Role In Sperm Competition Research Articles

Evolution of sexual size monomorphism: the influence of passive mate guarding

Some species have potential for intense mate competition yet exhibit little or no sexual size dimorphism, despite predictions from sexual selection theory. Using a conceptual model, we show the conditions for which passive mate guarding with copulatory plugs can be an alternative and more successful strategy to active (direct) guarding, reducing selection pressure on large male size. The model predicts that copulatory plugs in mammals should be favoured in species for which females have short sexual receptivity periods. Using data on 62 primate species and a phylogenetic regression approach, we show that, as predicted, copulatory plugs are negatively associated with degree of sexual dimorphism and females' sexual receptivity length. Penile spines are also significantly associated with plug use and short receptivity periods suggesting a possible offensive role in sperm competition. Results highlight that life-history characteristics, such as sexual receptivity lengths, may alter the costs and benefits of alternative male strategies and thus alter the strength of sexual selection.

SPERM COMPETITION AND REPRODUCTIVE MODE INFLUENCE SPERM DIMENSIONS AND STRUCTURE AMONG SNAKES

The role of sperm competition in increasing sperm length is a controversial issue, because findings from different taxa seem contradictory. We present a comparative study of 25 species of snakes with different levels of sperm competition to test whether it influences the size and structure of different sperm components. We show that, as levels of sperm competition increase, so does sperm length, and that this elongation is largely explained by increases in midpiece length. In snakes, the midpiece is comparatively large and it contains structures, which in other taxa are present in the rest of the flagellum, suggesting that it may integrate some of its functions. Thus, increases in sperm midpiece size would result in more energy as well as greater propulsion force. Sperm competition also increases the area occupied by the fibrous sheath and outer dense fibers within the sperm midpiece, revealing for the first time an effect upon structural elements within the sperm. Finally, differences in male-male encounter rates between oviparous and viviparous species seem to lead to differences in levels of sperm competition. We conclude that the influence of sperm competition upon different sperm components varies between taxa, because their structure and function is different.

Gamete plasticity in a broadcast spawning marine invertebrate

Sperm competition has classically been thought to maintain anisogamy (large eggs and smaller sperm) because males are thought to maximize their chance of winning fertilizations by trading sperm size for number. More recently it has been recognized that sperm quality (e.g., size, velocity) can also influence sperm competition, although studies have yielded conflicting results. Because sex evolved in the sea, debate has continued over the role of sperm competition and sperm environment in determining both sperm and egg size in externally fertilizing broadcast spawners. Remarkably, however, there have been no direct tests of whether broadcast spawners change the traits of their gametes depending on the likelihood of sperm competition. We manipulated the density (and thus, sperm environment) of a broadcast spawning ascidian (Styela plicata) in the field and then determined whether the phenotype of eggs and sperm changed. We found that sperm from adults kept at high density were larger and more motile than sperm from low-density adults. In vitro fertilizations revealed that sperm from high-density adults also lived longer and induced less polyspermy. Adult density also affected egg traits: eggs from high-density adults were smaller targets for sperm overall but produced larger ovicells than eggs from low-density adults. This suggests that broadcast spawning mothers balance (potentially conflicting) pre- and postzygotic selection pressures on egg size. Overall, our results suggest that sperm competition does not represent a strong force maintaining anisogamy in broadcast spawners. Instead, sperm limitation seems to select for large eggs and smaller, more numerous sperm.

AN EVOLUTIONARY EXPRESSED SEQUENCE TAG ANALYSIS OF DROSOPHILA SPERMATHECA GENES

This study investigates genes enriched for expression in the spermatheca, the long-term sperm storage organ (SSO) of female Drosophila. SSO genes are likely to play an important role in processes of sexual selection such as sperm competition and cryptic female choice. Although there is keen interest in the mechanisms of sexual selection at the molecular level, very little is known about the female genes that are involved. In the present study, a high proportion of genes enriched for expression in the spermatheca are evolving rapidly. Most of the rapidly evolving genes are proteases and genes of unknown function that could play a specialized role in the spermatheca. A high percentage of the rapidly evolving genes have secretion signals and thus could encode proteins that directly interact with ejaculate proteins and coevolve with them. In addition to identifying rapidly evolving genes, the present study documents categories of genes that could play a role in spermatheca function such as storing, maintaining, and utilizing sperm. In general, candidate genes discovered in this study could play a key role in sperm competition, cryptic female choice of sperm, and sexually antagonistic coevolution, and ultimately speciation.

