( or even traces of extinct species in Europe ( Dubey and Dufresnes, 2017). ...
A molecular multiplex PCR method for identification of East European green frog species (Pelophylax ridibundus, P. cf. bedriagae and P. lessonae) and their hybrids was developed. This simple and rapid method can be used for identification of species-specific mitochondrial and nuclear DNA. The method is based on species-specific differences in primary structure of the subunit 1 of the mitochondrial cytochrome C oxidase gene (COI) and the intron-1 of the nuclear serum albumin gene (SAI-1). Based on the method, we analyzed numerous individuals of these species and their hybrids from East European Plain, the Crimea, the Caucasus, the Ural, as well as introduced populations from Western Siberia and the Kamchatka. In all cases, identification of species performed by use of the multiplex PCR method coincided with results of study of primary nucleotide sequences.
... lessonae and P. bergeri), and restricted to the Alpine catchments valleys of the Po plain (named "Pelophylax. n. t. 2", [29]). Mostly based on the intronic sequence marker Serum Albumin intron 1 (SAI-1), but lacking mitochondrial divergence, the origin of this lineage is pending additional analyses. ...
... In order to characterize the genetic nature and hybridogenetic mechanisms of the subalpine Pelophylax populations, we conducted a population genomic and morphometric survey of nine sites inhabited by P. lessonae and P. kl. esculentus in southern Switzerland. The objectives were (1) to assess the genetic composition of putative L-E and E-E populations, (2) to understand whether E-E populations are maintained through triploid individuals or other mechanisms, and (3) to infer the nature and origin of the P. n. t. 2 lineage previously proposed [29]. ...
... All south-alpine frogs belong to the P. lessonae clade, expect for the five P. ridibundus females collected at STA, which branch to the corresponding P. ridibundus clade. The intron-based phylogeny of Dubey & Dufresnes [29] is provided for comparison (~1.6 kb from two markers, including 1.4 kb from SAI-1); "P. n. t. 1": hemiclone sequenced in the Italian hybridogens P. kl. hispanicus; "P. ...
Background – Hybridogenesis can represent the first stage towards hybrid speciation where the hybrid taxon eventually weans off its parental species. In hybridogenetic water frogs, the hybrid Pelophylax kl. esculentus (genomes RL) usually eliminates one genome from its germline and relies on its parental species P. lessonae (genomes LL) or P. ridibundus (genomes RR) to perpetuate in so-called L-E and R-E systems. But not exclusively: some all-hybrid populations (E-E system) bypass the need for their parental species and fulfill their sexual cycle via triploid hybrid frogs. Genetic surveys are essential to understand the great diversity of these hybridogenetic dynamics and their evolution. Here we conducted such study using RAD-sequencing on Pelophylax from southern Switzerland (Ticino), a geographically-isolated region featuring different assemblages of parental P. lessonae and hybrid P. kl. esculentus.
Results – We found two types of hybridogenetic systems in Ticino: an L-E system in northern populations and a presumably all-hybrid E-E system in the closely-related southern populations, where P. lessonae was not detected. In the latter, we did not find evidence for triploid individuals from the population genomic data, but identified a few P. ridibundus (RR) as offspring from interhybrid crosses (LR×LR).
Conclusions – Assuming P. lessonae is truly absent from southern Ticino, the putative maintenance of all-hybrid populations without triploid individuals would require an unusual lability of genome elimination, namely that P. kl. esculentus from both sexes are capable of producing gametes with either L or R genomes. This could be achieved by the co-existence of L- and R- eliminating lineages or by “hybrid amphigamy”, i. e. males and females producing sperm and eggs among which both genomes are represented. These hypotheses imply that polyploidy is not the exclusive evolutionary pathway for hybrids to become reproductively independent, and challenge the classical view that hybridogenetic taxa are necessarily sexual parasites.
... While such an approach can prioritize sampling sites and/ or catchments, in-depth whole genome studies would still be needed to unequivocally disprove extinction. This limitation is mirrored in other groups harbouring presumed ghost species 4,16 . ...
Although hybridization between non-sibling species rarely results in viable or fertile offspring, it occasionally produces self-perpetuating or sexually-parasitic lineages in which ancestral genomes are inherited clonally and thus may persist as ‘ghost species’ after ancestor extinction. Ghost species have been detected in animals and plants, for polyploid and diploid organisms, and across clonal, semi-clonal, and even sexual reproductive modes. Here we use a detailed investigation of the evolutionary and taxonomic status of a newly-discovered, putative ghost lineage (HX) in the fish genus Hypseleotris to provide perspectives on several important issues not previously explored by other studies on ghost species, but relevant to ongoing discussions about their detection, conservation, and artificial re-creation. Our comprehensive genetic (allozymes, mtDNA) and genomic (SNPs) datasets successfully identified a threatened sexual population of HX in one tiny portion of the extensive distribution displayed by two hemi-clonal HX-containing lineages. We also discuss what confidence should be placed on any assertion that an ancestral species is actually extinct, and how to assess whether any putative sexual ancestor represents a pure remnant, as shown here, or a naturally-occurring resurrection via the crossing of compatible clones or hemi-clones.
... esculentus), which stem from ancient hybridizations between P. ridibundus and P. perezi or P. lessonae, respectively. In central Italy, the endemic P. kl. hispanicus is present, carrying the parental genomes of P. bergeri and a new endemic Eastern-Mediterranean lineage, nowadays extinct in the wild (Dubey and Dufresnes 2018). ...
... esculentus), which stem from ancient hybridizations between P. ridibundus and P. perezi or P. lessonae, respectively. In central Italy, the endemic P. kl. hispanicus is present, carrying the parental genomes of P. bergeri and a new endemic Eastern-Mediterranean lineage, nowadays extinct in the wild (Dubey and Dufresnes 2018). ...
Phtisica marina, originally described by Slabber, 1769 from Netherlands, is one of the most abundant caprellid amphipod species reported from numerous regions around the globe and is primarily associated with fouling communities in harbours. This study chronicles the further spreading out of P. marina into the Indian coastal waters. During a regular coastal survey in Gulf of Kachchh (Northwest coast of India), an established population of P. marina was observed in the subtidal regions of Vadinar and Sikka during April 2017. The caprellid could be a possible alien species in Indian waters as the species met the criteria for exotic taxa. The most possible introductory vectors and pathways are discussed in this study. As this species can survive in the stressed environments of low hydrodynamics and it has opportunistic behaviour, further studies are necessary to reveal its potential impact on local communities.
... esculentus), which stem from ancient hybridizations between P. ridibundus and P. perezi or P. lessonae, respectively. In central Italy, the endemic P. kl. hispanicus is present, carrying the parental genomes of P. bergeri and a new endemic Eastern-Mediterranean lineage, nowadays extinct in the wild (Dubey and Dufresnes 2018). ...
