Skip to main content
SpringerLink
Log in

Invasiveness of an introduced species: the role of hybridization and ecological constraints

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Introduced species are confronted with new environments to which they need to adapt. However, the ecological success of an introduced species is generally difficult to predict, especially when hybridizations may be involved in the invasion success. In western Europe, the lake frog Pelophylax ridibundus appears to be particularly successful. A reason for this species’ success might be the presence of the invader’s genetic material prior to the introduction in the form of a hybrid between P. ridibundus and a second indigenous water frog species. These hybrids reproduce by hybridogenesis, only transmitting the ridibundus genome to gametes and backcrossing with the indigenous species (i.e. P. lessonae). This reproductive system allows the hybrid to be independent from P. ridibundus, and allows the ridibundus genome to be more widely spread than the species itself. Matings among hybrids produce newly formed P. ridibundus offspring (N), if the genomes are compatible. Therefore, we hypothesize that hybridogenesis increases the invasiveness of P. ridibundus (1) by enhancing propagule pressure through N individuals, and/or (2) by increasing adaptation of invaders to the native water frogs’ habitat through hybrid-derived ridibundus genomes that are locally adapted. We find support for the first hypothesis because a notable fraction of N tadpoles is viable. However, in our semi-natural experiments they did not outperform ridibundus tadpoles in the native water frogs’ habitat, nor did they differ physiologically. This does not support the second hypothesis and highlights ecological constraints on the invasion. However, we cannot rule out that these constraints may fall with ongoing selection, making a replacement of indigenous species highly probable in the future.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Akin C, Bilgin CC, Beerli P, Westaway R, Ohst T, Litvinchuk SN, Uzzell T, Bilgin M, Hotz H, Guex GD, Plotner J (2010) Phylogeographic patterns of genetic diversity in eastern Mediterranean water frogs were determined by geological processes and climate change in the Late Cenozoic. J Biogeogr 37:2111–2124

    Article  Google Scholar 

  • Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspect Plant Ecol Evol Syst 3:52–66

    Article  Google Scholar 

  • Altwegg R, Reyer HU (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882

    PubMed  Google Scholar 

  • Arano B, Llorente GA, Herrero P, Sanchiz B (1994) Current studies on Iberian water frogs. Zoologica Poloniae 39:365–375

    Google Scholar 

  • Arioli M, Jakob C, Reyer HU (2010) Genetic diversity in water frog hybrids (Pelophylax esculentus) varies with population structure and geographic location. Mol Ecol 19:1814–1828

    Article  PubMed  Google Scholar 

  • Barney JN, Whitlow TH (2008) A unifying framework for biological invasions: the state factor model. Biol Invasions 10:259–272

    Article  Google Scholar 

  • Berger L (1983) Western Palearctic water frogs (Amphibia, Ranidae): systematics, genetics and population compositions. Experientia 39:27–130

    Google Scholar 

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

  • Berger L, Uzzell T, Hotz H (1988) Sex determination and sex ratios in western Palearctic water frogs: XX and XY female hybrids in the Pannonian Basin? Proc Acad Nat Sci Phila 140:220–239

    Google Scholar 

  • Berven KA (1990) Factors Affecting Population Fluctuations in Larval and Adult Stages of the Wood Frog (Rana Sylvatica). Ecology 71:1599–1608

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Christiansen DG, Reyer HU (2009) From clonal to sexual hybrids: genetic recombination via triploids in all-hybrid populations of water frogs. Evolution 63:1754–1768

    Article  PubMed  CAS  Google Scholar 

  • Christiansen DG, Fog K, Pedersen V, Boomsma JJ (2005) Reproduction and hybrid load in all-hybrid populations of Rana esculenta water frogs in Denmark. Evolution 59:1348–1361

    PubMed  Google Scholar 

  • Culley TM, Hardiman NA (2009) The role of intraspecific hybridization in the evolution of invasiveness: a case study of the ornemental pear tree Pyrus calleryana. Biol Invasions 11:1107–1119

    Article  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050

    Article  PubMed  CAS  Google Scholar 

  • Facon B, Jarne P, Pointier JP, David P (2005) Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance. J Evol Biol 18:524–535

    Article  PubMed  CAS  Google Scholar 

  • Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, David P (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21:130–135

    Article  PubMed  Google Scholar 

  • Frost DR, Grant T, Faivovich R, Bain RH, Haas A, Haddad CFB, De Sa RO, Channing A, Wilkinson M, Donnellan SC (2006) The amphibian tree of life. Bull Am Mus Nat Hist 297:8–370

