Sperm competition and the evolution of sperm design in mammals

Background  

The influence of sperm competition upon sperm size has been a controversial issue during the last 20 years which remains unresolved for mammals. The hypothesis that, when ejaculates compete with rival males, an increase in sperm size would make sperm more competitive because it would increase sperm swimming speed, has generated contradictory results from both theoretical and empirical studies. In addition, the debate has extended to which sperm components should increase in size: the midpiece to accommodate more mitochondria and produce more energy to fuel motility, or the principal piece to generate greater propulsion forces.     

Sperm design and function in the redside dace Clinostomus elongatus

A study was undertaken to examine sperm morphometry in relation to sperm velocity and sperm longevity in the redside dace Clinostomus elongatus . There was significant between-male variance in sperm size and shape metrics (total sperm length, sperm head length, flagellum length and sperm head length to width ratio) and positive relationships were found between these morphometrics and sperm velocity. There were no significant relationships found between sperm morphometry and sperm longevity, nor was there a trade-off between sperm velocity and sperm longevity.     

Sperm viability and sperm competition in insects

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. In insects, however, the importance of sperm quality has never been considered, despite sperm competition being widespread and well studied in this group. We 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), we 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. Our results suggest that sperm viability is one of a suite of male adaptations to sperm competition in insects.     

Sperm competition, sperm numbers and sperm quality in muroid rodents

Sperm competition favors increases in relative testes mass and production efficiency, and changes in sperm phenotype that result in faster swimming speeds. However, little is known about its effects on traits that contribute to determine the quality of a whole ejaculate (i.e., proportion of motile, viable, morphologically normal and acrosome intact sperm) and that are key determinants of fertilization success. Two competing hypotheses lead to alternative predictions: (a) sperm quantity and quality traits co-evolve under sperm competition because they play complementary roles in determining ejaculate's competitive ability, or (b) energetic constraints force trade-offs between traits depending on their relevance in providing a competitive advantage. We examined relationships between sperm competition levels, sperm quantity, and traits that determine ejaculate quality, in a comparative study of 18 rodent species using phylogenetically controlled analyses. Total sperm numbers were positively correlated to proportions of normal sperm, acrosome integrity and motile sperm; the latter three were also significantly related among themselves, suggesting no trade-offs between traits. In addition, testes mass corrected for body mass (i.e., relative testes mass), showed a strong association with sperm numbers, and positive significant associations with all sperm traits that determine ejaculate quality with the exception of live sperm. An "overall sperm quality" parameter obtained by principal component analysis (which explained 85% of the variance) was more strongly associated with relative testes mass than any individual quality trait. Overall sperm quality was as strongly associated with relative testes mass as sperm numbers. Thus, sperm quality traits improve under sperm competition in an integrated manner suggesting that a combination of all traits is what makes ejaculates more competitive. In evolutionary terms this implies that a complex network of genetic and developmental pathways underlying processes of sperm formation, maturation, transport in the female reproductive tract, and preparation for fertilization must all evolve in concert.     

Sperm morphology and sperm velocity in passerine birds

Sperm velocity is one of the main determinants of the outcome of sperm competition. Since sperm vary considerably in their morphology between and within species, it seems likely that sperm morphology is associated with sperm velocity. Theory predicts that sperm velocity may be increased by enlarged midpiece (energetic component) or flagellum length (kinetic component), or by particular ratios between sperm components, such as between flagellum length and head size. However, such associations have rarely been found in empirical studies. In a comparative framework in passerine birds, we tested these theoretical predictions both across a wide range of species and within a single family, the New World blackbirds (Icteridae). In both study groups, sperm velocity was influenced by sperm morphology in the predicted direction. Consistent with theoretical models, these results show that selection on sperm morphology and velocity are likely to be concomitant evolutionary forces.     

Sperm size and sperm competition in birds.

In a sample of 20 species of North American passerine birds we found no relation between sperm size and mating system like that previously reported in mammals (Gomendio & Roldan (Proc. R. Soc. Lond. B 243, 181 (1991)). Instead, we found a positive correlation between sperm length and the length of female sperm storage tubules (SSTS) and a negative correlation between sperm length and the number of SSTS. Both of these correlations suggest that the more than fivefold variation in sperm size we found among species can be explained by sperm competition for access to storage sites (SSTS) in females. As longer sperm appear to be able to swim faster, selection should favour long sperm when SSTS are in short supply; sperm long enough to fill an SST might also prevent access to SSTS by the sperm of other males. Conversely, selection should favour shorter sperm when there is an advantage to sperm layering within an SST promoting a last-male mating advantage. Although we conclude that sperm competition influences sperm size in birds, little is known about the interactions between sperm and SSTS. It seems clear, however, that detailed study of this interaction will provide a new dimension to the study of avian mating systems.     

