Skip to main content

Advertisement

Springer Nature Link
Log in

Variation in fertilisation abilities between hemiclonal hybrid and sexual parental males of sympatric water frogs (Rana lessonae, R. esculenta, R. ridibunda)

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

In many species, males and females mate with multiple partners, which gives rise to sperm competition and multiple paternity. The experiments on water frogs presented here demonstrate that such sperm competition can affect the structure and dynamics of mixed-species communities. The hybrid frog Rana esculenta (LR) mates with one of its parental species, usually R. lessonae (LL), although in some areas R. ridibunda (RR), to regain the premeiotically eliminated parental genome ("hybridogenesis"). Mixed LL/LR-populations are stable although hybrid numbers should continuously increase at the expense of parental animals, because of differences in female fecundity and other factors. This would finally lead to the extinction of the sexual host, followed by that of the sexual parasite, unless the reproductive superiority of R. esculenta is reduced by other factors, such as lower hybrid male fertility. Eggs from LL- and LR-females were fertilised in vitro by single- and multi-male sperm suspensions of LL-, LR- and RR-males. In all experiments, the proportion of offspring sired by R. esculenta sperm was significantly lower than that sired by R. lessonae or R. ridibunda sperm. Gonad mass, sperm morphology, sperm swimming velocity, and sperm survival did not explain these differences in fertilisation success; nor did gamete recognition and compatibility. Sperm density was the only trait that paralleled fertilisation success, but it offers no explanation either, because densities were equalised for the in-vitro fertilisations. In natural LL/LR populations, the significantly smaller amount, poorer competitive ability and lower long-term survival of R. esculenta compared to R. lessonae sperm will reduce the initial reproductive superiority of hybrids and contribute to the stabilisation of mixed water-frog populations. Differences in fertilisation ability are also likely to be relevant for the structure and dynamics of several other systems with encounters between eggs and sperm from different genotypes, ecotypes, ploidy levels and/or species.

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

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1a–c.
Fig. 2a–c.

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

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

    Google Scholar 

  • Al-Anzi B, Chandler DE (1998) A sperm chemoattractant is released from Xenopus egg jelly during spawning. Dev Biol 198:366–375

    Article  CAS  PubMed  Google Scholar 

  • Alves MJ, Coelho MM, Collares-Pereira MJ (2001) Evolution in action through hybridisation and polyploidy in an Iberian fresh water fish: a review. Genetica 211:375–385

    Article  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

  • Arnold MR (1997) Natural hybridization and evolution. Oxford University Press, Oxford

  • Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164

    Article  PubMed  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 1992:275–283

    Google Scholar 

  • Berger L (1973) Sexual maturity of males within forms of the Rana esculenta complex. Zool Pol 22:177–188

    Google Scholar 

  • Berger L (1977) Systematics and hybridization in the Rana esculenta complex. In: Taylor DH, Guttmann SI (eds) The reproductive biology of Amphibians. Plenum, New York, pp 367–388

  • Berger L, Rybacki M (1992) Sperm competition in European waterfrogs. Alytes 10:113–116

    Google Scholar 

  • Berger L, Rybacki M (1994) Sperm competition between two species of European waterfrogs (Rana ridibunda and Rana lessonae). Zool Pol 39:281–291

    Google Scholar 

  • Berger L, Uzzell T (1980) The eggs of European waterfrogs of the Rana esculenta-complex and their hybrids. Folia Biol 28:3–26

    CAS  Google Scholar 

  • Berger L, Rybacki M, Hotz H (1994) Artificial fertilisation of water frogs. Amphibia-Reptilia 15:408–413

    Google Scholar 

  • Birkhead TR (1998) Cryptic female choice; criteria for establishing female sperm choice. Evolution 52:1212–1218

    Google Scholar 

  • Blankenhorn HJ (1977) Reproduction and mating behavior in Rana lessonae-Rana esculenta mixed populations. In: Taylor DH, Guttmann SI (eds) The reproductive biology of Amphibians. Plenum, New York, pp 389–410

  • Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339

    CAS  Google Scholar 

  • Bullini L (1994) Origin and evolution of hybrid species. Trends Ecol Evol 9:422–426

    Google Scholar 

  • Coe M (1974) Observations on the ecology and breeding biology of the genus Chiromantis (Amphibia: Rhacophoridae). J Zool Lond 172:13–34

    Google Scholar 

  • Clutton-Brock TH, Parker GA (1995) Sexual coercion in animal societies. Anim Behav 49:1345–1365

    Article  Google Scholar 

  • Cummins JM, Woodall PF (1995) On mammalian sperm dimensions. J Reprod Fertil 75:153–175

    Google Scholar 

  • Cunningham EJA, Birkhead TR (1998) Sex roles and sexual selection. Anim Behav 56:1311–1321

    Google Scholar 

  • Dawley RM, Bogart JP (1989) Evolution and ecology of unisexual vertebrates, Bulletin 466. New York State Museum, Albany

  • D'Orgeix CA, Turner BJ (1995) Multiple paternity in the red-eyed treefrog Agalychnis callidryas (Cope). Mol Ecol 4:505–508

    CAS  PubMed  Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  • Ellstrand NC (1992) Gene flow by pollen: implications for plant conservation genetics. Oikos 63:77–86

    Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection and the evolution of mating systems. Science 197:215–223

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fukuyama K (1991) Spawning behaviour and male mating tactics of a foam-nesting treefrog, Rhacophorus arboreus. Anim Behav 42:193–199

    Google Scholar 

  • Gage MJG (1994) Association between body size, mating pattern, testis size and sperm length across butterflies. Proc R Soc Lond B 258:247–254

    Google Scholar 

  • Garcia-Varquez E, Moran P, Perez J, Martinez JL, Izquierdo JI, Gaudemar B de, Beall E (2002) Interspecific barriers between salmonids when hybridisation is due to sneak mating. Heredity 89:288–292

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gomendio M, Roldan ERS (1991) Sperm competition influences sperm size in mammals. Proc R Soc Lond B 243:181–185

    CAS  PubMed  Google Scholar 

  • Gowaty PA (1997) Sexual dialects, sexual selection, and variation in mating behavior. In: Gowaty PA (ed) Feminism and evolutionary biology: boundaries, intersections, and frontiers. Chapman and Hall, New York, pp 351–384

  • Graf J-D, Müller WP (1979) Experimental gynogenesis provides evidence of hybridogenetic reproduction in the Rana esculenta complex. Experientia 35:1574–1576

    CAS  PubMed  Google Scholar 

  • Grossenbacher K (1988) Verbreitungsatlas der Amphibien der Schweiz. Doc Faun Helvet 7:1–207

    Google Scholar 

  • Günther R (1973) Über die verwandtschaftlichen Beziehungen zwischen den europäischen Grünfröschen und den Bastardcharakter von Rana esculenta L. (Anura, Amphibia). Zool Anz 190:250–285

    Google Scholar 

  • Günther R (1990) Die Wasserfrösche Europas (Anuren-Froschlurche). Neue Brehm Bücherei, Wittenberg

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

    PubMed  Google Scholar 

  • Hebert PDN, Beaton MJ (1993) Methodologies for allozyme analysis using cellulose acetate electrophoresis. Helena Laboratories, Beaumont, Tex

  • 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 

  • Hettyey A, Pearman P (2003) Social environment and reproductive interference affect reproductive success of the red-listed frog, Rana latastei. Behav Ecol (in press)

  • Holenweg Peter A-K, Reyer H-U, Abt Tietje G (2002) Ecological factors affecting genotype and sex ratios in mixed populations of Rana lessonae, R. ridibunda and their hybridogenetic associate R. esculenta. Ecoscience 9:1–11

    Google Scholar 

  • Hotz H (1983) Genetic diversity among water frog genomes inherited with and without recombination. PhD Thesis, University of Zürich

