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3. SPERM COOPERATION

ON SPERM COOPERATION IN THE WOOD MOUSE

R.V. Short (University of Melbourne, AU) discusses sperm cooperation, the author making the following points:

1) After animals have mated, sperm in the female reproductive tract race to produce fertilization of an egg. Because sperm express little of their genetic make-up in their outward appearance, it is difficult to select the good from the bad. So it might be better for an individual's sperm to cooperate rather than compete with one another. For species in which females mate with multiple partners, this will be particularly true if the sperm of one male could unite to defeat those of its rivals.

2) Moore et al (2002) describe an amazing example of such altruistic behavior in the sperm of the common European wood mouse, Apodemus sylvaticus (Nature 418, 174 177; 2002). They find that hundreds or thousands of sperm link hooked structures on their heads and swim en masse in a train, which enables them to progress at almost twice the speed of a single sperm. These trains must break up before fertilization, so many of the component sperm commit genetic hara-kiri by undergoing a premature "acrosome reaction". This involves the release of enzymes that break down cell adhesion molecules, which also makes it impossible for the sperm concerned to fertilize the egg. Somewhere on the train -- perhaps the locomotive driver up front --there must be one acrosome-intact sperm that has retained its capacity to perform fertilization.

3) Sperm motility is ultimately driven by the engine of mitochondrial DNA in the sperm's midpiece. M Anderson and A Dixson (Nature 416, 496; 2002) have shown that in primates the volume of the sperm midpiece is highly correlated with relative testicular size and mating behavior, the most sexually athletic species having the largest mitochondrial midpieces to power their sperm. So we can look forward to further work to see whether the wood mice have vast mitochondrial midpieces to power their sperm trains, and whether the sperm of especially promiscuous primates such as chimpanzees would leave their human counterparts for dead in the Olympic swimming pool.

Nature 2002 418:137

Related Background:

EXCEPTIONAL SPERM COOPERATION IN THE WOOD MOUSE

The wood mouse, A. sylvaticus, is a murid rodent common throughout Western Europe, with a breeding season from February to October.

H. Moore et al (University of Sheffield, UK) discuss sperm cooperation, the authors making the following points:

1) 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 time(1). Among small mammals, multiple matings resulting in sperm competition and mixed paternity in littermates are believed to be widespread(1). 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 intense(2).

2) Several examples of sperm cooperation have been reported mainly in molluscs and insects(3,4). A possible exception in Mammalia is the spermatozoa of opossums that conjugate to form pairs during sperm maturation and disengage immediately before fertilization(5). Sperm will benefit from cooperation if "Hamilton's rule" is fulfilled. This depends on the probability of sperm survival in terms of reaching the site of fertilization and the difference in relatedness of cooperating sperm and other sperm competing for fertilization. For true altruism, the fertilizing capacity of one spermatozoon is compromised or sacrificed to benefit another; however, evidence in Eutheria has been largely lacking. Spermatozoa of some rodents (for example, guinea-pig) stack in rouleaux formation or agglutinate, but these cell associations do not appear particularly advantageous. Conversely, it has been suggested that a primary function of some spermatozoa in the rat and human ejaculate is to incapacitate spermatozoa of another male, so-called kamikaze spermatozoa; however, this hypothesis is not supported by experimental evidence.

3) In summary: The authors report the probable altruistic behavior 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. The authors propose that 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.

References (abridged):

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

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

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

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)

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)

Nature 2002 418:174

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