How We Do It

The evolution and future of human reproduction

Kamikaze Sperms or Flawed Products?

Why do men produce so many defective sperms?

Astoundingly, the average human ejaculate contains about 250 million sperms. And studies have revealed that fertility increasingly falls as the total count declines below 70 million (see my May 21 post "Sperm Counts Updated"). Successful fertilization clearly needs vast numbers of sperms. Yet there is another, equally stunning fact: Many sperms in an average human ejaculate are malformed. Substantial evidence shows that the optimal human sperm has an oval head, a medium-sized midpiece and a fairly long, straight tail. But many sperms in a human ejaculate are markedly different in shape. Common defects include rounded, tapered, lumpy, double, undersized or oversized heads, midpieces that are too small or too large, and stunted, coiled or doubled tails. Why do we need vast numbers of sperms if so many are evidently defective?

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Sperm defects in Humans and Apes

The unusual prevalence of defective sperm in human semen was first clearly recognized in 1974 by J. Michael Bedford in a broad review of comparisons with other primates. Bedford stated that abnormal sperms in human ejaculates are far more common than in other mammals, wild or domestic, and suggested that clothing might be responsible. Three years later, Hectór Seuánez and colleagues published a landmark paper reporting on semen analyses for all great apes in comparison to humans. They showed that levels of defective sperms were far lower in bonobos (2%), common chimpanzees (4.5%) and orangutans (1.5%) than in humans (27%). But the level in gorillas (29%) was very close to that in humans. This rules out the suggestion that the high level of defective sperms in human semen is attributable to clothing. In 1981, Björn Afzelius followed up with an interesting discussion, referring to “an abundance of abnormal sperm cells in the human ejaculate, with 20-35% structurally abnormal spermatozoa even in fully fertile men, compared to less than 5% in most other species". He noted five possible causes of defects: (1) clothing; (2) heating of the scrotum; (3) environmental contaminants; (4) degeneration; (5) mating habits.

Confusingly, the proportion of sperms in human ejaculates recognized as “normal” has decreased steadily since the 1970s. Whereas it was originally thought that about 70% of sperms lack visible abnormalities, the latest figures using strict criteria indicate that in fertile men only 4% of sperms are free of defects. The new criteria are based on the appearance of sperms that manage to survive migration through cervical mucus.

The kamikaze hypothesis

Proceeding from the notion that deviant sperms might be linked to mating habits, in 1988 Robin Baker and Mark Bellis proposed that different kinds of sperms might be adapted for different functions. They suggested that most are adapted for a “kamikaze” role, to block sperms of other males while only a few sperms in an ejaculate are “egg-getters”. The following year, in response to a challenge from Sandy Harcourt, Baker and Bellis expanded their hypothesis. In particular, they speculated that egg-getters “may be the least, not the most, common sperm in an ejaculate” and hence not normally shaped, and opined that “far from being egg-getters, the so-called ‘normal’ sperm are actually the most important of the kamikaze morphs.” Subsequently, in their 1995 book, Baker and Bellis expanded their hypothesis even further, dividing kamikaze sperms into two categories, some with coiled tails to block channels in cervical mucus and others with normal shape serving to seek and destroy. They reported on experimental mixing of semen samples from two men, which apparently increased the proportion of dead and coiled-tail sperms. Evidence was also cited indicating a positive relationship between conception and large-headed sperms. Unfortunately for the hypothesis, careful experiments on ejaculate mixing published by Harry Moore and colleagues in 1999 provided no confirmation. They “observed very few significant changes in sperm aggregation or performance in mixtures of sperm from different males compared with mixtures from the same male and none that were consistent with previously reported findings." An incisive 1998 review of the Baker and Bellis book Human Sperm Competition by Roger Short made the telling point that relatively rare large-headed sperms in human ejaculates have a double set of chromosomes, with disastrous consequences for fertilization. So much for the kamikaze hypothesis.

Defective sperms are due to poor quality control

In fact, it is now abundantly clear that the high level of defective sperms in human ejaculates reflects poor quality management, not evolution of different kinds for different functions. As Alan Dixson notes, adding to findings from Harcourt, Short and others, kamikaze sperm should surely be most abundant in species facing intense sperm competition. Yet defective sperms are much less common in chimpanzees and bonobos, which mate promiscuously and have notably large testes to yield particularly large numbers of sperms (see my August 7 post Sperm Wars: Dispatch from a Conscientious Objector). By contrast, gorillas and humans have relatively small testes but produce many defective sperms. So species that are not adapted to counter significant sperm competition, such as humans and gorillas, seemingly fail to eliminate abnormal sperms from their ejaculates. As with so much of reproduction, they leave that task to the females!

References

Afzelius, B.A. (1981) Abnormal human spermatozoa including comparative data from apes. American Journal of Primatology 1:175-182.

Baker, R.R. & Bellis, M.A. (1988) ‘Kamikaze’ sperm in mammals? Animal Behaviour 36:936-939.

Baker, R.R. & Bellis, M.A. (1989) Elaboration of the Kamikaze Sperm Hypothesis: a reply to Harcourt. Animal Behaviour 37:865-867.

Baker, R.R. & Bellis, M.A. (1995) Human Sperm Competition: Copulation, Masturbation and Infidelity. London: Chapman & Hall.

Bedford, J.M. (1974) Biology of primate spermatozoa. Contributions to Primatology 3:97-139.

Dixson, A.F. (2012) Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings (Second Edition). Oxford: Oxford University Press.

Harcourt, A.H. (1989) Deformed sperm are probably not adaptive. Animal Behaviour 37:863-865.

Harcourt, A.H. (1991) Sperm competition and the evolution of nonfertilizing sperm in mammals. Evolution 45:314-328.

Moore, H.D.M., Martin, M. & Birkhead, T.R. (1999) No evidence for killer sperm or other selective interactions between human spermatozoa in ejaculates of different males in vitro. Proceedings of the Royal Socety London B 266:2343-2350.

Seuánez, H.N., Carothers, A.C., Martin, D.E. & Short, R.V. (1977) Morphological abnormalities in the spermatozoa of the great apes and man. Nature  270:345-347.

Short, R.V. (1998) Review of Human Sperm Competition: Copulation, Masturbation, and Infidelity (1995) by Robin R. Baker & Mark A. Bellis (London & New York: Chapman & Hall). Newsletter of the European Sociobiological Society 47:20-23.

And here is a link to that fiery book review by Roger Short:

http://rint.rechten.rug.nl/rth/ess/ess47.htm

 

Robert Martin, Ph.D., is the A. Watson Armour III Curator of Biological Anthropology at the Field Museum in Chicago.

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