Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Sperm morphology, motility and fertilisation capacity in the myobatrachid frog Crinia georgiana

Martin A. Dziminski A , J. D. Roberts A and Leigh W. Simmons A B

A Centre for Evolutionary Biology, School of Animal Biology (M092), The University of Western Australia, Crawley, WA 6009, Australia.

B Corresponding author. Email: lsimmons@cyllene.uwa.edu.au

Reproduction, Fertility and Development 22(3) 516-522 https://doi.org/10.1071/RD09124
Submitted: 22 May 2009  Accepted: 10 September 2009   Published: 12 February 2010

Abstract

Sperm traits have been found to vary between individuals within populations in a variety of taxa. Sperm motility, morphometry and viability may be expected to have important effects on male fertility, although previous studies have found varying patterns, especially in external fertilisers. In the present study, we examined the effects of sperm swimming velocity, the proportion of motile spermatozoa, sperm head and tail length and the proportion of live spermatozoa on fertilisation success in the externally fertilising myobatrachid frog Crinia georgiana using IVF techniques and by controlling sperm numbers. We found no effect of any of the sperm traits we measured on IVF success. Neither did we find any relationship between sperm morphology and sperm performance. There was a negative relationship between sperm viability and male body size, which could be a function of age or an alternative tactic of differential investment in spermatozoa by smaller-sized males using sneak tactics in multiple matings. In contrast with most externally fertilising aquatic organisms, high rates of fertilisation appear to be achieved in C. georgiana with relatively low sperm swimming speeds.

Additional keywords: anuran amphibians, fertility, sperm length, swimming velocity.


Acknowledgements

This research was funded by the Australian Research Council. The authors thank Beverly Roberts, Vicki Cartledge and Aimee Silla for help with the viability assays.


References

Au, D. W. T. , Chiang, M. W. L. , Tang, J. Y. M. , Yuen, B. B. H. , Wang, Y. L. , and Wu, R. S. S. (2002). Impairment of sea urchin sperm quality by UV-B radiation: predicting fertilization success from sperm motility. Mar. Pollut. Bull. 44, 583–589.
CrossRef | PubMed | CAS |

Burness, G. , Casselman, S. J. , Schulte-Hostedde, A. I. , Moyes, C. D. , and Montgomerie, R. (2004). Sperm swimming speed and energetics vary with sperm competition risk in bluegill. Behav. Ecol. Sociobiol. 56, 65–70.
CrossRef |

Byrne, P. G. (2002). Climatic correlates of breeding, simultaneous polyandry and potential for sperm competition in the frog Crinia georgiana. J. Herpetol. 36, 125–129.


Byrne, P. G. (2004). Male sperm expenditure under sperm competition risk and intensity in quacking frogs. Behav. Ecol. 15, 857–863.
CrossRef |

Byrne, P. G. , and Roberts, J. D. (1999). Simultaneous mating with multiple males reduces fertilization success in the myobatrachid frog Crinia georgiana. Proc. R. Soc. Lond. B Biol. Sci. 266, 717–721.
CrossRef |

Byrne, P. G. , and Roberts, J. D. (2004). Intrasexual selection and group spawning in quacking frogs (Crinia georgiana). Behav. Ecol. 15, 872–882.
CrossRef |

Casselman, S. J. , Schulte-Hostedde, A. I. , and Montgomerie, R. (2006). Sperm quality influences male fertilization success in walleye (Sander vitreus). Can. J. Fish. Aquat. Sci. 63, 2119–2125.
CrossRef |

Dziminski, M. A. , Roberts, J. D. , and Simmons, L. W. (2008). Fitness consequences of parental compatibility in the frog Crinia georgiana. Evolution 62, 879–886.
CrossRef | PubMed |

Dziminski, M. A. , Vercoe, P. E. , and Roberts, J. D. (2009). Variable offspring provisioning and fitness: a direct test in the field. Funct. Ecol. 23, 164–171.
CrossRef |

Edwards, D. L. , Mahony, M. J. , and Clulow, J. (2004). Effect of sperm concentration, medium osmolality and oocyte storage on artificial fertilisation success in a myobatrachid frog (Limnodynastes tasmaniensis). Reprod. Fertil. Dev. 16, 347–354.
CrossRef | PubMed | CAS |

Edwards, D. L. , Roberts, J. D. , and Keogh, S. J. (2007). Impact of Plio-Pleistocene arid cycling on the population history of a southwestern Australian frog. Mol. Ecol. 16, 2782–2796.
CrossRef | PubMed |