A comparison of nuclear and cytoplasmic genetic effects on sperm competitiveness and female remating in a seed beetle

It is widely assumed that male sperm competitiveness evolves adaptively. However, recent studies have found a cytoplasmic genetic component to phenotypic variation in some sperm traits presumed important in sperm competition. As cytoplasmic genes are maternally transmitted, they cannot respond to selection on sperm and this constraint may affect the scope in which sperm competitiveness can evolve adaptively. We examined nuclear and cytoplasmic genetic contributions to sperm competitiveness, using populations of Callosobruchus maculatus carrying orthogonal combinations of nuclear and cytoplasmic lineages. Our design also enabled us to examine genetic contributions to female remating. We found that sperm competitiveness and remating are primarily encoded by nuclear genes. In particular, a male's sperm competitiveness phenotype was contingent on an interaction between the competing male genotypes. Furthermore, cytoplasmic effects were detected on remating but not sperm competitiveness, suggesting that cytoplasmic genes do not generally play a profound evolutionary role in sperm competition.

Of mice and sperm

When females are sexually promiscuous, the ejaculates of different males may compete for the fertilization of a set of ova, a process known as sperm competition. In internally fertilizing species, potential for sperm competition occurs whenever the ejaculates of different males cooccur in the female reproductive tract at the time of ovulation. Sperm competition is now recognized as a powerful agent of evolutionary change, and the signal of its selective pressure is being detected on a number of male physiological and behavioral traits (1, 2). One of the major determinants of the outcome of sperm competition is the relative numerical representation of different ejaculates at the time of fertilization. All else being equal, the male that inseminates more sperm into a female has a fertilizing edge over his competitors (1, 3). The rate of spermatogenesis is determined by gonadal mass, and under more intense sperm competition we would expect males to grow relatively large testicles to inseminate more sperm. Evidence that sperm competition favors the evolution of larger testes relative to body mass (gonadosomatic index) comes from multiple comparative and experimental evolution studies across a number of taxa (1, 4–7). In addition to the number of sperm inseminated, the fertilizing efficiency of sperm also plays a critical role in sperm competition (8). Therefore, traits associated with the fertilizing performance of an ejaculate are also expected to evolve in response to sperm competition. The work by Gomendio et al. (9) in this issue of PNAS reveals that sperm competition may also have shaped the evolution of sperm function in eutherian mammals. Fertilization in eutherian mammals is a complicated business. After ejaculation, spermatozoa face two hierarchical challenges. First, sperm must undergo a process of maturation in the female uterus and oviduct. This process is known as capacitation … *E-mail: tommaso.pizzari{at}zoo.ox.ac.uk

Life history and sex allocation in the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema: the role of sperm competition

Sex allocation theory predicts that, in hermaphroditic organisms, individuals allocate a fixed amount of resources divided among male and female functions to reproduction and that the proportion devoted to each sex depends on the mating group size. As the mating group size increases, hermaphrodites are predicted to allocate proportionally more resources to the male and less resources to the female function (approaching equal allocation to both sexes) to face increased sperm competition. Up to now little experimental evidence has been provided to support the theory in hermaphroditic animals. Facultative shift between male and female allocation in response to variation in local group size does occur in several taxa but not always in the expected direction and not with similar patterns. In the protandric and then simultaneously hermaphroditic polychaete worm Ophryotrocha diadema reproductive resources are flexibly allocated in the protandrous and the hermaphroditic phase. The cost of male reproduction during adolescence is spread over the whole energy budget of the animal as shown by the shortening of lifespan and the lowering of growth rate in individuals with enhanced male expenditure during the protandrous phase. Moreover, in this species, short term sex allocation adjustments differ from those described in other taxa. Individuals regulate their reproductive output so that where reproductive competitors are present, the number of female gametes is strongly reduced but the number of male gametes (although it changes) is not significantly increased. Resources subtracted from the female function are not directly allocated to sperm production, but to expensive male behaviors that are likely to enhance male reproductive success. These results are discussed in the light of the relevance of sexual selection in large populations of hermaphrodites.

