Hybridogenesis in Water Frogs

Abstract

Several water frogs from the genus Pelophylax have a hybrid origin and perpetuate by hybridogenesis, a peculiar mode of reproduction ruled by complex phenomena such as clonality and polyploidy, and which can constitute a transient stage towards the formation of novel species. Different kinds of hybridogenetic complexes have been documented throughout Europe, and a tremendous diversity of breeding systems allows their maintenance in space and time, each with its own subtilities to bypass the numerous challenges posed by a semi‚Äźsexual life cycle. The other side of the coin is that hybridogenesis can boost the invasive potential of introduced frogs by altering the fragile dynamics of these natural populations, hence illustrating the thin line that separates ephemeral hybrid forms versus perennial reticulate taxa.

Key Concepts

  • Hybrids between diverged species can avoid sterility by abandoning sexual reproduction.
  • Hybridogenetic hybrids typically transmit a single, clonal genome to offspring.
  • Clonality promotes genetic decay and the need to breed with a sexual species.
  • Reliance on a sexual host can be bypassed by polyploidy.
  • Clonal genomes have various opportunities to recombine in populations.
  • Genetic integrity, ecomorphological differentiation and sexual independence of hybridogenetic hybrids may represent steps towards hybrid speciation.
  • Hybridogenetic systems can collapse due to invasive parental species.

Keywords: edible frog; hemiclone; hybridisation; hybridogenesis; hybrid speciation; marsh frog; Pelophylax; polyploidy; pool frog

Figure 1. Steps of genome elimination in Pelophylax hybridogens, exemplified here by a L‐eliminating L individual obtained from a P. fortis (FF) × P. lessonae (LL) cross. When gonads maturate (during tadpole development), one selected genome (here the L) is progressively eliminated from the germline and degraded by autophagy. The remaining F genome is then endoreplicated, and subsequent meiosis only produces gametes with that genome, which is thus transmitted in a clonal manner (noted). Source: Adapted from Dedukh D, Riumin S, Chmielewska M et al. Micronuclei in germ cells of hybrid frogs from Pelophylax esculentus complex contain gradually eliminated chromosomes. Scientific Reports 10: 8720.
Figure 2. (a) Primary hybridisation scheme (L‐E‐F) and breeding systems enabling the maintenance of LF hybridogens (‘P. esculentus’) through backcrossing with P. l. lessonae (L‐E systems) and P. fortis (F‐E systems). The eliminated genomes (−) and the clonal genomes ([]) are shown. (b) Maintenance in all‐hybrid populations with triploids, obtained by the production of diploid gametes (schematised eggs and sperm). In the well‐studied Baltic populations, LF eggs develop in LLF or LFF individuals upon fertilisation by L and F sperm, respectively. These triploids recombine the genome in double dose (labelled L‐rec and F‐rec). Additional genotypes are produced but do not actively contribute to the populations, e.g. LL and FF individuals clones are not fit. Note that triploids are also found in some L‐E and F‐E systems from central and eastern Europe.
Figure 3. Native distribution ranges of Pelophylax taxa involved in hybridogenetic complexes, and breeding systems of the LF hybridogens (‘P. esculentus’), compiled from a literature search spanning 702 localities taken from 101 different publications. The presence of polyploids is reported, when documented. Note that the diversity of western European ranges has been modified by introductions and biological invasions (not shown): P. l. lessonae is admixed by P. l. bergeri (Dufresnes and Dubey, ), and P. fortis is now found all the way through the Atlantic and Mediterranean coasts (Pagano et al., ). Photo: LF hybridogen (credit: CD). Source: Compilation by the authors.
Figure 4. Maintenance of the P. perezi / fortis hybridogens in France (‘P. grafi’, PF) and P. l. bergeri / fortis hybridogens in Italy (BF). Original crosses are unclear, as they may involve either the parental P. fortis (FF), or the L hybridogen P. esculentus. In both cases, the F genome is hemiclonally transmitted, and hybrids rely on the associated sexual parent (P. perezi and P. l. bergeri).
Figure 5. The water frogs involved in hybridogenesis, with parental species on the left, and associated hybridogens on the right (arranged as in the top‐right labels). Photo credit as follows: P. fortis: M. Denoël; P. l. lessonae: CD; P. l. bergeri: S. Dubey; P. perezi: CD; LF hybrid: CD; BF hybrid: W. Beukema; PF hybrid: CD.
close

References

Abt G and Reyer H‐U (1993) Mate choice and fitness in a hybrid frog: Rana esculenta females prefer Rana lessonae males over their own. Behavioral Ecology and Sociobiology 32: 221–228.