Fitzpatrick, J. L. , Desjardins, J. K. , Milligan, N. , Montgomerie, R. , and Balshine, S. (2007). Reproductive-tactic-specific variation in sperm swimming speeds in a shell-brooding cichlid. Biol. Reprod. 77, 280–284.
CrossRef | PubMed | CAS |

Fitzpatrick, J. L. , Montgomerie, R. , Desjardins, J. K. , Stiver, K. A. , Kolm, N. , and Balshine, S. (2009). Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc. Natl Acad. Sci. USA 106, 1128–1132.
CrossRef | PubMed | CAS |

Foote, R. H. (2003). Fertility estimation: a review of past experience and future prospects. Anim. Reprod. Sci. 75, 119–139.
CrossRef | PubMed |

Gage, M. J. G. , Macfarlane, C. P. , Yeates, S. , Ward, R. G. , Searle, J. B. , and Parker, G. A. (2004). Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr. Biol. 14, 44–47.
PubMed | |  CAS |

García-González, F. , and Simmons, L. W. (2005a). The evolution of polyandry: intrinsic sire effects contribute to embryo viability. J. Evol. Biol. 18, 1097–1103.
CrossRef | PubMed |

García-González, F. , and Simmons, L. W. (2005b). Sperm viability matters in insect sperm competition. Curr. Biol. 15, 271–275.
CrossRef | PubMed |

Garda, A. A. , Costa, G. C. , Colli, G. R. , and Báo, S. N. (2004). Spermatozoa of Pseudinae (Amphibia, Anura, Hylidae), with a test of the hypothesis that sperm ultrastructure correlates with reproductive modes in anurans. J. Morphol. 261, 196–205.
CrossRef | PubMed |

Gomendio, M. , Malo, A. F. , Garde, J. , and Roldan, E. R. S. (2007). Sperm traits and male fertility in natural populations. Reproduction 134, 19–29.
CrossRef | PubMed | CAS |

Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190.


Hettyey, A. , and Roberts, J. D. (2006). Sperm traits of the quacking frog, Crinia georgiana: intra- and interpopulation variation in a species with a high risk of sperm competition. Behav. Ecol. Sociobiol. 59, 389–396.
CrossRef |

Hettyey, A. , and Roberts, J. D. (2007). Sperm traits in the quacking frog (Crinia georgiana), a species with plastic alternative mating tactics. Behav. Ecol. Sociobiol. 61, 1303–1310.
CrossRef |

Humphries, S. , Evans, J. P. , and Simmons, L. W. (2008). Sperm competition: linking form to function. BMC Evol. Biol. 8, 319.
CrossRef | PubMed |

Johnson, D. D. P. , and Briskie, J. V. (1999). Sperm competition and sperm length in shorebirds. Condor 101, 848–854.
CrossRef |

Kupriyanova, E. , and Havenhand, J. N. (2002). Variation in sperm swimming behaviour and its effect on fertilization success in the serpulid polychaete Galeolaria caespitosa. Invertebr. Reprod. Dev. 4, 21–26.


Leclair, R. , Leclair, M. H. , Dubois, J. , and Daoust, J. L. (2000). Age and size of wood frogs, Rana sylvatica from Kuujjuarapik, northern Quebec. Can. Field Nat. 114, 381–387.


Lee, M. S. Y. , and Jamieson, B. G. M. (1992). The ultrastructure of the spermatozoa of three species of myobatrachid frogs (Anura, Amphibia) with phylogenetic considerations. Acta Zool. 73, 213–222.


Levitan D. R. (1998). Sperm limitation, gamete competition, and sexual selection in external fertilizers. In ‘Sperm Competition and Sexual Selection’. (Eds T. R. Birkhead and A. P. Møller.) pp. 175–217. (Academic Press: London.)

Levitan, D. R. (2000). Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc. R. Soc. Lond. B Biol. Sci. 267, 531–534.
CrossRef | CAS |

Locatello, L. , Pilastro, A. , Deana, R. , Zarpellon, A. , and Rasotto, M. B. (2007). Variation pattern of sperm quality traits in two gobies with alternative mating tactics. Funct. Ecol. 21, 975–981.
CrossRef |

Malo, A. F. , Garde, J. J. , Soler, A. J. , García, A. J. , Gomendio, M. , and Roldan, E. R. S. (2005). Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biol. Reprod. 72, 822–829.
CrossRef | PubMed | CAS |

Malo, A. F. , Gomendio, M. , Garde, J. , Lang-Lenton, B. , Soler, A. J. , and Roldan, E. R. S. (2006). Sperm design and sperm function. Biol. Lett. 2, 246–249.
CrossRef | PubMed |