Sperm viability matters in insect sperm competition

Experimental studies in insects have shown how sperm competition can be a potent selective force acting on an array of male reproductive traits . However, the role of sperm quality in determining paternity in insects has been neglected, despite the fact that sperm quality has been shown to influence the outcome of sperm competition in vertebrates . A recent comparative analysis found that males of polyandrous insect species show a higher proportion of live sperm in their stores . Here, we test the hypothesis that sperm viability influences paternity at the within-species level. We use the cricket Teleogryllus oceanicus to conduct sperm competition trials involving prescreened males that differ in the viability of their sperm. We find that paternity success is determined by the proportion of live sperm in a male's ejaculate. Furthermore, we were able to predict the paternity patterns observed on the basis of the males' relative representation of viable sperm in the female's sperm-storage organ. Our findings provide the first experimental evidence for the theory that sperm competition selects for higher sperm quality in insects. Between-male variation in sperm quality needs to be considered in theoretical and experimental studies of insect sperm competition.     

Sperm morphology and evidence for sperm competition among parrots

Sperm competition is an important component of post‐copulatory sexual selection that has shaped the evolution of sperm morphology. Previous studies have reported that sperm competition has a concurrently directional and stabilizing effect on sperm size. For example, bird species that show higher levels of extrapair paternity and larger testes (proxies for the intensity of sperm competition) have longer sperm and lower coefficients of variation in sperm length, both within and between males. For this reason, these sperm traits have been proposed as indexes to estimate the level of sperm competition in species for which other measures are not available. The relationship between sperm competition and sperm morphology has been explored mostly for bird species that breed in temperate zones, with the main focus on passerine birds. We measured sperm morphology in 62 parrot species that breed mainly in the tropics and related variation in sperm length to life‐history traits potentially indicative of the level of sperm competition. We showed that sperm length negatively correlated with the within‐male coefficient of variation in sperm length and positively with testes mass. We also showed that sperm is longer in sexually dichromatic and in gregarious species. Our results support the general validity of the hypothesis that sperm competition drives variation in sperm morphology. Our analyses suggest that post‐copulatory sexual selection is also important in tropical species, with more intense sperm competition among sexually dichromatic species and among species that breed at higher densities.     

Sperm competition influences sperm size in mammals.

Among mammals sperm competition leads to selection for increased sperm numbers but it is not known whether it also leads to changes in sperm size. Two contrasting theoretical predictions have been made. The first hypothesis relies on the assumption that there is a trade-off between sperm numbers and sperm size and predicts that, in species confronting sperm competition, there will be a concomitant decrease in sperm size as sperm numbers increase. In contrast, the second hypothesis suggests that longer sperm may outcompete rival sperm; if longer sperm may swim faster, they will reach the ova sooner and will be selected when sperm competition prevails. We tested these hypotheses in both primates and rodents. We report that males from species in which females mate promiscuously have longer sperm than species in which females mate with one male. In addition, we also found that sperm length is positively correlated with maximum sperm velocity. Our findings thus support the view that longer sperm may be adaptive in the context of sperm competition.     

