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Sperm Competition Enhances Functional Capacity of Mammalian Sperm competition enhances functional capacity SEE COMMENTARY of mammalian spermatozoa Montserrat Gomendio, Juan Martin-Coello, Cristina Crespo, Concepcio´ n Magan˜ a, and Eduardo R. S. Roldan* Reproductive Ecology and Biology Group, Department of Evolutionary Ecology, Museo Nacional de Ciencias Naturales (CSIC), Jose´Gutierrez Abascal 2, 28006 Madrid, Spain Edited by Ryuzo Yanagimachi, University of Hawaii, Honolulu, HI, and approved August 15, 2006 (received for review July 12, 2006) When females mate promiscuously, sperm from rival males com- Atlantic salmon (Salmo salar), sperm velocity is the key deter- pete within the female reproductive tract to fertilize ova. Sperm minant of sperm competition success (14). competition is a powerful selective force that has shaped sexual Among mammals, evidence of longer spermatozoa in polyan- behavior, sperm production, and sperm morphology. However, drous species suggests that improved sperm swimming velocity nothing is known about the influence of sperm competition on under sperm competition could be achieved by an increase in fertilization-related processes, because it has been assumed that sperm size (15). Sperm competition can also select for unique sperm competition only involves a race to reach the site of morphological traits that improve swimming velocity, as is the fertilization. We compared four closely related rodent species with case in the male common wood mouse (Apodemus sylvaticus), different levels of sperm competition to examine whether there which has spermatozoa with extremely long apical hooks by are differences in the proportion of spermatozoa that become which they intertwine, forming ‘‘trains’’ of spermatozoa (16). ready to interact with the ovum (‘‘capacitated’’) and in the pro- These sperm associations swim nearly twice as fast as nonasso- portion of spermatozoa that experience the acrosome reaction in ciated sperm toward the site of fertilization. Evidence of an response to a natural stimulant. Our results show that differences association between sperm competition and increased sperm between species in levels of sperm competition were associated size comes from diverse taxa [birds (4), butterflies (17), fish (18), with the proportion of spermatozoa that undergo capacitation and and frogs (19)], although other studies have found no relation- with the proportion of spermatozoa that respond to progesterone, ship (20) or an inverse relationship [fish (6)]. The finding that EVOLUTION an ovum-associated signal. Sperm competition thus favors a larger there is coevolution between the size of spermatozoa and the size population of spermatozoa that are competent to fertilize, and of the female sperm storage organs (21) suggests that some spermatozoa that are more sensitive to the signals emitted by the inconsistencies may be due to the need to consider both male and ovum and that may penetrate the ova vestments more rapidly. female traits simultaneously. In groups with ameboid sperm, These results suggest that, contrary to previous assumptions, sperm competition does favor larger sperm (22, 23), which crawl competition between spermatozoa from rival males continues at faster and displace smaller sperm from the spermathecae (24). the site of fertilization. These findings may have further evolu- Experimental evidence shows that increased sperm competition tionary implications because the enhanced competitiveness of leads to an increase in sperm size (25). spermatozoa during fertilization may increase the risk of Sperm competition may also improve other aspects of ejacu- polyspermy to females. This could lead to antagonistic coevolution late quality, such as an increase in the proportion of viable between the sexes and may contribute to the explanation of the spermatozoa in the ejaculate (26). Experiments involving sperm rapid divergence observed in fertilization-related traits. competition trials have shown that, among insects, paternity success is determined by the proportion of live spermatozoa in sperm function ͉ capacitation ͉ acrosome reaction fertilization ͉ a male’s ejaculate (27). antagonistic coevolution Although there is ample evidence of the effects of sperm competition on sperm numbers and quality, the possibility that sperm competition has also influenced processes that take place ostcopulatory sexual selection occurs when females mate around the time of fertilization has not been explored. Yet the Pwith more than one male, creating the potential for compe- race to fertilize the available ova does not only imply greater tition between rival ejaculates to fertilize the available ova (1) motility to reach the site of fertilization first. Mammalian and for cryptic female choice (2). Among internal