Biological Invasions

, 12:1 | Cite as

Potential impact of genome exclusion by alien species in the hybridogenetic water frogs (Pelophylax esculentus complex)

  • G. HolsbeekEmail author
  • R. Jooris
Perspectives and Paradigms


Globalization and increasing human impact on natural aquatic systems have facilitated the movement of species and the establishment of nonindigenous species enhancing hybridisation opportunities between naturally allopatric species. In this review, we focus on a special case of natural hybrid speciation and the consequences of recent anthropogenic hybridisation in the water frog complex (Pelophylax esculentus complex), which consists of two parental species, Pelophylax lessonae and Pelophylax ridibundus and a hybrid taxon. The hybrid water frogs reproduce hybridogenetically and eliminate the genome of the syntopic water frog species. Although the actual cause triggering chromosome exclusion remains elusive, it has been proposed that chromosome elimination takes place prior to meiosis and may involve enzymatic degradation of the discarded genome. Translocations of water frogs in Western Europe have become frequent the last decade leading to rapid expansion of the range of the marsh frog P. ridibundus. Subsequent hybridisation of the exotic P. ridibundus may dramatically affect the viability and maintenance of hybrid water frog populations throughout Europe. Interestingly, the impact of this introduced species may differ depending on their geographic origin, which defines the ability to induce genome elimination. This may result in fertile or sterile hybrids, making global conservation guidelines challenging. We predict a severe genetic and ecological impact of nonindigenous P. ridibundus prompting for strict conservation measures to reduce species translocations and for studies on the geographic origin of exotic frog species.


European water frogs Hybrid complex Hybridisation Pelophylax ridibundus Translocations 



The authors thank L. De Meester whose input improved this manuscript to a great extent, and G. Maes, F. Bossuyt and F. Volckaert for providing valuable comments on earlier drafts. We thank J. Mergeay for skilful graphical assistance. GH enjoys a Ph.D. grant of the Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen).


  1. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613. doi: 10.1016/S0169-5347(01)02290-X CrossRefGoogle Scholar
  2. Arano B, Llorente G, Garcia-Paris M, Herrero P (1995) Species translocation menaces iberian waterfrogs. Conserv Biol 9:196–198. doi: 10.1046/j.1523-1739.1995.09010196.x CrossRefGoogle Scholar
  3. Arnold ML (2004) Natural hybridization and the evolution of domesticated, pest and disease organisms. Mol Ecol 13:997–1007. doi: 10.1111/j.1365-294X.2004.02145.x CrossRefPubMedGoogle Scholar
  4. Berger L (1967) Embryonal and larval development of F1 generation of green frogs of different combinations. Acta Zool Cracov 12:123–160Google Scholar
  5. Berger L (1970) Some characteristics of the crosses within Rana esculenta complex in postlarval development. Ann Zool 27:373–416Google Scholar
  6. Berger L (1973) Some characteristics of backcrosses within forms of Rana esculenta complex. Genet Pol 14:413–430Google Scholar
  7. Berger L (1988) On the origin of genetic systems in European water frog hybrids. Zool Pol 35:5–32Google Scholar
  8. Binkert J, Borner P, Chen PS (1982) Rana esculenta complex: an experimental analysis of lethality and hybridogenesis. Cell Mol Life Sci 38:1283CrossRefGoogle Scholar
