Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Oct 25;91(22):10399–10402. doi: 10.1073/pnas.91.22.10399

Another way of being anisogamous in Drosophila subgenus species: giant sperm, one-to-one gamete ratio, and high zygote provisioning.

C Bressac 1, A Fleury 1, D Lachaise 1
PMCID: PMC45027  PMID: 7937962

Abstract

It is generally assumed that sexes in animals have arisen from a productivity versus provisioning conflict; males are those individuals producing gametes necessarily small, in excess, and individually bereft of all paternity assurance. A 1- to 2-cm sperm, 5-10 times as long as the male body, might therefore appear an evolutionary paradox. As a matter of fact, species of Drosophila of the Drosophila subgenus differ from those of other subgenera by producing exclusively sperm of that sort. We report counts of such giant costly sperm in Drosophila littoralis and Drosophila hydei females, indicating that they are offered in exceedingly small amounts, tending to a one-to-one gamete ratio after a single mating. As a result, most of them are successfully involved in a fertilization. Hence, the concept of "paternity assurance of individual sperm" arises. Evidence is further provided here that almost the entire sperm is incorporated into the egg during fertilization. Labeling with specific antibodies in fertilized eggs reveals intact axonemes up to late gastrulation. The question, then, is why selection has favored such an unusual strategy. Explanations related to some prefertilization functions are ruled out. It is therefore tentatively proposed that virtually every giant sperm constitutes a "direct paternal legacy to the embryo," which, in contrast to any male-derived nuptial gift, cannot be minimized by female remating. We suggest that dramatic shortage of giant sperm with a high prospect of fusion and increased zygote provisioning is merely another way of being anisogamous.

