Non-Primate Mammal Sperm Competition
KeywordsSperm Competition Sperm Quality Sperm Length Wild Ruminant Ruminant Species
Post-copulatory scenario in which the sperm of males of polygamous species competes within the female genital tract to fertilize the oocyte.
In many non-primate mammalian species, females may mate with more than one male. According to the sperm competition theory, the reproductive success of the males of such species depends on both the magnitude of inter-male rivalry and covert sperm competition. When the ejaculates of two or more males must compete to fertilize a set of ova, the quality of the sperm they carry becomes of great importance. The transfer of large numbers of spermatozoa in competitive situations is an effective strategy; males that transfer more sperm per ejaculate, or who copulate more often, are more likely to sire offspring. Usually, males of polygamous species have large testes and produce ejaculates with many sperm cells. Sperm competition also acts as a selective force driving evolutionary change in sperm morphology and function. The degree of sperm pleiomorphy shown by a species varies according to the degree of sperm competition its behavior entails.
Sperm Competition in Polyandrous Species
The sperm of some individuals appears to enjoy advantages over that of their rivals. This is particularly important in polygamous species that practice polyandry, including rodents and many ruminants. Females can benefit from polyandry since males successful in both pre-copulatory (e.g., intra-sexual fighting) and post-copulatory (sperm competition) sexual section are more likely to sire high-quality offspring.
In many species in which female preference is important in mate selection, males with large and conspicuous sexual selection traits are commonly favored; indeed, male ornaments, to which female attention is paid, play a significant role as part of pre-copulatory strategies. In polygynous species, mate selection focuses mainly on the role played by weaponized male secondary sexual characteristics. Antlers and horns are employed in the precoital strategies of several ruminant species, the males using them to establish their dominance. A relationship between horn development and seasonal changes in breeding activity is clearly evident, with wild ruminants attaining maximum horn development just before the onset of the breeding season. However, this weaponry also appears to be a sensitive indicator of genetic stress and a means of providing signals of male vigor to females. The role of symmetry, a characteristic of genetic vigor, in the attraction of females is well established in many species. Thus, dominant males with larger and more symmetrical horns are likely to be selected for reproduction via their improved access to receptive females, but also via the latter’s preference for them.
In some species in which females mate with more than one male, the sperm competition theory indicates that male reproductive success depends upon the magnitude of inter-male rivalry and covert sperm competition (Preston et al. 2003). Reproductive success is thus a function of both pre- and post-copulatory strategies. Certainly, larger weaponry is often associated with better sperm quality in polygynous ruminants. Horn and antler size in wild ruminants such as ibexes and red deer is associated with testis size and sperm velocity, and in ibexes, males with the largest and best-developed ornamentation produce semen with a larger proportion of motile spermatozoa and a smaller number of sperms showing primary morphological abnormalities (Santiago-Moreno et al. 2009). This provides some evidence to support the phenotype-linked fertility insurance hypothesis. It may even be that wild bovid and cervid females use horn/antler quality as an index of male genetic and sperm quality. However, when the ejaculates of two or more males compete to fertilize a set of ova, the quality of the sperm they carry becomes of great importance. The transfer of large numbers of sperm is guaranteed by ejaculates with high sperm concentrations, and males of polygamous species usually have large testes and produce ejaculates with high sperm concentrations (e.g., the testis size/body size ratio is higher in promiscuous dogs [Canis lupus familiaris] than in monogamous wolves [Canis lupus] [Asa et al. 2016]). Successful competition between rivals at the site of fertilization then depends on the number of spermatozoa that enter the oviductal isthmus (sperm reservoir), the proportion of spermatozoa that undergo capacitation and the proportion that respond to ovum-associated signals.
In mammals, sperm length has been positively correlated with maximum sperm velocity. Although larger sperm heads might be thought a handicap to rapid swimming, several reports show that sperms with longer heads may swim faster (Gomendio and Roldan 1991; Malo et al. 2005). In scenarios of sperm competition, this may afford them a competitive advantage, as may the ability of sperm to maintain high concentrations of intracellular ATP (Tourmente et al. 2015). Indeed, differences in the intensity of sperm competition appear to influence the sperm morphometric variables of wild polygamous ruminant species. For example, in mouflon (Ovis musimon), a species with intense polyandry, rams produce sperm with larger heads (and in greater numbers) than other Mediterranean mountain ungulates such as the ibex (Capra pyrenaica), aoudad (Ammotragus lervia), or chamois (Rupicapra pyrenaica). Chamois sperm, which has the smallest head dimensions and is produced in more modest concentrations, may indicate the species to be less polyandrous (Pradiee et al. 2016).
Sperm competition also acts as a selective force driving evolutionary change in sperm morphology. The degree of sperm pleiomorphy shown by a species varies according to the degree of sperm competition its behavior entails. Although this is more evident in birds, monogamous mammals (e.g., species of Felidae except for the lion) usually have a higher rate of sperm morphological abnormalities than do very polygamous species, such as many ruminant species.
Sperm variables in polygynous ruminant species in which polyandry plays an important role are related to horn/antler characteristics, revealing a likely strong genetic influence. The social environment may, however, also affect these variables. The social status of an animal varies over its lifetime, even though it might possess high-quality weaponry. The social environment affects physiological variables, such as plasma testosterone and cortisol concentrations, that in turn influence spermatogenesis and sperm maturation and subsequently sperm quality. An impact on seminal plasma composition, e.g., on the seminal fluid proteome composition, might also be expected. Indeed, in some rodents the plasticity of different ejaculate components may be strongly influenced by social environment (Ramm et al. 2015).
Reproductive success in polyandrous species is a function of both pre- and post-copulatory strategies. With respect to the latter, sperm competition plays an important role and is dependent on sperm concentration, sperm velocity variables, and the proportion of sperm produced with morphological abnormalities.
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