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Repeatability of sperm size in outbred and inbred Scathophaga stercoraria (Diptera: Scathophagidae)

Published online by Cambridge University Press:  02 April 2012

G. Bernasconi ,
P.I. Ward  and
B. Hellriegel
G. Bernasconi*
Affiliation:
Institute for Environmental Sciences, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
P.I. Ward
Affiliation:
Zoological Museum, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
B. Hellriegel
Affiliation:
Anthropological Institute and Museum, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
*
1Corresponding author (e-mail: [email protected]).
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Abstract

Variability in male gametic traits can depend on several genetic and environmental factors such as developmental instability as a consequence of inbreeding, developmental noise during spermatogenesis, or age- or condition-dependent changes in allocation to sperm cells. Variation in sperm size is particularly evident in species that produce more than one sperm morph but also occurs among males in sperm-monomorphic species. Both discrete and continuous sperm size variation have been implicated in male fertilization success when the sperm of several males directly compete for fertilization of the same set of ova. In this study, we investigated among-male variation in sperm length in field-collected, outbred male Scathophaga stercoraria (L.) flies, as well as in flies from the same natural population that had been subjected to 15 and 16 generations of inbreeding under laboratory conditions. Among-male variation in sperm length was significant and repeatable over subsequent matings in both inbred and outbred flies. We conclude that sperm length can be used as an individual male marker in sperm competition studies and that significant repeatability of sperm length supports heritability for this trait.

Résumé

La variation dans les caractéristiques des gamètes peut dépendre de plusieurs facteurs génétiques et environnementaux, tels que l'instabilité du développement causée par la consanguinité, les perturbations (bruit) dans le développement durant la spermatogenèse et les changements reliés à l'âge ou à la condition dans l'allocation des ressources aux cellules spermatiques. La variation dans la taille des spermatozoïdes est particulièrement évidente chez les espèces qui produisent plus d'un morphe de spermatozoïdes, mais elle est présente aussi chez les mâles à sperme monomorphe. Des variations, tant discrètes que continues, dans la taille des spermatozoïdes ont été invoquées pour expliquer le succès de la fécondation lorsque plusieurs mâles sont en compétition pour féconder la même masse d'oeufs. Dans notre étude, nous avons déterminé la variation d'un mâle à l'autre de la longueur des spermatozoïdes chez des mouches mâles Scathophaga stercoraria (L.) non consanguines et récoltées en nature, ainsi que chez des mouches provenant de la même population naturelle, mais élevées en laboratoire dans des conditions de consanguinité pendant 15 et 16 générations. La variation de la longueur des spermatozoïdes chez les mâles est significative et c'est un caractère qui se retrouve lors des accouplements subséquents, tant chez les mouches consanguines que non consanguines. La longueur des spermatozoïdes peut donc servir de marqueur mâle individuel lors des études de compétition spermatique et le fait que la longueur des spermatozoïdes se retrouve dans les générations suivantes est un indice qui appuie l'hypothèse qu'il s'agit d'une caractéristique héritable.

[Traduit par la Rédaction]

Type
Articles
Information
The Canadian Entomologist , Volume 139 , Issue 2 , April 2007 , pp. 228 - 234
Copyright
Copyright © Entomological Society of Canada 2007