Full text

PDF
10399

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adoutte A., Delgado P., Fleury A., Levilliers N., Lainé M. C., Marty M. C., Boisvieux-Ulrich E., Sandoz D. Microtubule diversity in ciliated cells: evidence for its generation by post-translational modification in the axonemes of Paramecium and quail oviduct cells. Biol Cell. 1991;71(1-2):227–245. doi: 10.1016/0248-4900(91)90069-y. [DOI] [PubMed] [Google Scholar]
  2. BEATTY R. A. Fertility of mixed semen from different rabbits. J Reprod Fertil. 1960 Feb;1:52–60. doi: 10.1530/jrf.0.0010052. [DOI] [PubMed] [Google Scholar]
  3. Bedford J. M., Rodger J. C., Breed W. G. Why so many mammalian spermatozoa--a clue from marsupials? Proc R Soc Lond B Biol Sci. 1984 Apr 24;221(1223):221–233. doi: 10.1098/rspb.1984.0031. [DOI] [PubMed] [Google Scholar]
  4. Bell G. The evolution of anisogamy. J Theor Biol. 1978 Jul 20;73(2):247–270. doi: 10.1016/0022-5193(78)90189-3. [DOI] [PubMed] [Google Scholar]
  5. Birky C. W., Jr Relaxed cellular controls and organelle heredity. Science. 1983 Nov 4;222(4623):468–475. doi: 10.1126/science.6353578. [DOI] [PubMed] [Google Scholar]
  6. Bressac C., Joly D., Devaux J., Lachaise D. Can we predict the mating pattern of Drosophila females from the sperm length distribution in males? Experientia. 1991 Jan 15;47(1):111–114. doi: 10.1007/BF02041270. [DOI] [PubMed] [Google Scholar]
  7. Briskie J. V., Montgomerie R. Sperm size and sperm competition in birds. Proc Biol Sci. 1992 Feb 22;247(1319):89–95. doi: 10.1098/rspb.1992.0013. [DOI] [PubMed] [Google Scholar]
  8. Charlesworth B. The population genetics of anisogamy. J Theor Biol. 1978 Jul 20;73(2):347–357. doi: 10.1016/0022-5193(78)90195-9. [DOI] [PubMed] [Google Scholar]
  9. Cohen J. Why so many sperms? An essay on the arithmetic of reproduction. Sci Prog. 1969 Spring;57(225):23–41. [PubMed] [Google Scholar]
  10. Cosmides L. M., Tooby J. Cytoplasmic inheritance and intragenomic conflict. J Theor Biol. 1981 Mar 7;89(1):83–129. doi: 10.1016/0022-5193(81)90181-8. [DOI] [PubMed] [Google Scholar]
  11. Cummins J. M., Woodall P. F. On mammalian sperm dimensions. J Reprod Fertil. 1985 Sep;75(1):153–175. doi: 10.1530/jrf.0.0750153. [DOI] [PubMed] [Google Scholar]
  12. Curgy J. J., Anderson W. A. Synthèse d'ARN dans le chondriome au cours de la spermiogenèse chez la Drosophile. Z Zellforsch Mikrosk Anat. 1972;125(1):31–44. [PubMed] [Google Scholar]
  13. Eberhard W. G. Evolutionary consequences of intracellular organelle competition. Q Rev Biol. 1980 Sep;55(3):231–249. doi: 10.1086/411855. [DOI] [PubMed] [Google Scholar]
  14. Gomendio M., Roldan E. R. Sperm competition influences sperm size in mammals. Proc Biol Sci. 1991 Mar 22;243(1308):181–185. doi: 10.1098/rspb.1991.0029. [DOI] [PubMed] [Google Scholar]
  15. Hodgkin J., Barnes T. M. More is not better: brood size and population growth in a self-fertilizing nematode. Proc Biol Sci. 1991 Oct 22;246(1315):19–24. doi: 10.1098/rspb.1991.0119. [DOI] [PubMed] [Google Scholar]
  16. Hoekstra R. F. The evolution of sexes. Experientia Suppl. 1987;55:59–91. doi: 10.1007/978-3-0348-6273-8_3. [DOI] [PubMed] [Google Scholar]
  17. Hoekstra R. F. Why do organisms produce gametes of only two different sizes? Some theoretical aspects of the evolution of anisogamy. J Theor Biol. 1980 Dec 21;87(4):785–793. doi: 10.1016/0022-5193(80)90117-4. [DOI] [PubMed] [Google Scholar]
  18. Karr T. L. Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech Dev. 1991 Jun;34(2-3):101–111. doi: 10.1016/0925-4773(91)90047-a. [DOI] [PubMed] [Google Scholar]
  19. Kondo R., Satta Y., Matsuura E. T., Ishiwa H., Takahata N., Chigusa S. I. Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics. 1990 Nov;126(3):657–663. doi: 10.1093/genetics/126.3.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Markow T. A., Ankney P. F. Drosophila males contribute to oogenesis in a multiple mating species. Science. 1984 Apr 20;224(4646):302–303. doi: 10.1126/science.224.4646.302. [DOI] [PubMed] [Google Scholar]
  21. Moore T., Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 1991 Feb;7(2):45–49. doi: 10.1016/0168-9525(91)90230-N. [DOI] [PubMed] [Google Scholar]
  22. Parker G. A., Baker R. R., Smith V. G. The origin and evolution of gamete dimorphism and the male-female phenomenon. J Theor Biol. 1972 Sep;36(3):529–553. doi: 10.1016/0022-5193(72)90007-0. [DOI] [PubMed] [Google Scholar]
  23. Parker G. A. Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J Theor Biol. 1982 May 21;96(2):281–294. doi: 10.1016/0022-5193(82)90225-9. [DOI] [PubMed] [Google Scholar]
  24. Partridge L., Harvey P. H. Evolutionary biology. What the sperm count costs. Nature. 1992 Dec 3;360(6403):415–415. doi: 10.1038/360415a0. [DOI] [PubMed] [Google Scholar]
  25. Perotti M. E. The mitochondrial derivative of the spermatozoon of Drosophila before and after fertilization. J Ultrastruct Res. 1973 Aug;44(3):181–198. doi: 10.1016/s0022-5320(73)80055-3. [DOI] [PubMed] [Google Scholar]
  26. Racey P. A. The prolonged storage and survival of spermatozoa in Chiroptera. J Reprod Fertil. 1979 May;56(1):391–402. doi: 10.1530/jrf.0.0560391. [DOI] [PubMed] [Google Scholar]
  27. Synnott A. L., Fulkerson W. J., Lindsay D. R. Sperm output by rams and distribution amongst ewes under conditions of continual mating. J Reprod Fertil. 1981 Mar;61(2):355–361. doi: 10.1530/jrf.0.0610355. [DOI] [PubMed] [Google Scholar]
  28. Van Voorhies W. A. Production of sperm reduces nematode lifespan. Nature. 1992 Dec 3;360(6403):456–458. doi: 10.1038/360456a0. [DOI] [PubMed] [Google Scholar]
  29. Zouros E., Freeman K. R., Ball A. O., Pogson G. H. Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature. 1992 Oct 1;359(6394):412–414. doi: 10.1038/359412a0. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES