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ScienceWeek
REPRODUCTIVE BIOLOGY: ON MALE PREGNANCY
The following points are made by A.G. Jones and J.C. Avise (Current Biology 2003 13:R791):
1) Male pregnancy is an alien concept in mammals. Yet this phenomenon is the universal reproductive mode of pipefishes, seahorses and sea dragons (family Syngnathidae, with more than 200 species). During mating, a female uses an ovipositor to transfer dozens or hundreds of her unfertilized eggs to the underside of a male, where he fertilizes them. The male then carries his developing offspring for several weeks until they are born as tiny, independent young. The enclosed brood sacs of most syngnathid species are reminiscent of female kangaroo pouches, except that these fish pouches are male contraptions.
2) During a mammalian pregnancy, the placenta allows the mother to nourish her progeny in the womb and remove their waste products. If male pipefishes and seahorses merely provided a bag for fish eggs to develop and hatch, it might not fully qualify as bona-fide pregnancy. However, current research suggests that in syngnathid species with well developed brood pouches, males do provide nutrients, osmoregulation, and oxygenation to the embryos they carry.
3) One favorable feature of male pregnancy for the father is his complete confidence of paternity: a pregnant male can rest assured that he is the true biological sire of offspring in his pouch. This contrasts with the situation in many fish species where males care for offspring (typically in nests) following external fertilization of eggs. In such situations, the resident or "bourgeois" male sometimes gets cuckolded when a sneaker male darts into his nest and releases sperm during a spawning event, thereby "stealing" some fertilizations and making the bourgeois male a foster parent to some of the newborns he raises. Male pregnancy offers a solid defense against this cuckolding strategy by sneaker males.
4) Although it is true that male pregnancy relieves a female from the burden of caring for her offspring, she still must provide the nutrients that are packaged in eggs. Thus, female pipefish invest more in offspring than deadbeat fathers in female-pregnant species. However, female pipefish usually leave their mates after mating, perhaps never to see them again. In monogamous seahorses, by contrast, a female remains "married" to her mate and checks on him frequently. By so doing, she can be prepared with a new batch of eggs as soon as her husband gives birth.(1-4)
References (abridged):
1. Jones, A.G. and Avise, J.C. (2001). Mating systems and sexual selection in male-pregnant pipefishes and seahorses: insights from microsatellite-based studies of maternity. J. Hered. 92, 150-158
2. Jones, A.G., Moore, G.I., Kvarnemo, C., Walker, D., and Avise, J.C. (2003). Sympatric speciation as a consequence of male pregnancy in seahorses. Proc. Natl. Acad. Sci. USA 100, 6598-6603
3. Lourie, S.A., Vincent, A.C.J., Hall, H.J., (1999). Seahorses: An Identification Guide to the World's Species and Their Conservation. Project Seahorse
4. Vincent, A.C.J., Ahnesjö, I., Berglund, A., and Rosenqvist, G. (1992). Pipefishes and seahorses: are they all sex role reversed?. Trends Ecol. Evol. 7, 237-241
Current Biology http://www.current-biology.com
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ON SPERM COOPERATION IN THE WOOD MOUSE
The following points are made by R.V. Short (Nature 2002 418:137):
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 http://www.nature.com/nature
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EXCEPTIONAL SPERM COOPERATION IN THE WOOD MOUSE
In this context, the term "Hamilton's rule" refers to a rule put forth by WD Hamilton (1964) that in general states that a social act is favored by natural selection if it increases the inclusive fitness of the performer. Hamilton's theory is often referred to as "kin selection".
The wood mouse, A. sylvaticus, is a murid rodent common throughout Western Europe, with a breeding season from February to October.
The following points are made by H. Moore et al (Nature 2002 418:174):
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 http://www.nature.com/nature
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SPERM VIABILITY AND SPERM COMPETITION IN INSECTS
The following points are made by FM Hunter and TR Birkhead (Current Biology 2002 12:121):
1) Sperm quality plays an important role in vertebrates in determining which male has the advantage when two or more males compete to fertilize a female's ova [1,2]. In insects, however, the importance of sperm quality has never been considered, despite sperm competition being widespread and well studied in this group [3,4].
2) The authors report they tested the hypothesis that sperm viability, measured as the proportion of live sperm, covaried with the intensity of sperm competition in insects. In a pairwise comparison of seven closely related species pairs, each comprising a monandrous and a polyandrous species (i.e., with and without sperm competition, respectively), the authors found that in all cases the polyandrous species had a higher proportion of live sperm in their sperm stores. The distribution of the percentage of live sperm showed considerable inter- and intraspecific variation, suggesting that, all else being equal, males will vary in their ability to fertilize ova on the basis of sperm viability alone. The authors suggest their results indicate that sperm viability is one of a suite of male adaptations to sperm competition in insects.
3) The authors suggest their results also indicate that considerable intraspecific variation exists in the proportion of dead sperm. To evaluate this properly, one should establish whether individual males show consistent differences in ejaculate viability. Such information is potentially available for a number of vertebrates where it is possible to obtain replicate semen samples from males, and it is already well established that consistent differences in fertilizing capacity exist among males. The consistency of sperm viability in individual male insects remains to be tested.[5]
References (abridged):
1. Dziuk P.J. (1996) Factors that influence the proportion of offspring sired by a male following heterospermic insemination. Anim. Reprod. Sci., 43:65-88
2. Birkhead T.R., Martinez J.G., Burke T. and Froman D.P. (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc. R Soc. Lond. B Biol. Sci., 266:1759-1764
3. Parker G.A. (1970) Sperm competition and its evolutionary consequences in the insects. Biol. Rev., 45:525-567
4. Simmons L.W. and Siva-Jothy M.T. (1998) Sperm competition in insects: mechanisms and the potential for selection. In: Birkhead T.R. and M›ller A.P. (Eds.) Sperm Competition and Sexual Selection. London: Academic Press
5. Wishart G.J. and Palmer F.H. (1986) Correlation of the fertilizing ability of semen from individual male fowls with sperm motility and ATP content. Br. Poult. Sci., 27:97-102
Current Biology http://www.current-biology.com
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