Skip to main content

Masked Damage: Mutational Load in Hemiclonal Water Frogs

  • Chapter
  • First Online:
Lost Sex

Abstract

Hemiclonal hybrids of Western Palearctic water frogs of the Rana esculenta complex transmit only one parental genome to their offspring without recombination (hybridogenesis). Such genomes are thus prone to accumulate deleterious mutations. The frog complex is unique among hybridogens in that hemiclonal hybrids occur in both sexes. This provides the opportunity of using experimental crosses to produce offspring possessing two clonal genomes of various origins and thereby study their homozygous and heterozygous effects on fitness. Here we review work that made use of this possibility to assess the evolutionary consequences of clonal inheritance in water frogs. Overall, these studies indicate that clonally transmitted genomes bear a substantial load of fixed deleterious mutations, yet these mutations appear to have minor effects on fitness in the heterozygous state. We also point out potential mechanisms for episodic recombination by which otherwise clonal genomes may be purged of deleterious alleles, and we present evidence for such episodic recombination to occur in natural populations of hybridogenetic frogs. Finally, we provide an outlook on work in progress that exploits the peculiarities of this system to obtain relevant estimates of the frequency of segregating lethal mutations in sexual populations of water frogs.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    Please note that according to the latest revision of amphibian classification (Frost et al. 2006), the Western Palearctic water frogs are now contained in the genus Pelophylax, formerly considered a subgenus of Rana (Dubois 1992). The new classification is likely to take hold (Vences 2007). For consistency with the literature we review, however, we adhere to the old classification in this chapter.

References

  • Abt G, Reyer H-U (1993) Mate choice and fitness in a hybrid frog: Rana esculenta females prefer Rana lessonae males over their own. Behav Ecol Sociobiol 32: 221–228

    Article  Google Scholar 

  • Abt Tietje G, Reyer H-U (2004) Larval development and recruitment of juveniles in a natural population of Rana lessonae and Rana esculenta. Copeia 3: 638–646

    Article  Google Scholar 

  • Bergen K, Semlitsch RD, Reyer H-U (1997) Hybrid female matings are directly related to the availability of Rana lessonae and Rana esculenta males in experimental populations. Copeia 2: 275–283

    Article  Google Scholar 

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

    Google Scholar 

  • Berger L (1968) Morphology of F1-generation of various crosses within Rana esculenta-complex. Acta Zool Cracov 13: 301–324

    Google Scholar 

  • Berger L (1970) Some characteristics of the crosses within Rana esculenta complex in postlarval development. Ann Zool 27: 373–416

    Google Scholar 

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

    Google Scholar 

  • Blankenhorn HJ, Heusser H, Notter P (1973) Zur Verbreitung von Rana esculenta Linnaeus und Rana lessonae Camerano im Zürcher Oberland. Rev Suisse Zool 80: 662–666

    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: 1242–1247

    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

    PubMed  CAS  Google Scholar 

  • Chao L (1990) Fitness of RNA virus decreased by Muller’s ratchet. Nature 348: 454–455

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth B, Charlesworth D (1997) Rapid fixation of deleterious alleles can be caused by Muller’s ratchet. Genet Res 70: 63–73

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth B, Charlesworth D (1998) Some evolutionary consequences of deleterious mutations. Genetica 102/103: 3–19

    Article  Google Scholar 

  • Dubois A (1992) Notes sur la classification des Ranidae (amphibiens anoures). Bull Mens Soc Linn Lyon 61: 305–352

    Google Scholar 

  • Ebendal T (1979) Distribution, morphology and taxonomy of the Swedisch green frogs (Rana esculenta complex). Mitt Zool Mus Berl 55: 143–152

    Google Scholar 

  • Ellegren H, Fridolfsson AK (2003) Sex-specific mutation rates in salmonid fish. J Mol Evol 56: 458–463

    Article  PubMed  CAS  Google Scholar 

  • Engeler B, Reyer HU (2001) Choosy females and indiscriminate males: mate choice in mixed populations of sexual and hybridogenetic water frogs (Rana lessonae, Rana esculenta). Behav Ecol 12: 600–606

    Article  Google Scholar 

  • Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad DFB, de Sá RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto BL, Moler P, Drewes RC, Nussbaum RA, Lynch JD, Green DM, Wheeler WC (2006) The amphibian tree of life. Bull Am Mus Nat Hist 297: 1–370

    Google Scholar 

  • Graf J-D, Polls Pelaz M (1989) Evolutionary genetics of the Rana esculenta complex. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. Bulletin 466, New York State Museum, Albany, New York, pp. 289–301

    Google Scholar 

  • Guex G-D, Beerli P, Barbour AD, Hotz H (1993) A dynamic model to describe equilibrium conditions in mixed populations of a hemiclonal hybrid and its sexual host in European water frogs. In: Catzeflis FM, Gautier M (eds) Evolution 93. 4th congress of the European society for evolutionary biology. Université Montpellier II, Montpellier, pp. 158

    Google Scholar 

  • 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). A. Ziemsen Verlag, Wittenberg Lutherstadt

    Google Scholar 

  • Günther R, Uzzell T, Berger L (1979) Inheritance patterns in triploid Rana “esculenta” (Amphibia, Salientia). Mitt Zool Mus Berl 55: 35–57

    Google Scholar 

  • Halligan DL, Keightley PD (2003) How many lethal alleles? Trends Genet 19: 57–59

    Article  PubMed  CAS  Google Scholar 

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

    Article  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 

  • Higgs PG, Woodcock G (1995) The accumulation of mutations in asexual populations and the structure of genealogical trees in the presence of selection. J Math Biol 33: 677–702

