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Exceptional sperm cooperation in the wood mouse

Abstract

Spermatozoa from a single male will compete for fertilization of ova with spermatozoa from another male when present in the female reproductive tract at the same time1. Close genetic relatedness predisposes individuals towards altruism, and as haploid germ cells of an ejaculate will have genotypic similarity of 50%, it is predicted that spermatozoa may display cooperation and altruism to gain an advantage when inter-male sperm competition is intense2. We report here the probable altruistic behaviour of spermatozoa in an eutherian mammal. Spermatozoa of the common wood mouse, Apodemus sylvaticus, displayed a unique morphological transformation resulting in cooperation in distinctive aggregations or ‘trains’ of hundreds or thousands of cells, which significantly increased sperm progressive motility. Eventual dispersal of sperm trains was associated with most of the spermatozoa undergoing a premature acrosome reaction. Cells undergoing an acrosome reaction in aggregations remote from the egg are altruistic in that they help sperm transport to the egg but compromise their own fertilizing ability.

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Figure 1: Morphology of wood mouse sperm head.
Figure 2: Development of sperm train.
Figure 3: The change in progressive motility (average path velocity) of sperm trains (solid line) and single spermatozoa (dotted line) with increasing viscosity of medium.
Figure 4: Histogram of the proportion of spermatozoa displaying deployment of the apical hook, the acrosome reaction and hyperactivated motility in relation to sperm aggregation in vitro at different time points.

References

  1. 1

    Birkhead, T. R. & Moller, A. P. Sperm Competition and Sexual Selection (Academic, London, 1996)

    Google Scholar 

  2. 2

    Trivers, R. Social Evolution (Benjamin Cummings, California, 1985)

    Google Scholar 

  3. 3

    Sivinski, J. in Sperm Competition and the Evolution of Animal Mating Systems (ed. Smith, R. L.) 223–249 (Academic, Orlando, 1984)

    Google Scholar 

  4. 4

    Hayashi, F. Insemination through an externally attached spermatophore: bundled sperm and post-copulatory mate guarding by male fishflies (Megaloptera: corydalidae). J. Insect Physiol. 42, 859–866 (1996)

    CAS  Article  Google Scholar 

  5. 5

    Moore, H. D. Gamete biology of the new world marsupial, the grey short-tailed opossum, Monodelphis domestica. Reprod. Fertil. Dev. 8, 605–615 (1996)

    CAS  Article  Google Scholar 

  6. 6

    Hamilton, W. D. The genetical evolution of social behaviour. I. J. Theor. Biol. 7, 1–16 (1964)

    CAS  Article  Google Scholar 

  7. 7

    Shepherd, B. A. & Martan, J. Morphology and fertility of guinea-pig spermatozoa aged in vivo. Arch. Androl. 2, 53–58 (1979)

    CAS  Article  Google Scholar 

  8. 8

    Baker, R. R. & Bellis, M. A. Kamikaze sperm in mammals? Anim. Behav. 36, 936–939 (1988)

    Article  Google Scholar 

  9. 9

    Baker, R. R. & Bellis, M. A. Human Sperm Competition (Chapman Hall, London, 1995)

    Google Scholar 

  10. 10

    Moore, H. D., Martin, M. & Birkhead, T. R. No evidence for killer sperm or other selective interactions between human spermatozoa in ejaculates of different males in vitro. Proc. R. Soc. Lond. B 266, 2243–2350 (1999)

    Google Scholar 

  11. 11

    Hanak, V. & Mazak, V. Mammals (Aventinum, Prague, 1979)

    Google Scholar 

  12. 12

    Breed, W. G. & Taylor, J. Body mass, testes mass and sperm size in murine rodents. J. Mamm. 81, 758–768 (2000)

    Article  Google Scholar 

  13. 13

    Bedford, J. M. in The Spermatozoon (eds Fawcett, D. W. & Bedford, J. M.) 7–21 (Urban and Schwarzenberg, Baltimore, 1979)