    Article  Google Scholar 

  • Garner TWJ, Gautschi B, Rothlisberger S, Reyer HU (2000) A set of CA repeat microsatellite markers derived from the pool frog, Rana lessonae. Mol Ecol 9:2173–2175

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

  • Guex GD, Hotz H, Semlitsch RD (2002) Deleterious alleles and differential viability in progeny of natural hemiclonal frogs. Evolution 56:1036–1044

    PubMed  Google Scholar 

  • Günther R (1990) Die Wasserfrösche Europas (Anura–Froschlurche). Die Neue Brehm Bücherei, A. Ziemsen Verlag, Wittenberg Lutherstadt

  • Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Evol Syst 31:139–162

    Article  Google Scholar 

  • Hervant F, Mathieu J, Garin D, Fréminet A (1995) Behavioral, ventilatory and metabolic responses to severe hypoxia and subsequent recovery of the hypogean Niphargus rhenorhodanensis and the epigean Gammarus fossarum (Crustacea: Amphipoda). Physiol Zool 68:223–244

    Google Scholar 

  • Holsbeek G, Jooris R (2010) Potential impact of genome exclusion by alien species in the hybridogenetic water frogs (Pelophylax esculentus complex). Biol Invasions 12:1–13

    Google Scholar 

  • 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: consequences of uncontrolled commercial trade and weak international legislation. Mol Ecol 17:5023–5035

    Article  PubMed  CAS  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

    Article  Google Scholar 

  • Hotz H, Beerli P, Spolsky C (1992) Mitochondrial-DNA reveals formation of nonhybrid frogs by natural matings between hemiclonal hybrids. Mol Biol Evol 9:610–620

    PubMed  CAS  Google Scholar 

  • Kelly DW, Muirhead JR, Heath DD, Macisaac HJ (2006) Contrasting patterns in genetic diversity following multiple invasions of fresh and brackish waters. Mol Ecol 15:3641–3653

    Article  PubMed  CAS  Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  PubMed  Google Scholar 

  • Kondrashov AS, Houle D (1994) Genotype-environment interactions and the estimation of the genomic mutation-rate in Drosophila-melanogaster. Proc R Soc Lond B Biol Sci 258:221–227

    Article  CAS  Google Scholar 

  • Lalouette L, Kaufmann B, Konecny L, Renault D, Douady CJ (2010) Characterization and PCR multiplexing of 14 new polymorphic microsatellite loci for the invasive subantarctic carabid Merizodus soledadinus (Coleoptera: Carabidae). Cons Genet Resour 1:455–458

    Article  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228

    Article  PubMed  Google Scholar 

  • Lockwood JL, Hoopes MF, Marchetti MP (2007) Invasion ecology. Blackwell, Oxford

    Google Scholar 

  • Lutschinger G (1988) Zur Uberwinterung der Wasserfrösche in den Donau- und Marchauen. In: Günther R, Klewen R (ed) Beiträge zur Biologie und Bibliographie (1960–1987) der europäischen Wasserfrösche, Jb. Feldherp. Beiheft 1, Verlag für Okologie u. Faunistik, Duisburg, pp. 153–160

  • Mallet J (2005) Hybridization as an invasion of the genorne. Trends Ecol Evol 20:229–237

    Article  PubMed  Google Scholar 

  • Mezhzherin SV, Morozov-leonov SI, Nekrasova OD (2004) Natural transfer of nuclear genes in hybrid populations of green frogs Rana esculenta L., 1758 complex: space-time analysis of the phenomenon. Genetika 40:1646–1653

    Google Scholar 

  • Milinski M (1994) Hybridogenetic frogs on an evolutionary dead-end road. Trends Ecol Evol 9:62

    Article  PubMed  CAS  Google Scholar 

  • Pagano A, Schmeller DS (1999) Is recombination less negligible than previously described in hybridogenetic water frogs? In: Miaud C, Guyétant R (eds) 9th O.G. Meeting–current studies in herpetology. SEH, Le Bourget du Lac, France, pp 351–356

  • Pagano A, Joly P, Hotz H (1997) Taxon composition and genetic variation of water frogs in the mid-Rhone floodplain. C R Acad Sci Ser III Sci Vie 320:759–766

