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 http://dx.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.


References

Au D. W. T.Chiang M. W. L.Tang J. Y. M.Yuen B. B. H.Wang Y. L.Wu R. S. S.2002Impairment of sea urchin sperm quality by UV-B radiation: predicting fertilization success from sperm motility.Mar. Pollut. Bull.44583589doi:10.1016/S0025-326X(01)00288-0Pubmed Abstract

Burness G.Casselman S. J.Schulte-Hostedde A. I.Moyes C. D.Montgomerie R.2004Sperm swimming speed and energetics vary with sperm competition risk in bluegill.Behav. Ecol. Sociobiol.566570doi:10.1007/S00265-003-0752-7

Byrne P. G.2002Climatic correlates of breeding, simultaneous polyandry and potential for sperm competition in the frog Crinia georgiana.J. Herpetol.36125129

Byrne P. G.2004Male sperm expenditure under sperm competition risk and intensity in quacking frogs.Behav. Ecol.15857863
doi:10.1093/BEHECO/ARH098

Byrne P. G.Roberts J. D.1999Simultaneous mating with multiple males reduces fertilization success in the myobatrachid frog Crinia georgiana.Proc. R. Soc. Lond. B Biol. Sci.266717721doi:10.1098/RSPB.1999.0695

Byrne P. G.Roberts J. D.2004Intrasexual selection and group spawning in quacking frogs (Crinia georgiana).Behav. Ecol.15872882doi:10.1093/BEHECO/ARH100

Casselman S. J.Schulte-Hostedde A. I.Montgomerie R.2006Sperm quality influences male fertilization success in walleye (Sander vitreus).Can. J. Fish. Aquat. Sci.6321192125doi:10.1139/F06-108

Dziminski M. A.Roberts J. D.Simmons L. W.2008Fitness consequences of parental compatibility in the frog Crinia georgiana.Evolution62879886doi:10.1111/J.1558-5646.2008.00328.X

Dziminski M. A.Vercoe P. E.Roberts J. D.2009Variable offspring provisioning and fitness: a direct test in the field.Funct. Ecol.23164171doi:10.1111/J.1365-2435.2008.01480.X

Edwards D. L.Mahony M. J.Clulow J.2004Effect of sperm concentration, medium osmolality and oocyte storage on artificial fertilisation success in a myobatrachid frog (Limnodynastes tasmaniensis).Reprod. Fertil. Dev.16347354doi:10.1071/RD02079Pubmed Abstract

Edwards D. L.Roberts J. D.Keogh S. J.2007Impact of Plio-Pleistocene arid cycling on the population history of a southwestern Australian frog.Mol. Ecol.1627822796doi:10.1111/J.1365-294X.2007.03374.XPubmed Abstract

Fitzpatrick J. L.Desjardins J. K.Milligan N.Montgomerie R.Balshine S.2007Reproductive-tactic-specific variation in sperm swimming speeds in a shell-brooding cichlid.Biol. Reprod.77280284doi:10.1095/BIOLREPROD.106.059550Pubmed Abstract

Fitzpatrick J. L.Montgomerie R.Desjardins J. K.Stiver K. A.Kolm N.Balshine S.2009Female promiscuity promotes the evolution of faster sperm in cichlid fishes.Proc. Natl Acad. Sci. USA10611281132doi:10.1073/PNAS.0809990106Pubmed Abstract

Foote R. H.2003Fertility estimation: a review of past experience and future prospects.Anim. Reprod. Sci.75119139doi:10.1016/S0378-4320(02)00233-6Pubmed Abstract

Gage M. J. G.Macfarlane C. P.Yeates S.Ward R. G.Searle J. B.Parker G. A.2004Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success.Curr. Biol.144447Pubmed Abstract

García-González F.Simmons L. W.2005aThe evolution of polyandry: intrinsic sire effects contribute to embryo viability.J. Evol. Biol.1810971103doi:10.1111/J.1420-9101.2005.00889.XPubmed Abstract