fertilizers, the spermatozoa need to undergo a process known as ‘‘capacitation’’ features of the female reproductive tract set the rules of the to be able to fertilize the ova (28–30). Capacitation can take up competition and thus determine which ejaculate features will to several hours, and indirect experimental evidence suggests improve their competitiveness. that when spermatozoa are placed in direct competition, those Comparative studies between species have shown that sperm that capacitate faster are more successful at fertilizing the ova competition has favored an increase in testes size and enhanced (31). In addition, spermatozoa must experience the ‘‘acrosome sperm production in taxa as diverse as mammals (reviewed in ref. reaction’’ to release the enzymes needed to penetrate the ova 3), birds (4), butterflies (5), fishes (6), and amphibians (7). vestments and to be able to fuse with the ovum’s plasma Microevolutionary manipulations have induced changes in testes size and sperm production by modifying the intensity of sperm competition (8–10), providing strong support for a causal rela- Author contributions: M.G. and E.R.S.R. designed research; J.M.-C., C.C., C.M., and E.R.S.R. tionship. There is ample evidence that in competitive contexts performed research; E.R.S.R. contributed new reagents͞analytic tools; M.G., J.M.-C., and males with greater sperm numbers father more offspring (see E.R.S.R. analyzed data; and M.G. and E.R.S.R. wrote the paper. reviews in ref. 11). The authors declare no conflict of interest. The competitiveness of an ejaculate is also largely determined This paper was submitted directly (Track II) to the PNAS office. by sperm motility and sperm swimming velocity. In birds, males Freely available online through the PNAS open access option. with high sperm ‘‘mobility’’ (as measured by an in vitro motility Abbreviations: CTC, chlortetracycline; ZP, zona pellucida. assay) fathered the majority of offspring in sperm competition See Commentary on page 14983. experiments (12), because sperm mobility determines the rate at *To whom correspondence should be addressed. E-mail: [email protected]. which sperm are released from female storage sites (13). In the © 2006 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0605795103 PNAS ͉ October 10, 2006 ͉ vol. 103 ͉ no. 41 ͉ 15113–15117 Downloaded by guest on October 2, 2021 Table 1. Relative testes weight and relative number of spermatozoa in four species of murid rodents Relative no. of Relative testes spermatozoa Species* weight† (ϫ106)‡ M. pahari 0.004 Ϯ 0.000 2.825 Ϯ 0.01 M. musculus 0.006 Ϯ 0.000 10.954 Ϯ 1.20 M. spretus 0.017 Ϯ 0.000 23.887 Ϯ 4.21 M. spicilegus 0.030 Ϯ 0.000 32.666 Ϯ 3.45 *For each species, five males were examined. †Relative testes weight ϭ testes weight͞body weight. ‡Relative no. of spermatozoa ϭ total number of spermatozoa in epididymides and vasa deferentia͞body weight1/3. ate, and low levels of sperm competition to compare sperm function and the degree of sensitivity in response to signals released by the ovum. Fig. 1. Relation between body weight and testes weight in murid rodents For the four species examined, we have calculated differ- (r2 ϭ 0.4587, n ϭ 31, P Ͻ 0.0001). Filled circles: Apodemus agrarius, Apodemus ences in relative testes weight and in the relative number of flavicollis, Apodemus microps, A. sylvaticus, Micromys minutus, Mus bactria- spermatozoa produced (Table 1). Of the four species exam- nus, Mus castaneus, Mus cookii, Mus domesticus, Mus macedonicus, Notomys ined, Mus spicilegus was found to have the highest relative alexis, Notomys cervinus, Notomys fuscus, Notomys mitchelli, Praomys nata- testes weight, followed by M. spretus, M. musculus, and, finally, lensis, Pseudomys apodemoides, Pseudomys australis, Pseudomys delicatulus, M. pahari with the lowest values, being the differences in Pseudomys desertor, Pseudomys gracilicaudatus, Pseudomys hermannsbur- relative testes weight between these species statistically sig- gensis, Pseudomys nanus, Pseudomys novaehollandiae, Pseudomys short- nificant (ANOVA, F3,12 ϭ 1987.77, P Ͻ 0.0001; all post hoc ridgei, Rattus exulans, Rattus norvegicus, and Rattus rattus. Data are from Ͻ Kenagy and Trombulak (35), except for those of Mus species, which are our comparisons between pairs of species, P 0.0001) (Fig. 2a). own. Open circles: M. musculus, M. pahari, M. spicilegus, and M. spretus. The differences in relative testes weight were clearly associated with differences between species in the rate of sperm produc- tion, so that it was more than 10 times greater in M. spicilegus membrane (28, 32). The acrosome reaction must be carefully than in M. pahari, the two species with extreme values for synchronized with the ovum, because sperm that undergo the both traits. Differences between
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