Marconato, A. , and Shapiro, D. Y. (1996). Sperm allocation, sperm production and fertilization rates in the bucktooth parrotfish. Anim. Behav. 52, 971–980.
CrossRef |

Morrow, E. H. , and Gage, M. J. G. (2001). Consistent significant variation between individual males in spermatozoal morphometry. J. Zool. 254, 147–153.
CrossRef |

Oppliger, A. , Naciri-Graven, Y. , Ribi, G. , and Hosken, D. J. (2003). Sperm length influences fertilization success during sperm competition in the snail Viviparus ater. Mol. Ecol. 12, 485–492.
CrossRef | PubMed | CAS |

Parker, G. A. (1990). Sperm competition games: sneaks and extra-pair copulations. Proc. R. Soc. Lond. B Biol. Sci. 242, 127–133.
CrossRef |

Reinhardt, K. (2007). Evolutionary consequences of sperm cell aging. Q. Rev. Biol. 82, 375–393.
CrossRef | PubMed |

Reyer, H.-U. , Niederer, B. , and Hettyey, A. (2003). 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.
CrossRef |

Roberts, J. D. , Standish, R. J. , Byrne, P. G. , and Doughty, P. (1999). Synchronous polyandry and multiple paternity in the frog Crinia georgiana (Anura: Myobatrachidae). Anim. Behav. 57, 721–726.
CrossRef | PubMed |

Rudolfsen, G. , Figenschou, L. , Folstad, I. , and Kleven, O. (2008). Sperm velocity influence paternity in the Atlantic cod (Gadus morhua L.). Aquacult. Res. 39, 212–216.


Rugh R. (1962). ‘Experimental Embryology: Techniques and Procedures.’ (Burgess Publishing Company: Minneapolis.)

Schulte-Hostedde, A. I. , and Miller, J. S. (2004). Intraspecific variation in testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success. Behav. Ecol. Sociobiol. 55, 272–277.
CrossRef |

Simmons, L. W. , and Roberts, B. (2005). Bacterial immunity traded for sperm viability in male crickets. Science 309, 2031.
CrossRef | PubMed | CAS |

Simmons, L. W. , Roberts, J. D. , and Dziminski, M. A. (2009). Egg jelly influences sperm motility in the externally fertilizing frog, Crinea georgiana. J. Evol. Biol. 22, 225–229.
CrossRef | PubMed | CAS |

Smith, M. J. , and Roberts, J. D. (2003). No sexual size dimorphism in the frog Crinia georgiana (Anura: Myobatrachidae): an examination of pre- and postmaturational growth. J. Herpet. 37, 132–137.
CrossRef |

Stoltz, J. A. , and Neff, B. D. (2006). Sperm competition in a fish with external fertilization: the contribution of sperm number, speed and length. J. Evol. Biol. 19, 1873–1881.
CrossRef | PubMed | CAS |

Thomas, M. L. , and Simmons, L. W. (2007). Male crickets adjust the viability of their sperm in response to female mating status. Am. Nat. 170, 190–195.
CrossRef | PubMed |

Tuset, V. M. , Dietrich, G. J. , Wojtczak, M. , Slowinska, M. , de Monserrat, J. , and Ciereszko, A. (2008a). Relationships between morphology, motility and fertilization capacity in rainbow trout (Oncorhynchus mykiss) spermatozoa. J. Appl. Ichthyol. 24, 393–397.
CrossRef |

Tuset, V. M. , Trippel, E. A. , and de Monserrat, J. (2008b). Sperm morphology and its influence on swimming speed in Atlantic cod. J. Appl. Ichthyol. 24, 398–405.
CrossRef |

Urbach, D. , Bittner, D. , Lenz, T. L. , Bernet, D. , Wahli, T. , Wahli, T. , and Wedekind, C. (2007). Sperm velocity in an Alpine whitefish: effects of age, size, condition, fluctuating asymmetry and gonad abnormalities. J. Fish Biol. 71, 672–683.
CrossRef |

Vladić, T. V. , and Järvi, T. (2001). Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism. Proc. R. Soc. Lond. B Biol. Sci. 268, 2375–2381.
CrossRef |

Vladić, T. V. , Afzelius, B. A. , and Bronnikov, G. E. (2002). Sperm quality as reflected through morphology in salmon alternative life histories. Biol. Reprod. 66, 98–105.
CrossRef | PubMed |

Wolf, D. P. , and Hendrick, J. L. (1971). A molecular apprach to fertilisation. II. Viability and artificial fertilization of Xenopus laevis gametes. Dev. Biol. 25, 360–376.
CrossRef | PubMed | CAS |



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