  9. Christiansen DG, Fog K, Pedersen BV, Boomsma JJ (2005) Reproduction and hybrid load in all-hybrid populations of Rana esculenta water frog in Denmark. Evol Int J Org Evol 59:1348–1361Google Scholar
  10. Dowling TE, Secor CL (1997) The role of hybridization and introgression in the diversification of animals. Annu Rev Ecol Syst 28:593–619. doi: 10.1146/annurev.ecolsys.28.1.593 CrossRefGoogle Scholar
  11. Dubois A (1992) Notes sur la classification des Ranidae (Amphibiens, Anoures). Bull Mens Soc Linn Lyon 61:305–352Google Scholar
  12. Dubois A, Günther R (1982) Klepton and synklepton: two new evolutionary systematics categories in zoology. Zool Jahrb Syst 109:290–305Google Scholar
  13. Ellstrand N, Schierenbeck K (2006) Hybridization as a stimulus for the evolution of invasiveness in plants? Euphytica 148:35–46. doi: 10.1007/s10681-006-5939-3 CrossRefGoogle Scholar
  14. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. doi: 10.1146/annurev.ecolsys.34.011802.132419 CrossRefGoogle Scholar
  15. Forester DJ, Machlist GE (1996) Modeling human factors that affect the loss of biodiversity. Conserv Biol 10:1253–1263. doi: 10.1046/j.1523-1739.1996.10041253.x CrossRefGoogle Scholar
  16. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, p 640Google Scholar
  17. Frost DR, Grant T, Faivovich J, Bain RH, Raxworthy CJ, Wheeler W (2006) The amphibian tree of life. Bull Am Mus Nat Hist 297:1–370. doi: 10.1206/0003-0090(2006)297[0001:TATOL]2.0.CO;2 CrossRefGoogle Scholar
  18. Graf JD, Polls Pelaz M (1989) Evolutionary genetics of Rana esculenta complex. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. The New York State Museum Bulletin, Albany, pp 298–302Google Scholar
  19. Graf JD, Karch J, Moreillon MC (1977) Biochemical variation in the Rana esculenta complex: a new hybrid form related to Rana perezi and Rana ridibunda. Experientia 33:1582–1584. doi: 10.1007/BF01934010 CrossRefPubMedGoogle Scholar
  20. Grant PR, Grant BR (1992) Demography and the genetically effective sizes of two populations of Darwin’s finches. Evol Int J Org Evol 73:766–784Google Scholar
  21. Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711. doi: 10.1126/science.1070315 CrossRefPubMedGoogle Scholar
  22. Grossenbacher K (1988) Verbreitung der wasserfrösche in der schweiz. In: Günther R, Klewen R (eds) Beträge zur biologie und bibliographie (1960–1987) der europäischen wasserfröshe. Jahrbuch für Feldherpetologie, DuisburgGoogle Scholar
  23. Guerrini F, Bucci S, Ragghianti M, Mancino G, Hotz H, Uzzell T et al (1997) Genomes of two water frog species resist germ line exclusion in interspecies hybrids. J Exp Zool 279:163–176. doi: 10.1002/(SICI)1097-010X(19971001)279:2<163::AID-JEZ7>3.0.CO;2-M CrossRefPubMedGoogle Scholar
  24. Guex G-D, Hotz H, Semlitsch RD (2002) Deleterious alleles and differential viability in progeny of natural hemiclonal frogs. Evol Int J Org Evol 56:1036–1044Google Scholar
  25. Günther R, Uzzell T, Berger L (1979) Inheritance patterns in triploid Rana “esculenta” (Amphibia, Salientia). Mitt Zoolog Mus Berl 55:35–57Google Scholar
  26. Hofer-Polit D (1998) Aussterben von Rana lessonae und Rana esculenta durch die Ausbreitung von Rana ridibunda. Elaphe 6:79–80Google Scholar
  27. Holenweg Peter A-K (2001) Dispersal rates and distances in adult water frogs, Rana lessonae, R. ridibunda and their hybridogenetic associate R. esculenta. Herpetologica 57:449–460Google Scholar