  • Hotz H, Uzzell T, Berger L (1997) Linkage groups of protein-coding genes in western Palaearctic water frogs reveal extensive evolutionary conservation. Genetics 147:255–270

    CAS  PubMed  Google Scholar 

  • Jennions MD, Passmore NI (1992) Breeding behaviour of the African frog, Chiromantis xerampelina: multiple spawning and polyandry. Anim Behav 44:1091–1100

    Google Scholar 

  • Jennions MD, Passmore NI (1993) Sperm competition in frogs: testis size and a 'sterile male' experiment on Chiromantis xerampelina (Rhacophoridae). Biol J Linn Soc 50:211–220

    Article  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    CAS  Google Scholar 

  • Joly D, Cariou ML, Lachaise D (1991) Can female polyandry explain within-ejaculate dimorphism? In: Baccetti BD (ed) Comparative spermatology. Raven, New York

  • Kasuya E, Shigehara H, Hiroto M (1987) Mating aggregations in the Japanese treefrog, Rhacophorus arboreus (Anura: Rhacophoridae): a test of cooperation hypothesis. Zool Sci 4:693–697

    Google Scholar 

  • Katz DF, Drobnis EZ (1990) Analysis and interpretation of the forces generated by spermatozoa. In: Bavister BD, Cimmins J, Roldan ERS (eds) Fertilization in mammals. Sereno Symposia, Norwell, Mass, pp 125–137

  • Lambert CC (2000) Germ-cell warfare in ascidians: sperm from one species can interfere with the fertilization of a second species. Biol Bull 198:22–25

    CAS  PubMed  Google Scholar 

  • LaMunyon CW, Ward S (1998) Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc R Soc Lond B 265:1997–2002

    Article  PubMed  Google Scholar 

  • Laurila A, Seppä P (1998) Multiple paternity in the common frog (Rana temporaria): genetic evidence from tadpole kin groups. Biol J Linn Soc 63:221–232

    Article  Google Scholar 

  • Levitan DR (2000) Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc R Soc Lond B 267:531–534

    Article  CAS  PubMed  Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Parker GA (1984) Sperm competition and the evolution of animal mating strategies. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, London, pp 1–60

  • Parker GA (1990a) Sperm competition games: raffles and roles. Proc R Soc Lond B 242:120–126

    Google Scholar 

  • Parker GA (1990b) Sperm competition games: sneaks and extra-pair copulations. Proc R Soc Lond B 242:127–133

    Google Scholar 

  • Parker GA (1993) Sperm competition games: sperm size and sperm number under adult control. Proc R Soc Lond B 253:245–254

    CAS  PubMed  Google Scholar 

  • Pyburn WF (1970) Breeding behavior in the leaf-frogs Phyllomedusa callidryas and Phyllomedusa dacnicolor in Mexico. Copeia 1970:209–218

    Google Scholar 

  • Qvarström A, Forsgen E (1998) Should females prefer dominant males? Trends Ecol Evol 13:498–501

    Google Scholar 

  • Rakitin A, Ferguson MM, Trippel EA (1999) Sperm competition and fertilization success in Atlantic cod (Gadus morhua): effect of sire size and condition factor on gamete quality. Can J Fish Aquat Sci 56:2315–2323

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ribi G, Oertli S (2000) Frequency of interspecific matings and of hybrid offspring in sympatric populations of Viviparus ater and V. contectus (Mollusca: Prosobranchia). Biol J Linn Soc 71:133–143

    Article  Google Scholar 

  • Ritterbusch D, Bohlen J (2000) On the ecology of spined loach in Lake Muggelsee. Folia Zool 49:187–192

    Google Scholar 

  • Roberts JD, Standish RJ, Byrne PG, Doughty P (1999) Synchronous polyandry and multiple paternity in the frog Crinia georgiana (Anura: Myobatrachidae). Anim Behav 57:721–726

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Romeis B (1948) Mikroskopische Technik. Redaktion Oldenbourg, Munich