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References

Bernasconi, G., and Hellriegel, B. 2005. Fertilization competence and sperm size variation in sperm-heteromorphic insects. Evolutionary Ecology, 19: 45–54.CrossRefGoogle Scholar
Bernasconi, M.V., Pawlowski, J., Valsangiacomo, C., Piffaretti, J.C., and Ward, P.I. 2001. Phylogeny of the genus Scathophaga (Diptera: Scathophagidae) inferred from mitochondrial DNA sequences. Canadian Journal of Zoology1, 79: 517–524.Google Scholar
Birkhead, T.R. 1998. Cryptic female choice: criteria for establishing female sperm choice. Evolution, 52: 1212–1218.CrossRefGoogle ScholarPubMed
Blanckenhorn, W.U., and Hellriegel, B. 2002. Against Bergmann's rule: fly sperm size increases with temperature. Ecology Letters, 5: 7–10.CrossRefGoogle Scholar
Briskie, J.V., Montgomery, R., and Birkhead, T.R. 1997. The evolution of sperm size in birds. Evolution, 51: 937–945.CrossRefGoogle ScholarPubMed
Cook, P.A., and Gage, M.J.G. 1995. Effects of risks of sperm competition on the numbers of eupyrene and apyrene sperm ejaculated by the moth Plodia interpunctella (Lepidoptera: Pyralidae). Behavioral Ecology and Sociobiology, 36: 261–268.CrossRefGoogle Scholar
Cummins, J., and Woodall, P. 1985. On mammalian sperm dimensions. Journal of Reproduction and Fertility, 75: 153–175.CrossRefGoogle ScholarPubMed
Foster, W. 1967. Hormonal-mediated nutritional control of sexual behavior in male dung flies. Science (Washington, D.C.), 158: 1597.CrossRefGoogle Scholar
Gage, M.J.G. 1994. Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proceedings of the Royal Society of London, Series B: Biological Sciences, 258: 247–254.Google Scholar
Gage, M.J.G., Stockley, P., and Parker, G. 1998. Sperm morphometry in the Atlantic salmon. Journal of Fish Biology, 53: 835–840.CrossRefGoogle Scholar
Hellriegel, B., and Bernasconi, G. 2000. Femalemediated differential sperm storage in a fly with complex spermathecae, Scathophaga stercoraria. Animal Behaviour, 59: 311–317.Google Scholar
Hellriegel, B., and Blanckenhorn, W.U. 2002. Environmental influences on the gametic investments of yellow dung fly males. Evolutionary Ecology, 16: 505–522.CrossRefGoogle Scholar
Joly, D., Korol, A., and Nevo, E. 2004. Sperm size evolution in Drosophila: inter- and intraspecific analysis. Genetica, 120: 233–240.CrossRefGoogle ScholarPubMed
Keller, L., and Waller, D. 2002. Inbreeding effects in wild populations. Trends in Ecology and Evolution, 17: 230–241.CrossRefGoogle Scholar
LaMunyon, C.W., and Ward, S. 1998. Larger sperm outcompete smaller sperm in the nematode Caenorhaditis elegans. Proceedings of the Royal Society of London, Series B: Biological Sciences, 265: 1997–2002.CrossRefGoogle Scholar
Lessells, C.M., and Boag, P.T. 1987. Unrepeatable repeatabilities — a common mistake. The Auk, 104: 116–121.CrossRefGoogle Scholar
Levitan, D.R. 1993. The importance of sperm limitation to the evolution of egg size in marine invertebrates. American Naturalist, 141: 517–536.CrossRefGoogle Scholar
Lewis, S.M., and Austad, S.N. 1990. Sources of intraspecific variation in sperm precedence in red flour beetles. American Naturalist, 135: 351–359.Google Scholar
Martin, O.Y., Hosken, D.J., and Ward, P.I. 2004. Post-copulatory sexual selection and female fitness in Scathophaga stercoraria. Proceedings of the Royal Society of London, Series B: Biological Sciences, 271: 353–359.Google Scholar
Morrow, E.H., and Gage, M.J.G. 2001. Consistent significant variation between individual males in spermatozoal morphometry. Journal of Zoology (London), 254: 147–153.CrossRefGoogle Scholar
Oppliger, A., Hosken, D.J., and Ribi, G. 1998. Snail sperm production characteristics vary with sperm competition risk. Proceedings of the Royal Society of London, Series B: Biological Sciences, 265: 1527–1534.CrossRefGoogle Scholar