  28. Holenweg Peter A-K, Reyer H-U, Tietje GA (2001) Homing behavior of Rana lessonae, R. ridibunda and their hybridogenetic associate R. esculenta after experimental displacement. Amphib-reptil 22:475–480. doi: 10.1163/15685380152770435 CrossRefGoogle Scholar
  29. Holenweg Peter A-K, Reyer H-U, Abt G (2002) Species and sex ratio differences in mixed populations of hybridogenetic water frogs: the influence of pond features. Eoscience 9:1–11Google Scholar
  30. Holsbeek G, Mergeay J, Hotz H, Plötner J, Volckaert FAM, De Meester L (2008) A cryptic invasion within an invasion and widespread introgression in the European water frog complex: the toll of uncontrolled commercial trade and weak international legislation. Mol Ecol 17:5023–5035Google Scholar
  31. Hotz H, Uzzell T (1983) Interspecific hybrids of Rana ridibunda without germ line exclusion of a parental genome. Experientia 39:538–540. doi: 10.1007/BF01965196 CrossRefGoogle Scholar
  32. 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. doi: 10.1002/jez.1402360210 CrossRefGoogle Scholar
  33. Hotz H, Beerli P, Spolsky C (1992) Mitochondrial DNA reveals formation of nonhybrid frogs by natural matings between hemiclonal hybrids. Mol Biol Evol 9:610–620PubMedGoogle Scholar
  34. Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biol Conserv 89:143–152. doi: 10.1016/S0006-3207(98)00153-0 CrossRefGoogle Scholar
  35. Jooris R (2002) Pelophylax: de groene wachters aan de waterkant. Natuurpunt, MechelenGoogle Scholar
  36. Lamont BB, He T, Enright NJ, Krauss SL, Miller BP (2003) Anthropogenic disturbance promotes hybridization between Banksia species by altering their biology. J Evol Biol 16:551–557. doi: 10.1046/j.1420-9101.2003.00548.x CrossRefPubMedGoogle Scholar
  37. Levin DA, Francisco-Ortega J, Jansen RK (1996) Hybridization and the extinction of rare plant species. Conserv Biol 10:10–16. doi: 10.1046/j.1523-1739.1996.10010010.x CrossRefGoogle Scholar
  38. Lymberakis P, Poulakakis N, Manthalou G, Tsigenopoulos CS, Magoulas A, Mylonas M (2007) Mitochondrial phylogeography of Rana (Pelophylax) populations in the Eastern Mediterranean region. Mol Phylogenet Evol 44:115–125. doi: 10.1016/j.ympev.2007.03.009 CrossRefPubMedGoogle Scholar
  39. Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237. doi: 10.1016/j.tree.2005.02.010 CrossRefPubMedGoogle Scholar
  40. Mikulicek P, Kotlik P (2001) Two water frog populations from western Slovakia consisting of diploid females and diploid and triploid males of the hybridogenetic hybrid Rana esculenta (Anura, Ranidae). Mitt Mus Naturkunde Berl. Zoolog Reihe 77:59–64Google Scholar
  41. Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451. doi: 10.1073/pnas.091093398 CrossRefPubMedGoogle Scholar
  42. Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1:2–9. doi: 10.1016/0027-5107(64)90047-8 Google Scholar
  43. Ogielska M (1994a) Nucleus-like bodies in gonial cells of Rana esculenta (Amphibia, Anura) tadpoles—a putative way of chromosome elimination. Zool Pol 39:461–474Google Scholar
  44. Ogielska M (1994b) Rana esculenta developmental syndrome: fates of abnormal embryos from the first cleavage until spontaneous death. Zool Pol 39:447–459Google Scholar
  45. Pagano A, Joly P, Hotz H (1997) Taxon composition and genetic variation of water frogs in the Mid-Rhone floodplain. Life Sci 320:759–766Google Scholar
  46. Pagano A, Crochet PA, Graf JD, Joly P, Lodé T (2001a) Distribution and habitat use of water frog hybrid complexes in France. Glob Ecol Biogeogr 10:433–441. doi: 10.1046/j.1466-822X.2001.00246.x CrossRefGoogle Scholar
