iBet uBet web content aggregator. Adding the entire web to your favor.
iBet uBet web content aggregator. Adding the entire web to your favor.



Link to original content: https://doi.org/10.1023/A:1023346824722
A genetic mechanism of species replacement in European waterfrogs? | Conservation Genetics Skip to main content
Log in

A genetic mechanism of species replacement in European waterfrogs?

  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Introduced Rana ridibunda currentlyreplace the native waterfrogs R. lessonaeand R. esculenta in several areas ofcentral Europe. The unusual reproductive systemin waterfrogs of the Rana esculentacomplex suggests that this replacement may bedriven by a genetic mechanism: Ranaesculenta, a hybrid between R. ridibundaand R. lessonae, eliminates the lessonae genome from the germline and clonallytransmits the ridibunda genome(hybridogenesis). Hybrids form mixedpopulations with R. lessonae (L-E-system)in which they persist by backcrossing with theparental species. Matings between hybrids areunsuccessful, because their ridibundagenomes contain fixed recessive deleteriousmutations. When introduced into a L-E-system,R. ridibunda can mate with both nativetaxa, producing R. ridibunda offspringwith R. esculenta, and R. esculentaoffspring with R. lessonae (primaryhybridizations). If primary hybrids arehybridogenetic, they produce viable R.ridibunda offspring in matings with otherhybrids, because their clonal genomes areunlikely to share the deleterious allelespresent in the ancient clones. Thus, R.ridibunda will increase in the population atthe expense of both native taxa, eventuallyleaving a pure R. ridibunda population.We provide three lines of evidence for thisprocess from a currently invaded population inSwitzerland: (1) Primary hybridizations takeplace, as roughly 10% of hybrids in thepopulation possess ridibunda genomesderived from the introduced frogs. (2)Hybridogenesis occurs in primary hybrids,although at a low frequency. (3) Many hybrid ×hybrid matings in the population indeed produceviable offspring. Hence, the proposed geneticmechanism appears to contribute to the speciesreplacement, although its importance may belimited.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Beerli P (1994) Genetic isolation and Calibration of an Average Protein Clock in Western Palearctic Water Frogs of the Aegean Region. PhD thesis, University of Zürich, Switzerland.

    Google Scholar 

  • Berger L (1967) Embryonal and larval development of F1 generation of green frogs of different combinations. Acta Zool. Cracow, 12, 123–160.

    Google Scholar 

  • Berger L (1968) Morphology of the F1 generation of various crosses within Rana esculenta complex. Acta Zool. Cracow, 13, 301–324.

    Google Scholar 

  • Berger L (1976) Hybrids of B2 generation of European water frogs (Rana esculenta complex). Ann. Zool. (Warszawa), 33, 201–214.

    Google Scholar 

  • Berger L, Uzzell T (1977) Vitality and growth of progeny from different egg size classes of Rana esculenta L. (Amphibia, Salientia). Zool. Poloniae, 26, 291–317.

    Google Scholar 

  • Berger L, Rybacki M, Hotz H (1994) Artificial fertilization of water frogs. Amphibia-Reptilia, 15, 408–413.

    Google Scholar 

  • Berger L, Uzzell T, Hotz H (1994) Postzygotic reproductive isolation between Mendelian species of European water frogs. Zool. Poloniae, 39, 209–242.

    Google Scholar 

  • Binkert J, Borner P, Chen PS (1982) Rana esculenta complex: an experimental analysis of lethality and hybridogenesis. Experientia, 38, 1283–1292.

    Google Scholar 

  • Blankenhorn HJ, Heusser H, Vogel P (1971) Drei Phänotypen von Grünfröschen aus dem Rana esculenta-Komplex in der Schweiz. Rev. Suisse Zool., 78, 1242–247.

    Google Scholar 

  • Bucci S, Ragghianti M, Mancino G, Berger L, Hotz H, Uzzell T (1990) Lampbrush and mitotic chromosomes of the hemiclonally reproducing hybrid Rana esculenta and its parental species. J. Exp. Zool., 255, 37–56.

    Google Scholar 

  • Carmona JA, Sanjur OI, Doadrio I, Machordom A, Vrijenhoek RC (1997) Hybridogenetic reproduction and maternal ancestry of polyploid Iberian fish: The Tropidophoxinellus alburnoides complex. Genetics, 146, 983–993.