García-González F.Simmons L. W.2005bSperm viability matters in insect sperm competition.Curr. Biol.15271275doi:10.1016/J.CUB.2005.01.032Pubmed Abstract

Garda A. A.Costa G. C.Colli G. R.Báo S. N.2004Spermatozoa of Pseudinae (Amphibia, Anura, Hylidae), with a test of the hypothesis that sperm ultrastructure correlates with reproductive modes in anurans.J. Morphol.261196205doi:10.1002/JMOR.10238Pubmed Abstract

Gomendio M.Malo A. F.Garde J.Roldan E. R. S.2007Sperm traits and male fertility in natural populations.Reproduction1341929doi:10.1530/REP-07-0143Pubmed Abstract

Gosner K. L.1960A simplified table for staging anuran embryos and larvae with notes on identification.Herpetologica16183190

Hettyey A.Roberts J. D.2006Sperm traits of the quacking frog, Crinia georgiana: intra- and interpopulation variation in a species with a high risk of sperm competition.Behav. Ecol. Sociobiol.59389396
doi:10.1007/S00265-005-0062-3

Hettyey A.Roberts J. D.2007Sperm traits in the quacking frog (Crinia georgiana), a species with plastic alternative mating tactics.Behav. Ecol. Sociobiol.6113031310doi:10.1007/S00265-007-0361-Y

Humphries S.Evans J. P.Simmons L. W.2008Sperm competition: linking form to function.BMC Evol. Biol.8319doi:10.1186/1471-2148-8-319Pubmed Abstract

Johnson D. D. P.Briskie J. V.1999Sperm competition and sperm length in shorebirds.Condor101848854doi:10.2307/1370074

Kupriyanova E.Havenhand J. N.2002Variation in sperm swimming behaviour and its effect on fertilization success in the serpulid polychaete Galeolaria caespitosa.Invertebr. Reprod. Dev.42126

Leclair R.Leclair M. H.Dubois J.Daoust J. L.2000Age and size of wood frogs, Rana sylvatica from Kuujjuarapik, northern Quebec.Can. Field Nat.114381387


Lee M. S. Y.Jamieson B. G. M.1992The ultrastructure of the spermatozoa of three species of myobatrachid frogs (Anura, Amphibia) with phylogenetic considerations.Acta Zool.73213222


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.2000Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus.Proc. R. Soc. Lond. B Biol. Sci.267531534
doi:10.1098/RSPB.2000.1032

Locatello L.Pilastro A.Deana R.Zarpellon A.Rasotto M. B.2007Variation pattern of sperm quality traits in two gobies with alternative mating tactics.Funct. Ecol.21975981doi:10.1111/J.1365-2435.2007.01314.X

Malo A. F.Garde J. J.Soler A. J.García A. J.Gomendio M.Roldan E. R. S.2005Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa.Biol. Reprod.72822829doi:10.1095/BIOLREPROD.104.036368Pubmed Abstract

Malo A. F.Gomendio M.Garde J.Lang-Lenton B.Soler A. J.Roldan E. R. S.2006Sperm design and sperm function.Biol. Lett.2246249doi:10.1098/RSBL.2006.0449Pubmed Abstract

Marconato A.Shapiro D. Y.1996Sperm allocation, sperm production and fertilization rates in the bucktooth parrotfish.Anim. Behav.52971980doi:10.1006/ANBE.1996.0245

Morrow E. H.Gage M. J. G.2001Consistent significant variation between individual males in spermatozoal morphometry.J. Zool.254147153doi:10.1017/S0952836901000656

Oppliger A.Naciri-Graven Y.Ribi G.Hosken D. J.2003Sperm length influences fertilization success during sperm competition in the snail Viviparus ater.Mol. Ecol.12485492doi:10.1046/J.1365-294X.2003.01748.XPubmed Abstract

