Sperm pleiomorphism

Antoni van Leeuwenhoek was the first person to observe human spermatozoa; he reported his observations in a letter to the Secretary of the Royal Society, Nehemiah Grew, in 1677. His drawings of spermatozoa, published in the Philosophical Transactions of the Royal Society (1679), show individual variations in the shape of the head, and other features (Farley 1982). These variations may reflect, in part, the limitations of Leeuwenhoek's microscope lenses, lenses which he ground himself and mounted in his pioneering instruments. Or, perhaps the individual differences which Leeuwenhoek saw (Figure 3.6) also related to genuine variations (pleiomorphisms) among these gametes. For human ejaculates commonly include a high percentage of abnormally shaped gametes, as is also the case among gorillas (Seuânez et al. 1977; Seuânez 1980) and cheetahs (O'Brien et al. 1985).

Baker and Bellis (1988, 1995) proposed that human sperm pleiomorphism results from selection for sperm morphs which fulfill different roles in relation to sperm competition. 'Kamikaze' sperm were posited to occupy strategic positions in the female

Figure 3.6 Leeuwenhoek's drawings of spermatozoa ('spermatic animalcules') as reported in the Philosophical Transactions of the Royal

Society (1679).

Source: From Farley (1982).

Figure 3.6 Leeuwenhoek's drawings of spermatozoa ('spermatic animalcules') as reported in the Philosophical Transactions of the Royal

Society (1679).

Source: From Farley (1982).

reproductive tract and to block access to gametes of rival males. In mammals which produce copulatory plugs (e.g. rats, bats) it was proposed that the presence of kamikaze sperm functioned to form a mesh-work and a focus for plug formation. By contrast, a smaller population of fertilizing or "egg-getter" sperm in human beings, and other mammals, was hypothesized to specialize in reaching the oviduct and effecting fertilization. In their book, Human Sperm Competition (1995), Baker and Bellis also proposed that oval-headed 'killer sperm' exist in the human ejaculate. When semen of two men were mixed, increased mortality and decreased motility were reported to occur. Baker and Bellis suggested that killer sperm released their acrosomal enzymes in order to attack the gametes of the second male in these mixed samples.

Although these startling claims achieved notoriety via the popular media, they have received little support scientifically. Moore, Martin, and Birkhead (1999) conducted careful quantitative studies of the effects of mixing ejaculates from different males and were unable to confirm Baker and Bellis's findings or to find any support for the existence of killer sperm in human beings. Much earlier, Harcourt (1989) had pointed out inconsistencies in Baker and Bellis's (1988) kamikaze sperm hypothesis, especially in relation to comparative data on mammalian gamete biology. Abnormal sperm, such as those which are trapped in the copulatory plugs of bats, may be so situated because they lack normal motility and not because they are specialized, kamikaze morphs. Harcourt also noted that, among the primates, the occurrence of pleiomorphic sperm, including abnormal sperm, is greatest among gorillas and human beings, and least in chimpanzees. This is surprising, because chimpanzees engage in frequent multiple matings and sperm competition. Thus, we should expect sperm pleiomorphism, and kamikaze morphs to be better developed in chimps than in gorillas or human beings. To make this point clearer, Figure 3.7 presents data on percentages of pleiomorphic sperm in the ejaculates of all the great ape species, as well as in human males. These data (from Seuanez 1980) make it clear that there is actually an inverse relationship between relative testes size, sperm competition pressures, and numbers of abnormal sperm in the ejaculates of men and the great apes. Indeed, it might be argued that it is the very absence of selection pressures relating to sperm competition which allows abnormal sperm to persist in the ejaculates of gorillas and human beings. The production of such abnormal sperm might relate to errors which occur during the meiotic cellular divisions of spermatogenesis, and especially to errors of chiasmata formation which underlie the 'crossing-over' of genes (Cohen 1967). Selection may fail to eliminate such errors if there are insufficient negative selection pressures. Hence they may persist in the gorilla and human male but not in chimpanzees or bonobos where sperm competition is of paramount importance. These observations lead to some additional considerations concerning the quality, as well as the numbers, of spermatozoa produced by human beings and other mammals.

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