Alves MJ, Coelho MM and Collares‐Pereira MJ (1998) Diversity in the reproductive modes of females of the Rutilus alburnoides complex (Teleostei, Cyprinidae): a way to avoid the genetic constraints of uniparentalism. Molecular Biology and Evolution 15: 1233–1242.

Berger L (1967) Embryonal and larval development of F1 generation of green frogs' different combinations. Acta Zoologica Cracoviensia 12: 123–160.

Berger L (1968) Morphology of the F1 generation of various crosses within Rana esculenta complex. Acta Zoologica Cracoviensia 13: 301–324.

Berger L (1970) Sex ratio in the F1 progeny within forms of Rana esculenta complex. Genetica Polonica 12: 87–101.

Berger L, Uzzell T and Hotz H (1988) Sex determination and sex ratios in western Palearctic water frogs: XX and XY female hybrids in the Pannonian Basin? Proceedings of the Academy of Natural Sciences of Philadelphia 140: 220–239.

Biriuk O, Shabanov DA and Korshunov AV (2016) Gamete production patterns and mating systems in water frogs of the hybridogenetic Pelophylax esculentus complex in north‐eastern Ukraine. Journal of Zoological Systematics and Evolutionary Research 54: 215–225.

Chmielewska M, Dedukh D and Haczkiewicz K (2018) The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus. Scientific Reports 8: 7870.

Christiansen DF (2009) Gamete types, sex determination and stable equilibria of all‐hybrid populations of diploid and triploid edible frogs (Pelophylax esculentus). BMC Evolutionary Biology 9: 135.

Christiansen DG and Reyer H‐U (2009) From clonal to sexual hybrids: genetic recombination via triploids in all‐hybrid populations of water frogs. Evolution 63: 1754–1768.

Crochet P‐A, Dubois A, Ohler A, et al. (1995) Rana (Pelophylax) ridibunda Pallas, 1771, Rana (Pelophylax) perezi Seoane, 1885 and their associated klepton (Amphibia, Anura): morphological diagnoses and description of a new taxon. Bulletin du Muséum National d'Histoire Naturelle 17: 11–30.

Dedukh D, Litvinchuk S, Rosanov J, et al. (2017) Mutual maintenance of di‐ and triploid Pelophylax esculentus hybrids in R‐E systems: results from artificial crossings experiment. BMC Evolutionary Biology 17: 220.

Dedukh D, Litvinchuk J, Svinin A, et al. (2019) Variation in hybridogenetic hybrid emergence between populations of water frogs from the Pelophylax esuclentus complex. PLoS ONE 14: e0224759.

Dedukh D, Riumin S, Chmielewska M, et al. (2020) Micronuclei in germ cells of hybrid frogs from Pelophylax esculentus complex contain gradually eliminated chromosomes. Scientific Reports 10: 8720.

Dubey S, Maddalena T, Bonny L, et al. (2019) Population genomics of an exceptional hybridogenetic system of Pelophylax water frogs. BMC Evolutionary Biology 19: 164.

Dufresnes C, Denoël M, Di Santo L, et al. (2017) Multiple uprising invasions of Pelophylax water frogs, potentially inducing a new hybridogenetic complex. Scientific Reports 7: 6506.

Dufresnes C and Dubey S (2020) Invasion genomics supports an old hybrid swarm of pool frogs in Western Europe. Biological Invasions 22: 205–210.

Graf J‐D, Karch F and Moreillon M‐C (1977) Biochemical variation in the Rana esculenta complex: a new hybrid form related to Rana perezi and Rana ridibunda. Experientia 33: 1582–1584.

Graf J‐D and Müller WP (1979) Experimental gynogenesis provide evidence of hybridogenetic reproduction in the Rana esculenta complex. Experientia 35: 1574–1576.

