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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Notes
- 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
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
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
Berger L (1967) Embryonal and larval development of F1-generation of green frogs different combinations. Acta Zool Cracov 12: 123–160
Berger L (1968) Morphology of F1-generation of various crosses within Rana esculenta-complex. Acta Zool Cracov 13: 301–324
Berger L (1970) Some characteristics of the crosses within Rana esculenta complex in postlarval development. Ann Zool 27: 373–416
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
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
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
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
Chao L (1990) Fitness of RNA virus decreased by Muller’s ratchet. Nature 348: 454–455
Charlesworth B, Charlesworth D (1997) Rapid fixation of deleterious alleles can be caused by Muller’s ratchet. Genet Res 70: 63–73
Charlesworth B, Charlesworth D (1998) Some evolutionary consequences of deleterious mutations. Genetica 102/103: 3–19
Dubois A (1992) Notes sur la classification des Ranidae (amphibiens anoures). Bull Mens Soc Linn Lyon 61: 305–352
Ebendal T (1979) Distribution, morphology and taxonomy of the Swedisch green frogs (Rana esculenta complex). Mitt Zool Mus Berl 55: 143–152
Ellegren H, Fridolfsson AK (2003) Sex-specific mutation rates in salmonid fish. J Mol Evol 56: 458–463
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
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
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
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
Guex GD, Hotz H, Semlitsch RD (2002) Deleterious alleles and differential viability in progeny of natural hemiclonal frogs. Evolution 56: 1036–1044
Günther R (1990) Die Wasserfrösche Europas (Anura – Froschlurche). A. Ziemsen Verlag, Wittenberg Lutherstadt
Günther R, Uzzell T, Berger L (1979) Inheritance patterns in triploid Rana “esculenta” (Amphibia, Salientia). Mitt Zool Mus Berl 55: 35–57
Halligan DL, Keightley PD (2003) How many lethal alleles? Trends Genet 19: 57–59
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
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
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
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
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
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
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
Hurst LD, Ellegren H (1998) Sex biases in the mutation rate. Trends Genet 14: 446–452
Mantovani B, Scali V (1992) Hybridogenesis and androgenesis in the stick insect Bacillus rossius-grandii benazzii (Insecta, Phasmatodea). Evolution 46: 783–796
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
Milinski M (1994) Hybridogenetic frogs on an evolutionary dead end road. Trends Ecol Evol 9:62
Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 1: 2–9
Pagano A, Dubois A, Lesbarrères D, Lodé T (2003) Frog alien species: a way for genetic invasion? C R Biol 326: S85–S92
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
Plötner J (2005) Die westpaläarktischen Wasserfrösche. Laurenti-Verlag, Bielefeld
Redfield RJ (1994) Male mutation rates and the cost of sex for females. Nature 369: 145–147
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
Roesli M, Reyer H-U (2000) Male vocalization and female choice in the hybridogenetic Rana lessonae/Rana esculenta complex. Anim Behav 60: 745–755
Rybacki M, Berger L (1994) Distribution and ecology of water frogs in Poland. Zoologica Poloniae 39: 293–303
Rybacki M, Berger L (2001) Types of water frog populations (Rana esculenta complex) in Poland. Mitt Mus Naturkd Berlin, Zool Reihe 77: 51–57
Saitoh K, Kim IS, Lee EH (2004) Mitochondrial gene introgression between spined loaches via hybridogenesis. Zool Sci 21: 795–798
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
Schmeller DS (2004) Tying ecology and genetics of hemiclonally reproducing waterfrogs (Rana, Anura). Ann Zool Fenn 41: 681–687
Schmeller DS, O’Hara R, Kokko H (2005a) Male adaptive stupidity: male mating pattern in hybridogenetic frogs. Evol Ecol Res 7: 1039–1050
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
Schmidt BR (1993) Are hybridogenetic frogs cyclical parthenogens? Trends Ecol Evol 8: 271–273
Schultz RJ (1969) Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates. Am Nat 103:605–619
Schultz RJ (1973) Unisexual fish – laboratory synthesis of a species. Science 179: 180–181
Semlitsch RD (1993) Asymmetric competition in mixed populations of tadpoles of the hybridogenetic Rana esculenta complex. Evolution 47: 510–519
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
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
Som C, Reyer HU (2006) Variation in sex ratio and evolutionary rate of hemiclonal Rana esculenta populations. Evol Ecol 20: 159–172
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
Spolsky C, Uzzell T (1984) Natural interspecies transfer of mitochondrial DNA in amphibians. Proc Natl Acad Sci USA 81: 5802–5805
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
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
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
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
Tunner HG (1974) Die klonale Struktur einer Wasserfroschpopulation. Z Zool Syst Evol 12:309–314
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
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
Vences M (2007) The amphibian tree of life: Ideologie, Chaos oder biologische Realität? Z Feldherpetol 14: 153–162
Vorburger C (2001a) Fixation of deleterious mutations in clonal lineages: Evidence from hybridogenetic frogs. Evolution 55: 2319–2332
Vorburger C (2001b) Heterozygous fitness effects of clonally transmitted genomes in waterfrogs. J Evol Biol 14: 602–610
Vorburger C (2001c) Non-hybrid offspring from matings between hemiclonal hybrid waterfrogs suggest occasional recombination between clonal genomes. Ecol Lett 4: 628–636
Vorburger C, Reyer HU (2003) A genetic mechanism of species replacement in European waterfrogs? Conserv Genet 4: 141–155
Vrijenhoek RC, Angus RA, Schultz RJ (1977) Variation and heterozygosity in sexually vs. clonally reproducing populations of Poeciliopsis. Evolution 31: 767–781
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights 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
DOI: https://doi.org/10.1007/978-90-481-2770-2_20
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-90-481-2769-6
Online ISBN: 978-90-481-2770-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)