    Google Scholar 

  14. 14

    Harcourt, A. H., Harver, P. H., Larson, S. G. & Short, R. V. Testes weight, body weight and breeding systems in primates. Nature 293, 55–57 (1981)

    ADS  CAS  Article  Google Scholar 

  15. 15

    Tew, T. E. & Macdonald, D. W. Dynamics of space use and male vigor amongst wood mice, Apodemus sylvaticus in the cereal ecosystem. Behav. Ecol. Sociobiol. 34, 337–345 (1994)

    Article  Google Scholar 

  16. 16

    Yanagimachi, R. in Physiology of Reproduction (eds Knobil, E. & Neil, J.) 189–317 (Raven Press, New York, 1994)

    Google Scholar 

  17. 17

    Friend, G. F. The sperms of British muridae. Quart. J. Micro. Sci. 78, 419–443 (1936)

    Google Scholar 

  18. 18

    Moore, H. D., Hartman, T. D., Brown, A. C., Smith, C. A. & Ellis, D. A. Expression of sperm antigens during spermatogenesis and maturation detected with monoclonal antibodies. Exp. Clin. Immunogenet. 2, 84–96 (1985)

    CAS  Google Scholar 

  19. 19

    Fraser, L. R. & Drury, L. M. The relationship between sperm concentration and fertilisation in vitro of mouse eggs. Biol. Reprod. 13, 513–518 (1975)

    CAS  Article  Google Scholar 

  20. 20

    Moore, H. D. & Akhondi, M. A. Fertilizing capacity of rat spermatozoa is correlated with decline in straight-line velocity measured by continuous computer-aided sperm analysis. J. Androl. 17, 50–60 (1996)

    CAS  Google Scholar 

  21. 21

    Holt, C., Holt, W. V., Moore, H. D., Reed, H. C. & Curnock, R. M. Objectively measured boar sperm parameters correlate with the outcome of on-farm inseminations. Results of two fertility trials. J. Androl. 18, 312–323 (1996)

    Google Scholar 

  22. 22

    Birkhead, T. R., Martinez, J. G., Burke, T. & Froman, D. P. Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc. R. Soc. Lond. B 266, 1–6 (1999)

    Article  Google Scholar 

  23. 23

    Dawkins, R. The Selfish Gene (Oxford Univ. Press, Oxford, 1976)

    Google Scholar 

  24. 24

    Haig, D. Gestational drive and green-bearded placenta. Proc. Natl Acad. Sci. USA 93, 6547–6551 (1996)

    ADS  CAS  Article  Google Scholar 

  25. 25

    De Kretser, D. M. & Kerr, J. B. in Physiology of Reproduction (eds Knobil, E. & Neil, J.) 1177–1290 (Raven Press, New York, 1994)

    Google Scholar 

  26. 26

    Kleene, K. C. A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mech. Dev. 106, 3–23 (2001)

    CAS  Article  Google Scholar 

  27. 27

    Kim, E., Waters, S. H., Hake, L. E. & Hecht, N. B. Identification and developmental expression of a smooth muscle gamma-actin in post-meiotic male germ cells of mice. Mol. Cell Biol. 9, 1875–1881 (1989)

    CAS  Article  Google Scholar 

  28. 28

    Xu, X., Toselli, P. A., Russell, L. D. & Seldin, D. C. Globozoospermia in mice lacking the casein kinase II α catalytic subunit. Nature Genet. 23, 118–121 (1999)

    CAS  Article  Google Scholar 

  29. 29

    Wassarman, P. M., Jovine, L. & Litscher, E. S. A profile of fertilization in mammals. Nature Cell Biol. 3, E59–E64 (2000)

    Article  Google Scholar 

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Acknowledgements

We thank J. Waters for advice on wood mice husbandry. K.D. was supported by an Erasmus Exchange studentship.

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Correspondence to Harry Moore.

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Moore, H., Dvoráková, K., Jenkins, N. et al. Exceptional sperm cooperation in the wood mouse. Nature 418, 174–177 (2002). https://doi.org/10.1038/nature00832

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