    Google Scholar 

  • Gosner N (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183–190.

    Google Scholar 

  • Graf JD, Müller WP (1979) Experimental gynogenesis provides evidence of hybridogenetic reproduction in the Rana esculenta complex. Experientia, 35, 1574–1576.

    Google Scholar 

  • Graf JD, Polls Pelaz M (1989) Evolutionary genetics of the Rana esculenta complex. In: Evolution and Ecology of Unisexual Vertebrates (eds. Dawley RM, Bogart JP), pp. 298–302. The New York State Museum Bulletin 466, Albany, USA.

    Google Scholar 

  • Grossenbacher K (1988) Verbreitungsatlas der Amphibien der Schweiz. Doc. Faun. Helvetiae, 7, 1–207.

    Google Scholar 

  • Hebert PDN, Beaton MJ (1993) Methodologies for Allozyme Analysis Using Cellulose Acetate Electrophoresis. Helena Laboratories, Beaumont, TX.

    Google Scholar 

  • Hellriegel B, Reyer HU (2000) Factors influencing the composition of mixed populations of a hemiclonal hybrid and its sexual host. J. Evol. Biol., 13, 906–918.

    Google Scholar 

  • Heusser H, Blankenhorn HJ (1973) Crowding-Experimente mit Kaulquappen aus homo-und heterotypischen Kreuzungen der Phänotypen esculenta, lessonae und ridibunda (Rana esculenta-Komplex, Anura, Amphibia). Rev. Suisse Zool., 80, 543–569.

    Google Scholar 

  • Hofer-Polit D (1998) Aussterben von Rana lessonae und Rana esculenta durch die Ausbreitung von Rana ridibunda. Elaphe, 6, 79–80.

    Google Scholar 

  • Holenweg Peter AK (2001) Dispersal rates and distances in adult water frogs, Rana lessonae, R. ridibunda, and their hybridogenetic associate R. esculenta. Herpetologica, 57, 449–460.

    Google Scholar 

  • Holenweg Peter AK, Reyer HU, Abt Tietje G (2002) Species and sex ratio differences in mixed populations of hybridogenetic water frogs: The influence of pond features. Ecoscience, 9, 1–11.

    Google Scholar 

  • Hotz H (1983) Genic Diversity Among Water frog Genomes Inherited With and Without Recombination. PhD thesis, University of Zürich, Switzerland.

    Google Scholar 

  • Hotz H, Mancino G, Bucci-Innocenti S, Ragghianti M, Berger L, Uzzell T (1985) Rana ridibunda varies geographically in inducing clonal gametogenesis in interspecies hybrids. J. Exp. Zool., 236, 199–210.

    Google Scholar 

  • Hotz H, Uzzell T, Berger L (1997) Linkage groups of proteincoding genes in western Palearctic water frogs reveal extensive evolutionary conservation. Genetics, 147, 255–270.

    Google Scholar 

  • Hotz H, Semlitsch RD, Gutmann E, Guex GD, Beerli P (1999) Spontaneous heterosis for larval life-history traits of hemiclonal frog hybrids. Proc. Natl. Acad. Sci. USA, 96, 2171–2176.

    Google Scholar 

  • Johnson PTJ, Lunde KB, Ritchie EG, Launer AE (1999) The effect of trematode infection on amphibian limb development and survivorship. Science, 284, 802–804.

    Google Scholar 

  • Johnson PTJ, Lunde KB, Haight RW, Bowerman J, Blaustein AR (2001) Riebeiroia ondatrae (Trematoda: Digenea) infection induces severe limb malformations in western toads (Bufo boreas). Can. J. Zool., 79, 370–379.

    Google Scholar 

  • Leslie JF, Vrijenhoek RC (1980) Consideration of Muller's ratchet mechanism through studies of genetic linkage and genomic compatibilities in clonally reproducing Poeciliopsis. Evolution, 34, 1105–1115.

    Google Scholar 

  • Lynch M (1984) Destabilizing hybridization, general-purpose genotypes and geographic parthenogenesis. Q. Rev. Biol., 59, 257–290.

    Google Scholar 

  • Manchester SJ, Bullock JM (2000) The impacts of non-native species on UK biodiversity and the effectiveness of control. J. Appl. Ecol., 37, 845–864.

