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Are invasive marsh frogs (Pelophylax ridibundus) replacing the native P. lessonae/P. esculentus hybridogenetic complex in Western Europe? Genetic evidence from a field study

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Abstract

The water-frog L–E system, widespread in Western Europe, comprises the pool frog Pelophylax lessonae and the hybridogenetic edible frog P. esculentus, which originated from hybridization between pool frogs and marsh frogs (P. ridibundus). In P. esculentus, the lessonae (L) genome is eliminated during meiosis and has to be gained anew each generation from a P. lessonae partner, while the ridibundus (R′) genome is transmitted clonally. It therefore accumulates deleterious mutations, so that R′R′ offspring from P. esculentus×P. esculentus crosses are normally unviable. This system is now threatened by invasive P. ridibundus (RR) imported from Eastern Europe and the Balkans. We investigated the genetic interactions between invasive marsh frogs and native water frogs in a Swiss wetland area, and used genetic data collected in the field to validate several components of a recently postulated mechanism of species replacement. We identified neo-ridibundus individuals derived from crosses between invasive ridibundus and native esculentus, as well as newly arisen hybridogenetic esculentus lineages stemming from crosses between invasive ridibundus (RR) and native lessonae (LL). As their ridibundus genomes are likely to carry less deleterious mutations, such lineages are expected to produce viable ridibundus offspring, contributing to species replacement. However, such crosses with invasive ridibundus only occurred at a limited scale; moreover, RR×LL crosses did not induce any introgression from the ridibundus to the lessonae genome. We did not find any ridibundus stemming from crosses between ancient esculentus lineages. Despite several decades of presence on the site, introduced ridibundus individuals only represent 15 % of sampled frogs, and their spatial distribution seems shaped by specific ecological requirements rather than history of colonization. We therefore expect the three taxa to coexist stably in this area.

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Acknowledgments

We thank M. Antoniazza and A. Ghiraldi for sharing their knowledge of the Grande Cariçaie; C. Benjemia, S. Biollay, O. Darbellay, L. Dutoit, F. Goetschi, N. Hazi, A. Jost, H. Lovis, T. Martignier, L. Megali, G. Mottaz, A. Murakozy, M. Podolak, E. Rapin, M. Ribaux, N. Rodrigues, P. Roelli, A. Rogivue, M. Stojiljkovic and Q. Theiler for their help during field work; S. Röthlisberger and N. Pruvost from Uli Reyer’s lab in Zürich for sharing their experience with Pelophylax microsatellites; C. Aletti, C. Berney, C. Dufresnes, R. Savary and R. Sermier for their help in the lab; S. Dubey for his help in phylogenetic analyses; C. Betto-Colliard for discussions. We acknowledge financial support from the Association de la Grande Cariçaie, the School of Biology (University of Lausanne) and the Swiss National Science Foundation (Grant 31003A_129894 to NP). The samples were collected with the authorisation of the veterinary and nature offices of the Canton de Vaud (N°2012-24).

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Authors and Affiliations

  1. Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland

    Julien Leuenberger & Nicolas Perrin

  2. Association de la Grande Cariçaie, Chemin de la Cariçaie 3, 1400, Cheseaux-Noréaz, Switzerland

    Antoine Gander

  3. Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland

    Benedikt R. Schmidt

  4. KARCH, Passage Maximilien-de-Meuron 6, 2000, Neuchâtel, Switzerland

    Benedikt R. Schmidt

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  1. Julien Leuenberger
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Correspondence to Nicolas Perrin.

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10592_2014_585_MOESM2_ESM.docx

Distribution of Pelophylax species among the five sampling sites. Color legend to pie charts: dark blue RR ridibundus, pale blue neo-ridibundus (3_EN_13), dark green ancient R′L esculentus, pale green neo R′L esculentus, red LL lessonae (DOCX 2677 kb)

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Leuenberger, J., Gander, A., Schmidt, B.R. et al. Are invasive marsh frogs (Pelophylax ridibundus) replacing the native P. lessonae/P. esculentus hybridogenetic complex in Western Europe? Genetic evidence from a field study. Conserv Genet 15, 869–878 (2014). https://doi.org/10.1007/s10592-014-0585-0

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