Sperm competition games: sperm selection by females

We analyse a co-evolutionary sexual conflict game, in which males compete for fertilizations (sperm competition) and females operate sperm selection against unfavourable ejaculates (cryptic female choice). For simplicity, each female mates with two males per reproductive event, and the competing ejaculates are of two types, favourable (having high viability or success) or unfavourable (where progeny are less successful). Over evolutionary time, females can increase their level of sperm selection (measured as the proportion of unfavourable sperm eliminated) by paying a fecundity cost. Males can regulate sperm allocations depending on whether they will be favoured or disfavoured, but increasing sperm allocation reduces their mating rate. The resolution of this game depends on whether males are equal, or unequal. Males could be equal: each is favoured with probability, p, reflecting the proportion of females in the population that favour his ejaculate (the 'random-roles' model); different males are favoured by different sets of females. Alternatively, males could be unequal: given males are perceived consistently by all females as two distinct types, favoured and disfavoured, where p is now the frequency of the favoured male type in the population (the 'constant-types' model). In both cases, the evolutionarily stable strategy (ESS) is for females initially to increase sperm selection from zero as the viability of offspring from unfavourable ejaculates falls below that of favourable ejaculates. But in the random-roles model, sperm selection decreases again towards zero as the unfavourable ejaculates become disastrous (i.e. as their progeny viability decreases towards zero). This occurs because males avoid expenditure in unfavourable matings, to conserve sperm for matings in the favoured role where their offspring have high viability, thus allowing females to relax sperm selection. If sperm selection is costly to females, ESS sperm selection is high across a region of intermediate viabilities. If it is uncostly, there is no ESS in this region unless sperm limitation (i.e. some eggs fail to be fertilized because sperm numbers are too low) is included into the model. In the constant-types model, no relaxation of sperm selection occurs at very low viabilities of disfavoured male progeny. If sperm selection is sufficiently costly, ESS sperm selection increases as progeny viability decreases down towards zero; but if it is uncostly, there is no ESS at the lowest viabilities, and unlike the random-roles model, this cannot be stabilized by including sperm limitation. Sperm allocations in the ESS regions differ between the two models. With random roles, males always allocate more sperm in the favoured role. With constant types, the male type that is favoured allocates less sperm than the disfavoured type. These results suggests that empiricists studying cryptic female choice and sperm allocation patterns need to determine whether sperm selection is applied differently, or consistently, on given males by different females in the same population.     

Sperm competition and sperm precedence in the dragonfly Nanophya pygmaea

Abstract. The libellulid dragonfly, Nanophya pygmaea Rambur, has an average ejaculate volume of 0.16 mm³. During successive copulations the volume of sperm stored in the female's sperm storage organs increases in steps equivalent to this volume, suggesting that the sperm competition mechanism in this species is sperm repositioning, i.e. adding an ejaculate to what is already present in the female's sperm storage organ. By using sterile/normal males in double matings with females we have shown that this mechanism results in last male sperm precedence (P²= 0.979).     

Sperm number trumps sperm size in mammalian ejaculate evolution

Postcopulatory sexual selection is widely accepted to underlie the extraordinary diversification of sperm morphology. However, why does it favour longer sperm in some taxa but shorter in others? Two recent hypotheses addressing this discrepancy offered contradictory explanations. Under the sperm dilution hypothesis, selection via sperm density in the female reproductive tract favours more but smaller sperm in large, but the reverse in small, species. Conversely, the metabolic constraint hypothesis maintains that ejaculates respond positively to selection in small endothermic animals with high metabolic rates, whereas low metabolic rates constrain their evolution in large species. Here, we resolve this debate by capitalizing on the substantial variation in mammalian body size and reproductive physiology. Evolutionary responses shifted from sperm length to number with increasing mammalian body size, thus supporting the sperm dilution hypothesis. Our findings demonstrate that body-size-mediated trade-offs between sperm size and number can explain the extreme diversification in sperm phenotypes.     

Sperm duct contractions mediate centrally evoked sperm release in goldfish

In order to determine the peripheral mechanisms underlying sperm release (SR) in goldfish, the contractile activity of the sperm ducts (SD) and testes were monitored during SR responses evoked by electrical stimulation of the brain. Electrical stimulation of the brain triggered testicular and SD contractions, and SR, while electrical stimulation of the genital nerve branch to the SD evoked only SD contractions and SR. Centrally activated SD contractions and SR were blocked by sectioning the SD genital nerve, while testicular contractions were unaffected. Testicular contractions do not appear necessary for centrally evoked SR since the response can be elicited from preparations in which the testes were separated from the SD. The results indicate that SR in goldfish is primarily mediated by the SD and not the testes. Testicular contractions may, however, serve to load the SD with milt. The functional significance of the central pathway(s) associated with SD and testicular contractions are discussed.     

Sperm midpiece length predicts sperm swimming velocity in house mice

Evolutionary biologists have argued that there should be a positive relationship between sperm size and sperm velocity, and that these traits influence a male''s sperm competitiveness. However, comparative analyses investigating the evolutionary associations between sperm competition risk and sperm morphology have reported inconsistent patterns of association, and in vitro sperm competition experiments have further confused the issue; in some species, males with longer sperm achieve more competitive fertilization, while in other species males with shorter sperm have greater sperm competitiveness. Few investigations have attempted to address this problem. Here, we investigated the relationship between sperm morphology and sperm velocity in house mice (Mus domesticus). We conducted in vitro sperm velocity assays on males from established selection lines, and found that sperm midpiece size was the only phenotypic predictor of sperm swimming velocity.