    Google Scholar 

  • Mantovani B, Scali V (1997) Hybridogenesis and androgenesis in the stick insect Bacillus rossius-grandii benazzii (Insecta Phasmatodea). Evolution, 46, 783–796.

    Google Scholar 

  • Marchesi P, Fournier J, Rey A (1999) Etat des populations de “grenouilles vertes” Rana lessonae, Rana kl. esculenta du Bois de Finges (Salquenen, VS). Bull. Murithienne, 117, 13–22.

    Google Scholar 

  • Ogielska M (1994) Rana esculenta developmental syndrome: fates of abnormal embryos from the first cleavage until spontaneous death. Zool. Poloniae, 39, 447–459.

    Google Scholar 

  • Pimm SL (1987) The snake that ate Guam. Trends Ecol. Evol., 2, 293–295.

    Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Ann. Rev. Ecol. Syst., 27, 83–109.

    Google Scholar 

  • Schultz RJ (1969) Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates. Am. Nat., 103, 605–619.

    Google Scholar 

  • Schultz RJ (1973) Unisexual fish: Laboratory synthesis of a “species”. Science, 179, 180–181.

    Google Scholar 

  • Semlitsch RD, Reyer HU (1992) Performance of tadpoles from the hybridogenetic Rana esculenta complex: Interactions with pond drying and interspecific competition. Evolution, 46, 665–676.

    Google Scholar 

  • Söderbäck B (1995) Replacement of the native crayfish Astacus astacus by the introduced species Pacifastacus leniusculus in a Swedish lake: Possible causes and mechanisms. Freshwater Biol., 33, 291–304.

    Google Scholar 

  • Som C, Anholt BR, Reyer HU (2000) The effect of assortative mating on the coexistence of a hybridogenetic waterfrog and its sexual host. Am. Nat., 156, 34–46.

    Google Scholar 

  • Tunner HG (1974) Die klonale Struktur einer Wasserfrosch-Poplation. Z. Zool. Syst. Evol.-Forsch., 12, 309–314.

    Google Scholar 

  • Tunner HG, Heppich S (1981) Premeiotic genome exclusion during oogenesis in the common edible frog, Rana esculenta. Naturwissenschaften, 68, 207–208.

    Google Scholar 

  • Uzzell T, Berger L (1975) Electrophoretic phenotypes of Rana ridibunda, Rana lessonae, and their hybridogenetic associate, Rana esculenta. Proc. Acad. Nat. Sci. Phila., 127, 13–24.

    Google Scholar 

  • Uzzell T, Hotz H, Berger L (1980) Genome exclusion in gametogenesis by an interspecific Rana hybrid: Evidence from electrophoresis of individual oocytes. J. Exp. Zool., 214, 251–259.

    Google Scholar 

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

    Google Scholar 

  • Vorburger C (2001b) Heterozygous fitness effects of clonally transmitted genomes in waterfrogs. J. Evol. Biol., 14, 602–610.

    Google Scholar 

  • Vorburger C, Ribi G (1999) Aggression and competition for shelter between a native and an introduced crayfish in Europe. Freshwater Biol., 42, 111–119.

    Google Scholar 

  • Vrijenhoek RC (1989) Genetic and ecological constraints on the origins and establishment of unisexual vertebrates. In: Evolution and Ecology of Unisexual Vertebrates (eds. Dawley RM, Bogart JP), pp. 24–31. The New York State Museum Bulletin 466, Albany, New York.

    Google Scholar 

  • Wagner E, Ogielska M (1993) Oogenesis and ovary development in the natural hybridogenetic water frog, Rana esculenta L. II. After metamorphosis until adults. Zool. Jahrb. Allg. Zool., 97, 369–382.

    Google Scholar 

  • Wetherington JD, Kotora KE, Vrijenhoek RC (1987) A test of the spontaneous heterosis hypothesis for unisexual vertebrates. Evolution, 41, 721–731.

    Google Scholar 

  • Williamson M (1996) Biological Invasions. Chapman and Hall, London.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Heinz-Ulrich Reyer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vorburger, C., Reyer, HU. A genetic mechanism of species replacement in European waterfrogs?. Conservation Genetics 4, 141–155 (2003). https://doi.org/10.1023/A:1023346824722

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1023346824722

Navigation