Parker G. A.1990Sperm competition games: sneaks and extra-pair copulations.Proc. R. Soc. Lond. B Biol. Sci.242127133doi:10.1098/RSPB.1990.0115

Reinhardt K.2007Evolutionary consequences of sperm cell aging.Q. Rev. Biol.82375393doi:10.1086/522811Pubmed Abstract

Reyer H.-U.Niederer B.Hettyey A.2003Variation in fertilisation abilities between hemiclonal hybrid and sexual parental males of sympatric water frogs (Rana lessonae, R. esculenta, R. ridibunda).Behav. Ecol. Sociobiol.54274284

Roberts J. D.Standish R. J.Byrne P. G.Doughty P.1999Synchronous polyandry and multiple paternity in the frog Crinia georgiana (Anura: Myobatrachidae).Anim. Behav.57721726
doi:10.1006/ANBE.1998.1019Pubmed Abstract

Rudolfsen G.Figenschou L.Folstad I.Kleven O.2008Sperm velocity influence paternity in the Atlantic cod (Gadus morhua L.).Aquacult. Res.39212216

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

Schulte-Hostedde A. I.Miller J. S.2004Intraspecific variation in testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success.Behav. Ecol. Sociobiol.55272277
doi:10.1007/S00265-003-0707-Z

Simmons L. W.Roberts B.2005Bacterial immunity traded for sperm viability in male crickets.Science3092031doi:10.1126/SCIENCE.1114500Pubmed Abstract

Simmons L. W.Roberts J. D.Dziminski M. A.2009Egg jelly influences sperm motility in the externally fertilizing frog, Crinea georgiana.J. Evol. Biol.22225229doi:10.1111/J.1420-9101.2008.01628.XPubmed Abstract

Smith M. J.Roberts J. D.2003No sexual size dimorphism in the frog Crinia georgiana (Anura: Myobatrachidae): an examination of pre- and postmaturational growth.J. Herpet.37132137

Stoltz J. A.Neff B. D.2006Sperm competition in a fish with external fertilization: the contribution of sperm number, speed and length.J. Evol. Biol.1918731881
doi:10.1111/J.1420-9101.2006.01165.XPubmed Abstract

Thomas M. L.Simmons L. W.2007Male crickets adjust the viability of their sperm in response to female mating status.Am. Nat.170190195doi:10.1086/519404Pubmed Abstract

Tuset V. M.Dietrich G. J.Wojtczak M.Slowinska M.de Monserrat J.Ciereszko A.2008aRelationships between morphology, motility and fertilization capacity in rainbow trout (Oncorhynchus mykiss) spermatozoa.J. Appl. Ichthyol.24393397doi:10.1111/J.1439-0426.2008.01145.X

Tuset V. M.Trippel E. A.de Monserrat J.2008bSperm morphology and its influence on swimming speed in Atlantic cod.J. Appl. Ichthyol.24398405doi:10.1111/J.1439-0426.2008.01125.X

Urbach D.Bittner D.Lenz T. L.Bernet D.Wahli T.Wahli T.Wedekind C.2007Sperm velocity in an Alpine whitefish: effects of age, size, condition, fluctuating asymmetry and gonad abnormalities.J. Fish Biol.71672683doi:10.1111/J.1095-8649.2007.01537.X

Vladić T. V.Järvi T.2001Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism.Proc. R. Soc. Lond. B Biol. Sci.26823752381doi:10.1098/RSPB.2001.1768

Vladić T. V.Afzelius B. A.Bronnikov G. E.2002Sperm quality as reflected through morphology in salmon alternative life histories.Biol. Reprod.6698105doi:10.1095/BIOLREPROD66.1.98Pubmed Abstract

Wolf D. P.Hendrick J. L.1971A molecular apprach to fertilisation. II. Viability and artificial fertilization of Xenopus laevis gametes.Dev. Biol.25360376doi:10.1016/0012-1606(71)90037-6Pubmed Abstract



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