Invasion genetics of marsh frogs (Pelophylax ridibundus sensu lato) in Switzerland

Dufresnes, Christophe; Leuenberger, Julien; Amrhein, Valentin; Bühler, Christoph; Thiébaud, Jacques; Bohnenstengel, Thierry; Dubey, Sylvain

doi:10.1093/biolinnean/blx140

Cited by 39 publications

(39 citation statements)

References 18 publications

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“…First, the closely related T. cristatus and T. carnifex were reliably differentiated despite that our reference database was restricted to sequences from another T. carnifex clade (clade S introduced in the Geneva Basin; Dufresnes et al, 2016), deeply diverged from the Basel invaders (clade C). Note also that the technology discriminated and detected another notorious group of aliens: the marsh frogs (Pelophylax ridibundus sensu lato), which are invading the Swiss plateau (Dufresnes et al, 2018). Second, populations from both the native and invasive species could be efficiently mapped, as expected given the high detection probability of eDNA (up to 0.97) compared to traditional field surveys (Smart, Tingley, Weeks, van Rooyen, & McCarthy, 2015;Valentini et al, 2016).…”

Section: Edna For the Surveillance Of Aquatic Invasive Speciesmentioning

confidence: 76%

Early detection and spatial monitoring of an emerging biological invasion by population genetics and environmental DNA metabarcoding

Dufresnes

Déjean

Zumbach

et al. 2019

Conservat Sci and Prac

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Rapid management responses against invasive species soon after their establishment are the most efficient way to limit their biological and economic impacts. Early detection and reliable monitoring is however challenging when cryptic taxa are involved. Here we show how environmental DNA (eDNA) metabarcoding of water samples efficiently unveiled an emerging invasion of Italian crested newts (Triturus carnifex), one of the most successful amphibian invaders in Europe. We compared and validated an eDNA survey by multilocus population genetics of wild-caught individuals. Both approaches consistently mapped a localized T. carnifex invasion in northwestern Switzerland, most likely following imports from the Italian Po Plain. We found evidence of gene flow with the indigenous and endangered Triturus cristatus in nearby populations, suggesting a potential expansion. Yet the currently small invasive range should be efficiently contained by future eradication programs. This textbook case emphasizes the implementation of eDNA metabarcoding to screen aquatic communities for exotic species, from which targeted studies can be designed on emerging biological invasions.

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Section: Edna For the Surveillance Of Aquatic Invasive Speciesmentioning

confidence: 76%

Early detection and spatial monitoring of an emerging biological invasion by population genetics and environmental DNA metabarcoding

Dufresnes

Déjean

Zumbach

et al. 2019

Conservat Sci and Prac

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“…Second, all five possessed local P. lessonae mitotypes, while parental P. ridibundus normally conserve their maternal lineages throughout hybridogenesis, because of mating preferences: in mixed populations, the large P. ridibundus females are preferentially chosen by the males of the other smaller species, rarely the other way around (e.g. [26]). Third, the nuclear diversity of these females was extremely low (H o = 0.02), as expected for hemiclonal RR individuals.…”

Section: Discussionmentioning

confidence: 99%

“…Because of the high diversity of breeding systems, clonal genomes, sex-determination and genetic variation in this frog complex [21, 22], comparative analyses of closely-related groups of populations are of prime interest, since their biogeographic history should not be a confounding factor. In addition, many European populations have been largely compromised by multiple invasions of Pelophylax alien species, resulting in genetic pollution and/or disruption of their hybridogenetic complexes [23–26].…”

Section: Introductionmentioning

confidence: 99%

Population genomics of an exceptional hybridogenetic system of Pelophylax water frogs

Dubey

Maddalena²,

Bonny

et al. 2019

BMC Evol Biol

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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. Electronic supplementary material The online version of this article (10.1186/s12862-019-1482-4) contains supplementary material, which is available to authorized users.

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“…3). Two R-mtDNA haplotypes were found exclusively in P. ridibundus: RID01 and RID08 (following Dufresnes et al, 2018), in fish ponds in which this species predominated (sites 6, 7, 8) and in one LER population (site 5). Both are widespread across Central Europe and have recently spread into Switzerland and France.…”

Section: Diversity Of Cytb Haplotypesmentioning

confidence: 95%

“…Conversely, ancient as well as recent human-mediated introductions Department of Comparative Anatomy, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland have led to multiple range expansions and invasions of Pelophylax spp. native to Eastern Europe, the Balkans, Anatolia and Italy (Pagano et al, 2003;Zeisset and Beebee, 2003;Schmeller et al, 2007;Holsbeek et al, 2008;Leuenberger et al, 2014;Dufresnes et al, 2017a, b;Kolenda et al, 2017;Dufresnes et al, 2018;Dufresnes and Dubey, 2020). Habitat conversion seems to have also contributed to the expansion of some water frog species.…”

Section: Introductionmentioning

confidence: 99%

Recent shifts in taxonomic compositions of water frog populations (Anura: Pelophylax) inhabiting fish ponds in southern Poland

Jośko

Pabijan

2020

Amphib.-Reptilia

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In Central Europe, water frog species coexist in assemblages consisting of Pelophylax lessonae, P. ridibundus and their hybridogenetic hybrid, P. esculentus. Population compositions are poorly understood, partly because of difficulties in distinguishing hybrids from parentals by means of morphology alone. Environmental change and human-mediated, cryptic introductions of non-native water frog species have modified local assemblages. In this contribution we examined the structure of nine water frog populations inhabiting mostly large fish ponds in the Upper Vistula river valley of southern Poland using morphology and PCR-based genotyping of single loci in the nuclear and mitochondrial genomes. We found four different water frog population compositions: two with only P. ridibundus, one composed of P. lessonae and P. esculentus, three with P. ridibundus and P. esculentus, and three containing all three water frog taxa. Historical data show that the area was previously inhabited by lessonae-esculentus populations. We propose that both ecological and genetic replacement by expanding P. ridibundus may have contributed to the decline of the former. Overall, 18% of P. ridibundus frogs contained introgressed P. lessonae mtDNA, however, the frequency of introgressants was most pronounced in populations with a high proportion of P. esculentus. Exotic water frogs were not detected in the study area. Our results bear significance for water frog population dynamics and conservation in Central Europe and highlight the importance of long-term monitoring for the detection of changes in population composition in these amphibians.

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Invasion genetics of marsh frogs (Pelophylax ridibundus sensu lato) in Switzerland

Cited by 39 publications

References 18 publications

Early detection and spatial monitoring of an emerging biological invasion by population genetics and environmental DNA metabarcoding

Early detection and spatial monitoring of an emerging biological invasion by population genetics and environmental DNA metabarcoding

Population genomics of an exceptional hybridogenetic system of Pelophylax water frogs

Recent shifts in taxonomic compositions of water frog populations (Anura: Pelophylax) inhabiting fish ponds in southern Poland

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