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

    Article  Google Scholar 

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

    Google Scholar 

  • Semlitsch RD, Reyer H-U (1992) Performance of tadpoles from the hybridogenetic Rana esculenta complex: interactions with pond drying and interspecific competition. Evolution 46:665–676

    Google Scholar 

  • Semlitsch RD, Hotz H, Guex GD (1997) Competition among tadpoles of coexisting hemiclones of hybridogenetic Rana esculenta: support for the frozen niche variation model. Evolution 51:1249–1261

    Google Scholar 

  • Sivinsky J (1984) Sperm in competition. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, New York, pp 85–115

  • Smuts BB, Smuts RW (1993) Male aggression and sexual coercion of females in nonhuman primates and other mammals, evidence and theoretical implications. Adv Stud Behav 22:1–63

    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 

  • SYSTAT (1998) Version 8.0 for Windows. SPSS, Chicago

  • Taborsky M (1998) Sperm competition in fish: 'bourgeois' males and parasitic spawning. Trends Ecol Evol 13:222–227

    Article  Google Scholar 

  • Thornhill R (1980) Rape in Panorpa scorpionflies and a general rape hypothesis. Anim Behav 28:52–59

    Google Scholar 

  • Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Vacquier VD, Carner KR, Stout CD (1990) Species-specific sequences of abalone lysin, the sperm protein that creates a hole in the egg envelope. Proc Natl Acad Sci Biol 87:5792–5796

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Vorburger C (2002) Fixation of deleterious mutations in clonal lineages: evidence from hybridogenetic frogs. Evolution 55:2319–2332

    Google Scholar 

  • Wells KD (1977) The social behaviour of anuran amphibians. Anim Behav 25:666–693

    Google Scholar 

  • Wirtz P (1999) Mother species-father species: unidirectional hybridization in animals. Anim Behav 58:1–12

    Article  PubMed  Google Scholar 

  • Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1052–1063

    Article  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 Rana lessonae. Mol Ecol 9:1173–1174

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to G. Schwarzenbach, M.-O. Wälti, A. Schwarzenbach, N. Ramer and B. Gruber for their help in catching frogs. C. Vorburger taught us how to perform in-vitro fertilisation and D. Hosken showed us everything we needed to know about sperm handling. S. Röthlisberger and T. Garner kindly introduced us to enzyme electrophoresis, PCR and other laboratory techniques; T. Garner also conducted the paternity analysis. M. Nakano patiently assisted in computerising sperm images and tracking sperm speed and C. Som kept the computers running. Last, but not least, we thank L. Martin, P. Pearman, and J. Van Buskirk for making useful suggestions on an earlier version of the paper. This study was conducted with approval and under the ethical guidelines of the "Veterinäramt Kanton Zürich" (licence number 88/99) and was financially supported through Swiss National Science Foundation grant 31-40688.94 to H.-U. Reyer, and a scholarship, the "Eidgenössische Stipendienkommission für Ausländische Studierende" to A. Hettyey.

Author information

Authors and Affiliations

  1. Zoological Institute, University of Zurich, Winterthurerstrasse 190, 8059 , Zurich, Switzerland

    Heinz-Ulrich Reyer & Bettina Niederer

  2. Behavioural Ecology Group, Department of Systematic Zoology and Ecology, Eötvös Loránd University, Pázmány Péter s. 1/c, 1117, Budapest , Hungary

    Attila Hettyey

Authors
  1. Heinz-Ulrich Reyer
    View author publications

    Search author on:PubMed Google Scholar

  2. Bettina Niederer
    View author publications

    Search author on:PubMed Google Scholar

  3. Attila Hettyey
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Heinz-Ulrich Reyer.

Additional information

Communicated by A. Mathis

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reyer, HU., Niederer, B. & Hettyey, A. Variation in fertilisation abilities between hemiclonal hybrid and sexual parental males of sympatric water frogs (Rana lessonae, R. esculenta, R. ridibunda). Behav Ecol Sociobiol 54, 274–284 (2003). https://doi.org/10.1007/s00265-003-0635-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-003-0635-y

Keywords