    CAS  Google Scholar 

  • Pagano A, Crochet PA, Graf JD, Joly P, Lode T (2001) Distribution and habitat use of water frog hybrid complexes in France. Glob Ecol Biogeogr 10:433–441

    Article  Google Scholar 

  • Pagano A, Dubois A, Lesbarreres D, Lode T (2003) Frog alien species: a way for genetic invasion? C R Biol 326:S85–S92

    Article  PubMed  Google Scholar 

  • Pagano A, Lesbarrères D, Crivelli A, Veith M, Lodé T, O’Hara R, Schmeller DS (2008) Geographical and ecological distributions of frog hemiclones suggest occurrence of both “General Purpose Genotype” and “Frozen Niche Variation” clones. J Zool Syst Evol Res 46:162–168

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

  • Plénet S, Joly P, Pagano A (1998) Is habitat requirement by an oxygen-dependent frog (Rana ridibunda) governed by its larval stage? Arch Hydrobiol 143:107–119

    Google Scholar 

  • Plénet S, Hervant F, Joly P (2000a) Ecology of the hybridogenetic Rana esculenta complex: differential oxygen requirements of tadpoles. Evol Ecol 14:13–23

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Plénet S, Joly P, Hervant F, Fromont E, Grolet O (2005) Are hybridogenetic complexes structured by habitat in water frogs? J Evol Biol 18:1575–1586

    Article  PubMed  Google Scholar 

  • Plénet S, Joly P, Schmeller DS (2009) Nouvelle combinaison génétique par hybridation et accroissement du potentiel invasif, suite à une introduction. Genetic diversity of an introduced frog and ecological risks of species introduction. In: Barbault R, Atramentowiczs M (eds) Les invasions biologiques, une question de natures et de sociétés, INRA, Versailles, pp 24–25

  • Plötner J (2005) Die westpaläarktischen Wasserfrösche-von Märtyren der Wissenschaft zur biologischen Sensation. Laurenti-Verlag, Bielefeld

    Google Scholar 

  • Plötner J, Ohst T, Böhme W, Schreiber R (2001) Divergence in mitochondrial DNA of Near Eastern water frogs with special reference to the systematic status of Cypriote and Anatolian populations (Anura, Ranidae). Amphib-Reptilia 22:397–412

    Article  Google Scholar 

  • Plötner J, Uzzell T, Beerli P, Spolsky C, Ohst T, Litvinchuk SN, Guex GD, Reyer HU, Hotz H (2008) Widespread unidirectional transfer of mitochondrial DNA: a case in western Palaearctic water frogs. J Evol Biol 21:668–681

    Article  PubMed  Google Scholar 

  • Plötner J, Uzzell T, Beerli P, Akin C, Bilgin CC, Haefeli C, Ohst T, Köhler F, Schreiber R, Guex G-D, Litvinchuk AN, Westaway R, Reyer H-U, Hotz H (2010) Genetic divergence and evolution of reproductive isolation in eastern Mediterranean water frogs. In: Glaubrecht M (ed) Evolution in action. Case studies in adaptive radiation and the origin of biodiversity. Special volume from the SPP 1127 “Radiations: Genesis of Biological diversity” of the DFG. Springer, Berlin, pp 373–403

  • Räsänen K, Laurila A, Merilä J (2003) Carry-over effects of embryonic acid conditions on development and growth of Rana temporaria tadpoles. Freshwater Biol 47:19–30

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    Article  PubMed  Google Scholar 

  • Rybacki M, Berger L (2001) Types of water frog populations (Rana esculenta complex) in Poland. Mitteilungen aus dem Museum fuer Naturkunde in Berlin Zoologische Reihe 77:51–57

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Schierenbeck KA, Ellstrand NC (2009) Hybridization and the evolution of invasiveness in plants and other organisms. Annual Meeting of the American-Botanical-Society, Salt Lake City, UT, pp 1093–1105

  • Schmeller DS (2004) Tying ecology and genetics of hemiclonally reproducing waterfrogs (Rana, Anura). Ann Zool Fenn 41:681–687

    Google Scholar 

  • Schmeller DS, Seitz A, Crivelli A, Veith M (2005) Crossing species’ range borders: interspecies gene exchange mediated by hybridogenesis. Proc R Soc Biol Sci Ser B 272:1625–1631

    Article  CAS  Google Scholar 

  • Schmeller DS, Pagano A, Plénet S, Veith M (2007) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Google Scholar 

