Body size variation in hybrids among populations of European water frogs (Pelophylax esculentus complex) with different breeding systems
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Abstract
In some populations, hybrids reproduce with a parental species by eliminating the genome of this species from their own germline and produce gametes that only contain the genome of the other parental species (sexual host). This mode of reproduction, known as hybridogenesis, leads to a conflict of interest between the two parties because the sexual host should avoid mating with the hybrid to prevent a reduction in reproductive success, whereas the hybrid depends on such matings for survival. We investigated European water frogs (Pelophylax esculentus complex), including hybrids (P. esculentus, genotype LR) and two sexual host species (P. lessonae, LL and P. ridibundus, RR). We hypothesized that to maximize fitness, hybrid males should be morphologically more similar to the sexual host that is preferred by females for successful reproduction. To test this hypothesis, we compared hybrid males in two different population types, L-E (hybrids coexist with LL) and L-E-R (hybrids coexist with both LL and RR). The latter was described in terms of genome composition, sex ratio, and mate choice preferences; the sex ratio of hybrids was significantly male-biased. We found that LR males from the L-E-R populations were significantly larger than those from the L-E, which makes them more similar to P. ridibundus, the largest species within the P. esculentus complex. We suggest that a larger body size of hybrid males may provide a reproductive advantage in the L-E-R population type, where the most common type of pair caught in the breeding season was LR males × RR females.
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-
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.
-
Avise, J.C. (2008): Clonality: the Genetics, Ecology, and Evolution of Sexual Abstinence in Vertebrate Animals. Oxford University Press, Oxford.
-
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. Philadelphia 140: 220-239.
-
Berger, L. (2008): European Green Frogs and Their Protection. Ecological Library Foundation, Prodruk, Poznań.
-
Blankenhorn, H. (1977): Reproduction and mating behaviour in Rana lessonae-Rana esculenta mixed populations. In: The Reproductive Biology of Amphibians, p. 389-410. Taylor, D.H., Guttman, S.I., Eds, Plenum Press, New York.
-
Borkin, L.J., Caune, I.A., Pikulik, M.M., Sokolova, T.M. (1986): Distribution and structure of the green frog complex in the USSR. In: Studies in Herpetology, p. 675-678. Roček, Z., Ed., Societas Europaea Herpetologica, Prague.
-
Borkin, L.J., Litvinchuk, S.N., Mannapova, E.I., Pestov, M.V., Rosanov, J.M. (2002): The distribution of green frogs (Rana esculenta complex) in Nizhny Novgorod Province, central European Russia. Russ. J. Herpetol. 9: 195-208.
-
Borkin, L.J., Korshunov, A.V., Lada, G.A., Litvinchuk, S.N., Rosanov, J.M., Shabanov, D.A., Zinenko, A.I. (2004): Mass occurrence of polyploid green frogs (Rana esculenta complex) in eastern Ukraine. Russ. J. Herpetol. 11: 194-213.
-
Bove, P., Milazzo, P., Barbuti, R. (2014): The role of deleterious mutations in the stability of hybridogenetic water frog complexes. BMC Evol. Biol. 14: 107.
-
Christiansen, D.G. (2009): Gamete types, sex determination and stable equilibria of all-hybrid populations of diploid and triploid edible frogs (Pelophylax esculentus). BMC Evol. Biol. 9: 1-16.
-
Christiansen, D.G., Reyer, H.-U. (2009): From clonal to sexual hybrids: genetic recombination via triploids in all-hybrid populations of water frogs. Evolution 63: 1754-1768.
-
Clutton-Brock, T.H., Vincent, A.C.J. (1991): Sexual selection and the potential reproductive rates of males and females. Nature 351: 58-60.
-
Czernicka, E. (2013): Zróżnicowanie genetyczne i struktura mieszanych populacji żab zielonych kompleksu Pelophylax esculentus w Dolinie Baryczy. PhD thesis, University of Wrocław. (In Polish).
-
Doležálková-Kaštánková, M., Pruvost, N.B.M., Plötner, J., Reyer, H.-U., Janko, K., Choleva, L. (2018): All-male hybrids of a tetrapod Pelophylax esculentus share its origin and genetics of maintenance. Biol. Sex Differ. 9: 13.
-
Dries, L.A. (2003): Peering through the looking glass at a sexual parasite: are Amazon mollies red queens? Evolution 57: 1387-1396.
-
Emlen, S.T., Oring, L.W. (1977): Ecology, sexual selection and the evolution of mating systems. Science 197: 215-223.
-
Engeler, B., Reyer, H.-U. (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.