    Article  Google Scholar 

  • Holenweg Peter AK, Reyer HU, Tietje GA (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, Beerli P, Spolsky C (1992) Mitochondrial DNA revelas formation of nonhybrid frogs by natural matings between hemiclonal hybrids. Mol Biol Evol 9: 610–620

    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, Semlitsch RD, Gutmann E, Guex G-D, Beerli P (1999) Spontaneous heterosis in larval life-history traits of hemiclonal frog hybrids. Proc Natl Acad Sci USA 96: 2171–2176

    Article  PubMed  CAS  Google Scholar 

  • Hurst LD, Ellegren H (1998) Sex biases in the mutation rate. Trends Genet 14: 446–452

    Article  PubMed  CAS  Google Scholar 

  • Mantovani B, Scali V (1992) Hybridogenesis and androgenesis in the stick insect Bacillus rossius-grandii benazzii (Insecta, Phasmatodea). Evolution 46: 783–796

    Article  Google Scholar 

  • McCune AR, Fuller RC, Aquilina AA, Dawley RM, Fadool JM, Houle D, Travis J, Kondrashov AS (2002) A low genomic number of recessive lethals in natural populations of bluefin killifish and zebrafish. Science 296: 2398–2401

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1: 2–9

    Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Plötner J (2005) Die westpaläarktischen Wasserfrösche. Laurenti-Verlag, Bielefeld

    Google Scholar 

  • Redfield RJ (1994) Male mutation rates and the cost of sex for females. Nature 369: 145–147

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Roesli M, Reyer H-U (2000) Male vocalization and female choice in the hybridogenetic Rana lessonae/Rana esculenta complex. Anim Behav 60: 745–755

    Article  PubMed  Google Scholar 

  • Rybacki M, Berger L (1994) Distribution and ecology of water frogs in Poland. Zoologica Poloniae 39: 293–303

    Google Scholar 

  • Rybacki M, Berger L (2001) Types of water frog populations (Rana esculenta complex) in Poland. Mitt Mus Naturkd Berlin, Zool Reihe 77: 51–57

    Google Scholar 

  • Saitoh K, Kim IS, Lee EH (2004) Mitochondrial gene introgression between spined loaches via hybridogenesis. Zool Sci 21: 795–798

    Article  PubMed  CAS  Google Scholar 

  • Santucci F, Nascetti G, Bullini L (1996) Hybrid zones between two genetically differentiated forms of the pond frog Rana lessonae in southern Italy. J Evol Biol 9: 429–450

    Article  Google Scholar 

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

    Google Scholar 

  • Schmeller DS, O’Hara R, Kokko H (2005a) Male adaptive stupidity: male mating pattern in hybridogenetic frogs. Evol Ecol Res 7: 1039–1050

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schmidt BR (1993) Are hybridogenetic frogs cyclical parthenogens? Trends Ecol Evol 8: 271–273

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Schultz RJ (1973) Unisexual fish – laboratory synthesis of a species. Science 179: 180–181

    Article  PubMed  CAS  Google Scholar 

  • Semlitsch RD (1993) Asymmetric competition in mixed populations of tadpoles of the hybridogenetic Rana esculenta complex. Evolution 47: 510–519

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Som C, Bagheri HC, Reyer HU (2007) Mutation accumulation and fitness effects in hybridogenetic populations: a comparison to sexual and asexual systems. BMC Evol Biol 7

    Google Scholar 

  • Som C, Reyer HU (2006) Variation in sex ratio and evolutionary rate of hemiclonal Rana esculenta populations. Evol Ecol 20: 159–172

    Article  Google Scholar 

  • Som C, Reyer HU (2007) Hemiclonal reproduction slows down the speed of Muller’s ratchet in the hybridogenetic frog Rana esculenta. J Evol Biol 20: 650–660

    Article  PubMed  CAS  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 

  • Spolsky C, Uzzell T (1986) Evolutionary history of the hybridogenetic hybrid frog Rana esculenta as deduced from mtDNA analyses. Mol Biol Evol 3: 44–56

    PubMed  CAS  Google Scholar 

  • Szymura JM, Barton NH (1991) The genetic structure of the hybrid zone between the fire-bellied toads Bombina bombina and B. variegata – comparisons between transects and between loci. Evolution 45: 237–261

    Article  Google Scholar 

  • Tinti F, Mantovani B, Scali V (1995) Reproductive features of homospecific hybridogenetically-derived stick insects suggest how unisexuals can evolve. J Evol Biol 8: 81–92

    Article  Google Scholar 

  • Tunner HG (1973) Das Albumin und andere Bluteiweisse bei Rana ridibunda Pallas, Rana lessonae Camerano, Rana esculenta Linné und deren Hybriden. Z Zool Syst Evol 11: 219–233

    Google Scholar 

  • Tunner HG (1974) Die klonale Struktur einer Wasserfroschpopulation. Z Zool Syst Evol 12:309–314

    Article  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 

  • Vences M (2007) The amphibian tree of life: Ideologie, Chaos oder biologische Realität? Z Feldherpetol 14: 153–162

    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? Conserv Genet 4: 141–155

    Article  CAS  Google Scholar 

  • Vrijenhoek RC, Angus RA, Schultz RJ (1977) Variation and heterozygosity in sexually vs. clonally reproducing populations of Poeciliopsis. Evolution 31: 767–781

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christoph Vorburger .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Vorburger, C., Schmeller, D.S., Hotz, H., Guex, GD., Reyer, HU. (2009). Masked Damage: Mutational Load in Hemiclonal Water Frogs. In: Schön, I., Martens, K., Dijk, P. (eds) Lost Sex. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2770-2_20

Download citation

Publish with us

Policies and ethics