  47. Pagano A, Joly P, Plenet S, Lehman A, Grolet O (2001b) Breeding habitat partitioning in the Rana esculenta complex: the intermediate niche hypothesis supported. Ecoscience 8:294–300Google Scholar
  48. Pagano A, Lodé T, Crochet PA (2001c) New contact zone and assemblages among water frogs of Southern France. J Zool Syst Evol Res 39:63–67. doi: 10.1046/j.1439-0469.2001.00156.x CrossRefGoogle Scholar
  49. Pagano A, Dubois A, Lesbarreres D, Lodé T (2003) Frog alien species: a way for genetic invasion? C R Biol 326:S85–S92. doi: 10.1016/S1631-0691(03)00043-X CrossRefPubMedGoogle Scholar
  50. Pimm SL, Raven P (2000) Biodiversity: extinction by numbers. Nature 403:843–845. doi: 10.1038/35002708 CrossRefPubMedGoogle Scholar
  51. Plénet S, Hervant F, Joly P (2000a) Ecology of the hybridogenetic Rana esculenta complex: differential oxygen requirements of tadpoles. Evol Ecol 14:13–23. doi: 10.1023/A:1011056703016 CrossRefGoogle Scholar
  52. Plénet S, Pagano A, Joly P, Fouillet P (2000b) Variation of plastic responses to oxygen availability within the hybridogenetic Rana esculenta complex. J Evol Biol 13:20–28. doi: 10.1046/j.1420-9101.2000.00141.x CrossRefGoogle Scholar
  53. Plötner J (2005) Die westpaläarktischen wasserfrösche von märtyrern der wissenschaft zur biologischen sensation. Laurenti-Verlag, Bielefeld, p 160Google Scholar
  54. Plötner J, Uzzell T, Beerli P, Spolsky C, Ohst T, Litvinchuk SN et al (2008) Widespread unidirectional transfer of mitochondrial DNA: a case in western Palaearctic water frogs. J Evol Biol 21:668–681. doi: 10.1111/j.1420-9101.2008.01527.x CrossRefPubMedGoogle Scholar
  55. Ragghianti M, Bucci S, Marracci S, Casola C, Mancino G, Hotz H et al (2007) Gametogenesis of intergroup hybrids of hemiclonal frogs. Genet Res 89:39–45. doi: 10.1017/S0016672307008610 CrossRefPubMedGoogle Scholar
  56. Rey A, Michellod B, Grossenbacher K (1985) Inventaire des batraciens du Valais: situation en 1985. Bull Maurithienne 103:3–38Google Scholar
  57. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109. doi: 10.1146/annurev.ecolsys.27.1.83 CrossRefGoogle Scholar
  58. Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389. doi: 10.1146/annurev.ecolsys.28.1.359 CrossRefGoogle Scholar
  59. Rist L, Semlitsch RD, Hotz H, Reyer H-U (1997) Feeding behaviour, food consumption, and growth efficiency of hemiclonal and parental tadpoles of the Rana esculenta complex. Funct Ecol 11:735–742. doi: 10.1046/j.1365-2435.1997.00147.x CrossRefGoogle Scholar
  60. Schmeller D, Seitz A, Crivelli A, Pagano A, Veith M (2001) Inheritance in the water frog Rana ridibunda Pallas, 1771—is it Mendelian or hemiclonal? Mitt Mus Naturkunde Berl. Zoolog Reihe 77:39–42Google Scholar
  61. Schmeller D, Seitz A, Crivelli A, Veith M (2005) Crossing species’ range borders: interspecies gene exchange mediated by hybridogenesis. Proc R Soc Lond B Biol Sci 272:1625–1631. doi: 10.1098/rspb.2005.3129 CrossRefGoogle Scholar
  62. Schmeller DS, Pagano A, Plenet S, Veith M (2007) Introducing water frogs—Is there a risk for indigenous species in France? C R Biol 330:684–690. doi: 10.1016/j.crvi.2007.04.005 CrossRefPubMedGoogle Scholar
  63. Schultz R (1969) Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates. Am Nat 103:605–609CrossRefGoogle Scholar
  64. Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207. doi: 10.1016/j.tree.2004.01.003 CrossRefPubMedGoogle Scholar