Graf J‐D and Polls Pelaz M (1989) Evolutionary genetics of the Rana esculenta complex. In: Dawley RM and Bogart JP (eds) Evolution and Ecology of Unisexual Vertebrates. New York State Museum Bulletin 466, pp 289–302. New York State Museum: Albany, NY.

Günther R, Uzzell T and Berger L (1979) Inheritance patterns in triploid Rana “esculenta” (Amphibia, Salientia). Mitteilungen aus dem Zoologischen Museum in Berlin 55: 35–57.

Günther R (1991) European waterfrogs (Anura, Ranidae) and the biospecies concept. Mitteilungen aus dem Zoologischen Museum in Berlin 67: 39–53.

Hoffmann A, Plötner J, Pruvost NB, et al. (2015) Genetic diversity and distribution patterns of diploid and polyploid hybrid water frog populations (Pelophylax esculentus) across Europe. Molecular Ecology 24: 4371–4391.

Holsbeek G and Jooris R (2010) Potential impact of genome exclusion by alien species in the hybridogenetic water frogs (Pelophylax esculentus complex). Biological Invasions 123: 1–13.

Hotz H, Mancino G, Bucci‐Innocenti S, et al. (1985) Rana ridibunda varies geographically in inducing clonal gametogenesis in interspecies hybrids. Journal of Experimental Zoology 236: 199–210.

Hotz H, Semlitsch RD, Gutmann E, et al. (1999) Spontaneous heterosis in larval life‐history traits of hemiclonal frog hybrids. Proceedings of the National Academy of Sciences of the United States of America 96: 2171–2176.

Kierzkowski P, Paśko L, Rybacki M, et al. (2011) Genome dosage effect and hybrid morphology – the case of the hybridogenetic water frogs of the Pelophylax esculentus complex. Annales Zoologici Fennici 48: 56–66.

Luquet E, Vorburger C, Hervant F, et al. (2011) Invasiveness of an introduced species: the role of hybridization and ecological constraints. Biological Invasions 13: 1901–1915.

Mikulíček P, Kautman M, Kautman J, et al. (2015) Mode of hybridogenesis and habitat preferences influence population composition of water frogs (Pelophylax esculentus complex, Anura: Ranidae) in a region of sympatric occurrence (western Slovakia). Journal of Zoological Systematics and Evolutionary Research 53: 124–132.

Ogielska M (1994) Nucleus‐like bodies in gonial cells of Rana esculenta (Amphibia, Anura) tadpoles – a putative way of chromosome elimination. Zoologica Poloniae 39: 461–474.

Pagano A, Lodé T and Crochet P‐A (2001) New contact zone and assemblages among water frogs of Southern France. Journal of Zoological Systematics and Evolutionary Research 39: 63–67.

Plötner J and Ohst T (2001) New hypotheses on the systematics of the western Palearctic water frog complex (Anura, Ranidae). Mitteilungen aus dem Zoologischen Museum in Berlin 77: 5–21.

Plötner J (2005) Die Westpaläarktischen Wasserfrösche: Von Märtyrern der Wissenschaft zur Biologischen Sensation. Laurenti Verlag: Bielefeld.

Plötner J, Uzzell T, Beerli P, et al. (2008) Widespread unidirectional transfer of mitochondrial DNA: a case in western Palaearctic water frogs. Journal of Evolutionary Biology 21: 668–681.

Pruvost NBM, Hoffmann A and Reyer H‐U (2013a) Gamete production patterns, ploidy, and population genetics reveal evolutionary significant units in hybrid water frogs (Pelophylax esculentus). Ecology and Evolution 3: 2933–2946.

Pruvost NBM, Hollinger D and Reyer H‐U (2013b) Genotype‐temperature interactions on larval performance shape population structure in hybridogenetic water frogs (Pelophylax esculentus complex). Functional Ecology 27: 459–471.

Reyer H‐U, Arioli‐Jakob C and Arioli M (2015) Post‐zygotic selection against parental genotypes during larval development maintains all‐hybrid populations of the frog Pelophylax esculentus. BMC Evolutionary Biology 15: 131.