Otronen, M., Reguera, R., and Ward, P. 1997. Sperm storage in the yellow dung fly Scathophaga stercoraria: identifying the sperm of competing males in separate female spermathecae. Ethology, 103: 844–854.Google Scholar
Packer, C., Pusey, A.E., Gilbert, D.A., Martenson, J., and O'Brien, S.J. 1991. Case study of a population bottle-neck: lions of Ngoronogoro Crater. Conservation Biology, 5: 219–230.Google Scholar
Parker, G.A. 1970. The reproductive behaviour and the nature of sexual selection in Scatophaga stercoraria. II. The fertilization rate and the spatial and temporal relationship of each sex around the site of mating and oviposition. Journal of Animal Ecology, 39: 205–228.Google Scholar
Parker, G.A. 1993. Sperm competition games: sperm size and sperm number under adult control. Proceedings of the Royal Society of London, Series B: Biological Sciences, 253: 245–254.Google ScholarPubMed
Patterson, H.D., and Thompson, R. 1971. Recovery of inter-block information when block sizes are unequal. Biometrika, 58: 545–554.Google Scholar
Pitnick, S., and Markow, T.A. 1994. Male gametic strategies: sperm size, testes size, and the allocation of ejaculate among successive mates by the sperm-limited fly Drosophila pachea and its relatives. American Naturalist, 143: 785–819.Google Scholar
Radwan, J., and Siva-Jothy, M.T. 1996. The function of post-insemination mate association in the bulb mite, Rhizoglyphus robini. Animal Behaviour, 52: 651–657.Google Scholar
Sait, S.M., Gage, M.J.G., and Cook, P. 1998. Effects of a fertility-reducing baculovirus on sperm numbers and sizes in the Indian meal moth, Plodia interpunctella. Functional Ecology, 12: 56–62.CrossRefGoogle Scholar
Silberglied, R.E., Shepherd, J.D., and Dickinson, J.L. 1984. Eunuchs: the role of apyrene sperm in Lepidoptera? American Naturalist, 123: 255–265.Google Scholar
Simmons, L.W. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, New Jersey.Google Scholar
Simmons, L.W., and Kotiaho, J.S. 2002. Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution, 56: 1622–1631.Google ScholarPubMed
Simmons, L.W., and Ward, P.I. 1991. The heritability of sexually dimorphic traits in the yellow dung fly Scathophaga stercoraria (L). Journal of evolutionary Biology, 4: 593–601.CrossRefGoogle Scholar
Simmons, L.W., Tomkins, J.L., and Hunt, J. 1999. Sperm competition games played by dimorphic male beetles. Proceedings of the Royal Society of London, Series B: Biological Sciences, 266: 145–150.Google Scholar
Simmons, L.W., Wernham, J., García-González, F., and Dan Kamien, D. 2003. Variation in paternity in the field cricket Teleogryllus oceanicus: no detectable influence of sperm numbers or sperm length, Behavioral Ecology, 14: 539–545.Google Scholar
Snook, R.R., and Karr, T. 1998. Only long sperm are fertilization competent in six sperm-heteromorphic Drosophila species. Current Biology, 8: 291–294.CrossRefGoogle ScholarPubMed
Ward, P.I. 1998. Intraspecific variation in sperm size characters. Heredity, 80: 655–659.Google Scholar
Ward, P. 2000 a. Sperm length is heritable and sexlinked in the yellow dung fly Scathophaga stercoraria (L.). Journal of Zoology (London), 251: 349–353.Google Scholar
Ward, P. 2000 b. Cryptic female choice in the yellow dung fly Scathophaga stercoraria (L.). Evolution, 54: 1680–1686.Google ScholarPubMed
Ward, P.I., and Hauschteck-Jungen, E. 1993. Variation in sperm length in the yellow dung fly Scathophaga stercoraria. Journal of Insect Physiology, 39: 545–547.Google Scholar
Wildt, D.E., Bush, M., Goodrowe, K.L., Packer, C., Pusey, A.E., Brown, J.L., Joslin, P., and Obrien, S.J. 1987 a. Reproductive and genetic consequences of founding isolated lion populations. Nature (London), 329: 328–331.CrossRefGoogle Scholar
Wildt, D.E., Obrien, S.J., Howard, J.G., Caro, T.M., Roelke, M.E., Brown, J.L., and Bush, M. 1987 b. Similarity in ejaculate-endocrine characteristics in captive versus free-ranging cheetahs of two subspecies. Biology of Reproduction, 36: 351–360.Google Scholar