-
Garner, T.W.J., Gautschi, B., Röthlisberger, S., Reyer, H.-U. (2000): A set of CA repeat microsatellite markers derived from the pool frog, Rana lessonae. Mol. Ecol. 9: 2173-2175.
-
Graf, J.-D., Polls Pelaz, M. (1989): Evolutionary genetics of the Rana esculenta complex. In: Evolution and Ecology of Unisexual Vertebrates, p. 289-301. Dawley, R.M., Bogart, J.P., Eds, New York State Museum, Albany.
-
Guex, G.D., Hotz, H., Semlitsch, R.D. (2002): Deleterious alleles and differential viability in progeny of natural hemiclonal frogs. Evolution 56: 1036-1044.
-
Herczeg, D., Vörös, J., Christiansen, D.G., Benovics, M., Mikulíček, P. (2017): Taxonomic composition and ploidy level among European water frogs (Anura: Ranidae: Pelophylax) in eastern Hungary. J. Zool. Syst. Evol. Res. 55: 129-137.
-
Hermaniuk, A., Pruvost, N.B.M., Kierzkowski, P., Ogielska, M. (2013): Genetic and cytogenetic characteristics of pentaploidy in water frogs. Herpetologica 69: 36-45.
-
Hoffmann, A., Reyer, H.-U. (2013): Genomic effects on advertisement call structure in diploid and triploid hybrid water frogs (Anura, Pelophylax esculentus). BMC Ecol. 13: 47.
-
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.
-
Hotz, H., Semlitsch, R.D., Gutmann, E., Guex, G.D., Beerli, P. (1999): Spontaneous heterosis in larval life history traits of hemiclonal frog hybrids. P. Natl. Acad. Sci. USA 96: 2171-2176.
-
Hotz, H., Uzzell, T., Guex, G.D., Alpers, D., Semlitsch, R.D., Beerli, P. (2001): Microsatellites: a tool for evolutionary genetic studies of western Palearctic water frogs. Mitt. Mus. Naturkunde Berl., Zoolog. Reihe 77: 43-50.
-
Kierzkowski, P., Paśko, Ł., Rybacki, M., Socha, M., Ogielska, M. (2011): Genome dosage effect and hybrid morphology: the case of the hybridogenetic water frogs of the Phylophylax esculentus complex. Ann. Zool. Fenn. 48: 56-66.
-
Lada, G.A., Borkin, L.J., Vinogradov, A.E. (1995): Distribution, population systems and reproductive behavior of green frogs (hybridogenetic Rana esculenta complex) in the Central Chernozem Territory of Russia. Russ. J. Herpetol. 2: 46-57.
-
Lavanchy, G., Schwander, T. (2019): Hybridogenesis. Curr. Biol. 29: R1-R15.
-
Lengagne, T., Plenet, S., Joly, P. (2008): Breeding behaviour and hybridization: variation in male chorusing behaviour promotes mating among taxa in water frogs. Anim. Behav. 75: 443-450.
-
Litvinchuk, S.N., Borkin, L.J., Litvinchuk, Y.S., Rosanov, J.M. (2015): Distribution and population systems of green frogs (Pelophylax esculentus complex) in Kaliningrad oblast’, Russia (Baltic Sea region). Russ. J. Herpetol. 22: 188-196.
-
Mikulíček, P., Kautman, M., Demovič, B., Janko, K. (2014): When a clonal genome finds its way back to a sexual species: evidence from ongoing but rare introgression in the hybridogenetic water frog complex. J. Evol. Biol. 27: 628-642.
-
Mikulíček, P., Kautman, M., Kautman, J., Pruvost, N.B.M. (2015): Mode of hybridogenesis and habitat preferences influence population composition of water frogs (Pelophylax esculentus complex, Anura: Ranidae) in a region of sympatric occurrence (western Slovakia). J. Zool. Syst. Evol. Res. 53: 124-132.
-
Ogielska, M., Kierzkowski, P., Rybacki, M. (2004): DNA content and genome composition of diploid and triploid water frogs belonging to the Rana esculenta complex (Amphibia, Anura). Can. J. Zool. 82: 1894-1901.
-
Pfennig, K.S. (2000): Female spadefoot toads compromise on mate quality to ensure conspecific matings. Behav. Ecol. 11: 220-227.
-
Plötner, J. (2005): Die westpaläarktischen Wasserfrösche. Laurenti, Bielefeld.
-
Randler, C. (2002): Avian hybridization, mixed pairing and female choice. Anim. Behav. 63: 103-119.
-
Reyer, H.-U., Frei, G., Som, C. (1999): Cryptic female choice: frogs reduce clutch size when amplexed by undesired males. Proc. R. Soc. Lond. B 266: 2101-2107.