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

    Article  Google Scholar 

  • Shabalina SA, Yampolsky LY, Kondrashov AS (1997) Rapid decline of fitness in panmictic populations of Drosophila melanogaster maintained under relaxed natural selection. Proc Natl Acad Sci USA 94:13034–13039

    Article  PubMed  CAS  Google Scholar 

  • Smith DC (1987) Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344–350

    Article  Google Scholar 

  • Snijders TAB (2005) Fixed and random effects. In: Everitt BS, Howell DC (eds) Encyclopedia of statistics in behavioral science, vol 2. Wiley, Chicester, pp 664–665

  • Som C, Reyer HU (2006) Hemiclonal reproduction slows down the Muller’s ratchet in the hybridogenetic frog Rana esculenta. J Evol Biol 20:650–660

    Article  Google Scholar 

  • Spolsky C, Uzzell T (1984) Natural interspecies transfer of mitochondrial DNA in amphibians. Proc Natl Acad Sci USA 81:5802–5805

    Article  PubMed  CAS  Google Scholar 

  • Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360

    Article  PubMed  Google Scholar 

  • Szafraniec K, Borts RH, Korona R (2001) Environmental stress and mutational load in diploid strains of the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci USA 98:1107–1112

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2007) R: A language and environment for statistical computing. Austria, Vienna: R foundation for statistical computing. ISBN 3-900051-07-0 (http://www.R-project.org)

  • Tunner HG, Nopp H (1979) Heterosis in the common European water frog. Naturwissenschaften 66:268–269

    Article  PubMed  CAS  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, Günther R, Berger L (1977) Rana ridibunda and Rana esculenta: a leaky hybridogenetic system (Amphibia Salientia). Proc Acad Nat Sci Phila 128:147–171

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vorburger C (2001c) Non-hybrid offspring from matings between hemiclonal hybrid waterfrogs suggest occasional recombination between clonal genomes. Ecol Lett 4:628–636

    Article  Google Scholar 

  • Vorburger C, Reyer HU (2003) A genetic mechanism of species replacement in European waterfrogs? Cons Genet 4:141–155

    Article  CAS  Google Scholar 

  • Vorburger C, Schmeller DS, Hotz H, Guex GD, Reyer HU (2009) Masked damage: mutational load in hemiclonal water frogs. In: Van Dijk P, Martens K, Schoen I (eds) Lost sex—the evolutionary biology of parthenogenesis. Springer, Netherlands, pp 433–446

  • Zeisset I, Beebee TJC (2003) Population genetics of a successful invader: the marsh frog Rana ridibunda in Britain. Mol Ecol 12:639–646

    Article  PubMed  Google Scholar 

  • Zeisset I, Rowe G, Beebee TJC (2000) Polymerase chain reaction primers for microsatellite loci in the north European water frogs Rana ridibunda and R. lessoane. Mol Ecol 9:1173–1174

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank S. Kosellek and J. Cote for their help with field and laboratory works, as well as M. C. Fisher and D. C. Woodhams for linguistic corrections. Constructive comments on the manuscript were provided by an anonymous reviewer. This study was made possible by partnerships with Fondation Pierre Vérots (Saint-Jean-de-Thurigneux, Ain, France) and pumping site (Zone de captage “Crépieux-Charmy”, Villeurbanne, France) and was supported by grants from French Environment Ministry (program INVABIO).

Author information

Authors and Affiliations

  1. CNRS, UMR5023 Ecologie des Hydrosystèmes Naturels et Anthropisés, Villeurbanne, 69622, France

    E. Luquet, F. Hervant, P. Joly, B. Kaufmann, J. P. Léna, O. Grolet, L. Konecny & S. Plénet

  2. Institute of Integrative Biology, ETH Zürich, 8092, Zürich, Switzerland

    C. Vorburger

  3. EAWAG, Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, 8600, Dübendorf, Switzerland

    C. Vorburger

  4. Station d’Ecologie Experimentale du CNRS à Moulis, 09200, Saint Girons, France

    D. S. Schmeller

Authors
  1. E. Luquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Vorburger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Hervant
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Joly
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. Kaufmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. S. Schmeller
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. P. Léna
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. O. Grolet
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. L. Konecny
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. S. Plénet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Luquet.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Luquet, E., Vorburger, C., Hervant, F. et al. Invasiveness of an introduced species: the role of hybridization and ecological constraints. Biol Invasions 13, 1901–1915 (2011). https://doi.org/10.1007/s10530-011-0010-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-011-0010-2

Keywords

Search

Navigation