  65. Som C, Reyer HU (2006) Hemiclonal reproduction slows down the speed of Muller’s ratchet in hybridogenetic frog Rana esculenta. J Evol Biol 20:650–660. doi: 10.1111/j.1420-9101.2006.01243.x CrossRefGoogle Scholar
  66. Spolsky C, Uzzell T (1984) Natural interspecies transfer of mitochondrial DNA in amphibians. Proc Natl Acad Sci USA 81:5802–5805. doi: 10.1073/pnas.81.18.5802 CrossRefPubMedGoogle Scholar
  67. Spolsky C, Uzzell T (1986) Evolutionary history of the hybridogenetic hybrid frog Rana esculenta as deduced from mtDNA analyses. Mol Biol Evol 3:44–56PubMedGoogle Scholar
  68. Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97:5948–5953. doi: 10.1073/pnas.100110397 CrossRefPubMedGoogle Scholar
  69. Tunner HG, Heppich S (1981) Premeiotic genome exclusion during oogenesis in the common edible frog, Rana esculenta. Naturwissenschaften 68:207–208. doi: 10.1007/BF01047207 CrossRefPubMedGoogle Scholar
  70. Tunner HG, Heppich-Tunner S (1991) Genome exclusion and two strategies of chromosome duplication in oogenesis of a hybrid frog. Naturwissenschaften 78:32–34. doi: 10.1007/BF01134041 CrossRefGoogle Scholar
  71. Uzzell T, Hotz H (1979) Electrophoretic and morphological evidence for two forms of green frogs (Rana esculenta complex) in peninsular Italy (Amphibia, Salientia). Mitt Zoolog Mus Berl 55:13–27Google Scholar
  72. Uzzell T, Günther R, Berger L (1977) Rana ridibunda and Rana esculenta: a leaky hybridogenetic system (Amphibia Salienta). Proc Acad Nat Sci Phila 128:147–171Google Scholar
  73. 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. doi: 10.1002/jez.1402140303 CrossRefGoogle Scholar
  74. Vinogradov AE, Chubinishvili AT (1999) genome reduction in a hemiclonal frog Rana esculenta from radioactively contaminated areas. Genetics 151:1123–1125PubMedGoogle Scholar
  75. Vinogradov AE, Borkin LJ, Günther R, Rosanov JM (1991) Two germ cell lineages with genomes of different species in one and the same animal. Hereditas 114:245–251. doi: 10.1111/j.1601-5223.1991.tb00331.x CrossRefPubMedGoogle Scholar
  76. Vorburger C (2001a) Fixation of deleterious mutations in clonal lineages: evidence from hybridogenetic frogs. Evol Int J Org Evol 55:2319–2332Google Scholar
  77. Vorburger C (2001b) Heterozygous fitness effects of clonally transmitted genomes in waterfrogs. J Evol Biol 14:602–610. doi: 10.1046/j.1420-9101.2001.00307.x CrossRefGoogle Scholar
  78. Vorburger C (2001c) Non-hybrid offspring from matings between hemiclonal hybrid waterfrogs suggest occasional recombination between clonal genomes. Ecol Lett 4:628–636. doi: 10.1046/j.1461-0248.2001.00272.x CrossRefGoogle Scholar
  79. Vorburger C, Reyer H-U (2003) A genetic mechanism of species replacement in European waterfrogs? Conserv Genet 4:141–155. doi: 10.1023/A:1023346824722 CrossRefGoogle Scholar
  80. Wijnands HEJ (1976) Distribution and habitat of Rana esculenta complex in the Netherlands. Neth J Zool 27:277–286. doi: 10.1163/002829677X00135 CrossRefGoogle Scholar
  81. Zeisset I, Beebee TJC (2003) Population genetics of a successful invader: the marsh frog Rana ridibunda in Britain. Mol Ecol 12:639–646. doi: 10.1046/j.1365-294X.2003.01775.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Laboratory of Aquatic Ecology and Evolutionary BiologyKatholieke Universiteit LeuvenLouvainBelgium
  2. 2.Laboratory of Animal Diversity and SystematicsKatholieke Universiteit LeuvenLouvainBelgium
  3. 3.NatuurpuntMechlinBelgium

Personalised recommendations