-
Roesli, M., Reyer, H.-U. (2000): Male vocalisation and female choice in the hybridogenetic Rana lessonae/R. esculenta complex. Anim. Behav. 60: 745-755.
-
Rybacki, M., Berger, L. (2001): Types of water frog populations (Rana esculenta complex) in Poland. Mitt. Mus. Naturkunde Berl., Zoolog. Reihe 77: 51-57.
-
Schempp, W., Schmid, M. (1981): Chromosome banding in Amphibia. VI. BrdU-replication patterns in Anura and demonstration of XX-XY sex chromosomes in Rana esculenta. Chromosoma 83: 697-710.
-
Schröer, T. (1996): Morphologie und Ploidiegrade von Wasserfröschen aus unterschiedlichen Populationssystemen in Nordost-Polen. Z. Feldherpetol. 3: 133-150.
-
Schultz, R.J. (1969): Hybridization, unisexuallity, and polypoidy in the teleost Poeciliopsis (Poecilidae) and other vertebrates. Am. Nat. 103: 605-619.
-
Sherman, P.W., Reeve, H.K., Pfenning, D.W. (1997): Recognition systems. In: Behavioural Ecology: an Evolutionary Approach, p. 69-96, 4th Edition. Krebs, J.R., Davies, N.B., Eds, Blackwell, London.
-
Skierska, K. (2011): Dobór w pary i reprodukcja żab zielonych kompleksu Pelophylax esculentus w naturalnych populacjach mieszanych z udziałem P. lessonae i P. ridibundus. PhD thesis, University of Wrocław. (In Polish).
-
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.
-
Vorburger, C. (2001): Fixation of deleterious mutations in clonal lineages: evidence from hybridogenetic frogs. Evolution 55: 2319-2332.
-
Vorburger, C., Schmeller, D.S., Hotz, H., Guex, G.-D., Reyer, H.-U. (2009): Masked damage: mutational load in hemiclonal water frogs. In: Lost Sex. The Evolutionary Biology of Parthenogenesis, p. 433-446. Schön, I., Martens, K., van Dijk, P., Eds, Springer, Berlin.
-
Vrijenhoek, R.C., Parker Jr., E.D. (2009): Geographical parthenogenesis: general purpose genotypes and frozen niche variation. In: Lost Sex. The Evolutionary Biology of Parthenogenesis, p. 99-131. Schön, I., Martens, K., van Dijk, P., Eds, Springer, Berlin.
-
Zeisset, I., Rowe, G., Beebee, T.J.C. (2000): Polymerase chain reaction primers for microsatellite loci in the north European water frogs Rana ridibunda and R. lessonae. Mol. Ecol. 9: 1173-1174.
| All Time | Past 365 days | Past 30 Days | |
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Body size variation in hybrids among populations of European water frogs (Pelophylax esculentus complex) with different breeding systems
In: Amphibia-ReptiliaSearch for other papers by Adam Hermaniuk in
Current site
Google Scholar
PubMed
Search for other papers by Magdalena Czajkowska in
Current site
Google Scholar
PubMed
Search for other papers by Anetta Borkowska in
Current site
Google Scholar
PubMed
Search for other papers by Jan R.E. Taylor in
Current site
Google Scholar
PubMed
Abstract
In some populations, hybrids reproduce with a parental species by eliminating the genome of this species from their own germline and produce gametes that only contain the genome of the other parental species (sexual host). This mode of reproduction, known as hybridogenesis, leads to a conflict of interest between the two parties because the sexual host should avoid mating with the hybrid to prevent a reduction in reproductive success, whereas the hybrid depends on such matings for survival. We investigated European water frogs (Pelophylax esculentus complex), including hybrids (P. esculentus, genotype LR) and two sexual host species (P. lessonae, LL and P. ridibundus, RR). We hypothesized that to maximize fitness, hybrid males should be morphologically more similar to the sexual host that is preferred by females for successful reproduction. To test this hypothesis, we compared hybrid males in two different population types, L-E (hybrids coexist with LL) and L-E-R (hybrids coexist with both LL and RR). The latter was described in terms of genome composition, sex ratio, and mate choice preferences; the sex ratio of hybrids was significantly male-biased. We found that LR males from the L-E-R populations were significantly larger than those from the L-E, which makes them more similar to P. ridibundus, the largest species within the P. esculentus complex. We suggest that a larger body size of hybrid males may provide a reproductive advantage in the L-E-R population type, where the most common type of pair caught in the breeding season was LR males × RR females.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 620 | 178 | 29 |
| Full Text Views | 254 | 3 | 1 |
| PDF Views & Downloads | 221 | 10 | 2 |