Schempp W and Schmid M (1981) Chromosome banding in Amphibia. VI. BrdU‐replication patterns in Anura and demonstration of XX‐XY sex chromosomes in Rana esculenta. Chromosoma 83: 697–710.

Schultz RJ (1969) Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates. American Naturalist 103: 605–619.

Som C, Anholt BR and Reyer H‐U (2000) The effect of assortative mating on the coexistence of hybridogenetic waterfrog and its sexual host. American Naturalist 156: 34–46.

Som C and Reyer H‐U (2006) Variation in sex ratio and evolutionary rate of hemiclonal Rana esculenta populations. Evolutionary Ecology 20: 159–172.

Tunner HG (1974) Die klonale Struktur einer Wasserfroschpopulation. Zeitschrift fur Zoologische Systematik und Evolutionsforschung 12: 309–314.

Tunner HG and Heppich‐Tunner S (1991) Genome exclusion and two strategies of chromosome duplication in oogenesis of a hybrid frog. Naturwissenschaften 78: 32–34.

Uzzell T and Berger L (1975) Eletrophoretic phenotypes of Rana ridibunda, Rana lessonae, and their hybridogenetic associate, Rana esculenta. Proceedings of the Academy of Natural Sciences of Philadelphia 127: 13–24.

Uzzell T, Günther R and Berger L (1977) Rana ridibunda and Rana esculenta: a leaky hybridogenetic system (Amphibia Salientia). Proceedings of the Academy of Natural Sciences of Philadelphia 128: 147–171.

Uzzell T and Hotz H (1979) Electrophoretic and morphological evidence for two forms of green frogs (Rana esculenta complex) in peninsular Italy (Amphibia, Salientia). Mitteilungen Aus dem Zoologischen Museum in Berlin 55: 13–27.

Vinogradov AE, Borkin LJ, Günther R, et al. (1990) Genome elimination in diploid and triploid Rana esculenta males: cytological evidence from DNA flow cytometry. Genome 33: 619–627.

Vorburger C (2001a) Fixation of deleterious mutations in clonal lineages: evidence from hybridogenetic frogs. Evolution 55: 2319–2332.

Vorburger C (2001b) Non‐hybrid offspring from matings between hemiclonal hybrid waterfrogs suggest occasional recombination between clonal genomes. Ecology Letters 4: 628–636.

Zaleśna A, Choleva L, Ogielska M, et al. (2011) Evidence for integrity of parental genomes in the diploid hybridogenetic water frog Pelophylax esculentus by genomic in situ hybridization. Cytogenetic and Genome Research 134: 206–212.

Further Reading

Avise JC (2008) Clonality: the Genetics, Ecology, and Evolution of Sexual Abstinence in Vertebrate Animals. Oxford University Press: Oxford.

Beukeboom L and Perrin N (2014) The Evolution of Sex Determination. Oxford University Press: Oxford.

Chapman MA and Burke JM (2007) Genetic divergence and hybrid speciation. Evolution 61: 1773–1780.

Choleva L, Janko K, De Gelas K, et al. (2012) Synthesis of clonality and polyploidy in vertebrate animals by hybridization between two sexual species. Evolution 66: 2191–2203.

Coyne JA and Orr HA (2004) Speciation. Sinauer Associates: Sunderland, MA.

Cunha C, Doadrio I and Coelho MM (2008) Speciation towards tetraploidization after intermediate processes of non‐sexual reproduction. Philosophical Transactions of the Royal Society B 363: 2921–2929.

Mallet J (2008) Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philosophical Transactions of the Royal Society of London B: Biological Sciences 363: 2971–2986.

Ogielska M (2009) Reproduction of Amphibians. Biological Systems in Vertebrates. Science Publishers: Enfield, NH.

Schmid M, Evans BJ and Bogart JP (2015) Polyploidy in amphibia. Cytogenetics and Genome Research 145: 315–330.

Schön I, Martens K and van Dijk P (2009) Lost Sex. The Evolutionary Biology of Parthenogenesis. Springer: Dordrecht.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Dufresnes, Christophe, and Mazepa, Glib(Dec 2020) Hybridogenesis in Water Frogs. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029090]