Dam and Sire Effects on Sperm Penetration of the Perivitelline Layer and Resulting Fecundity of Different Lines of Turkeys

All birds studied thus far are able to store spermatozoa within their oviducts for periods that can vary from several days to weeks, depending upon the species. Turkeys have a relatively long storage period compared with chickens, an observation that leads to the suggestion that sperm residing within the oviduct may interact with sperm entering the oviduct from later inseminations. Multiple sources of sperm within the oviduct also lead to the hypothesis that sperm competition may be important for the maintenance of fertility and embryo livability in turkeys. The current study tested the hypothesis that selection for economically important traits in lines of turkeys may have an effect on sperm competition as measured by the ability to hydrolyze holes in the perivitelline layer, fertilize, and produce viable offspring.Lines of turkeys selected for egg production or rapid growth were compared with their respective randombred control lines. Reciprocal crosses of dams and sires of the selected and control lines were made to determine inherent sire and dam roles in sperm competition. Selection for increased egg production increased hydrolysis of the perivitelline layer and improved fertility but decreased early embryo death while increasing embryo deaths at pipping compared with controls, and these effects were primarily determined by the dam. Selection for increased body weight has created an interaction between dams and sires for sperm hydrolysis of the inner perivitelline layer, fertility and embryo survival. Thus, we concluded that genetic selection for economically important traits may affect sperm hydrolysis of the perivitelline layer and the subsequent fertility, and embryo livability.

The darting game in snails and slugs

Love darts are hard 'needles' that many snails and slugs use to pierce their partner during mating. In a few species, darts have been shown to play a role in sperm competition. Two new papers, by Davison et al., and Koene and Schulenburg, might further pique researchers' interest, because they show how the full potential of darts can be tapped for studies of sexual selection in hermaphrodites.

Male Mounting Alone Reduces Female Promiscuity in the Fowl

The fertilization success of an insemination is at risk when a female has the possibility to copulate with multiple males, generating sperm competition and sexual conflict over remating. Female propensity to remate is often reduced after copulation, and a staggering diversity of highly derived male traits that discourage female promiscuity have been investigated. However, it is difficult to separate the effect of such specialized traits and insemination products from the more basic effect that the act of mounting per se may have on female remating. Here, we use a novel approach that separates the influence of mounting from that of insemination on female remating in the promiscuous feral fowl. Mounting alone caused a transient but drastic reduction in female propensity to remate, and-crucially-the number of sperm that a female obtained from a new male. Therefore, like other taxa, female fowl show a reduction in promiscuity after copulation, but this is entirely due to mounting alone. This effect of mounting, independent of insemination and fertilization, indicates that even copulations that deliver little or no semen, a puzzling behavior common in many species including the fowl, may play a crucial role in sperm competition.

Positive Selection for Indel Substitutions in the Rodent Sperm Protein Catsper1

Catsper1 is a voltage-gated calcium channel located in the plasma membrane of the sperm tail and is necessary for sperm motility and fertility in mice. We here examine the evolutionary pattern of Catsper1 from nine species of the rodent subfamily Murinae of family Muridae. We show that the rate of insertion/deletion (indel) substitutions in exon 1 of the gene is 4-15 times that in introns or neutral genomic regions, suggesting the presence of strong positive selection that promotes fixations of indel mutations in exon 1. The number of indel polymorphisms within species appears higher than expected from interspecific comparisons, although there are too little data to provide a statistically significant conclusion. These results, together with an earlier report in primates, indicate that positive selection promoting length variation in Catsper1 may be widespread in mammals. A structural model of Catsper1 suggested the importance of the exon 1-encoded region in regulating channel inactivation, which may affect sperm mobility and sperm competition. Our findings provide a necessary foundation for future experimental investigations of Catsper1's function in sperm physiology and role in sperm competition using rodent models.

223. The epididymis secretes proteins involved in sperm competition: evidence from the echidna

Although there is general recognition that the mammalian epididymis is unique among the vertebrates and is essential for male fertility, there is relatively little understanding of its role in the process of reproduction. It has been suggested that it plays an important role in the competition between males to achieve paternity (sperm competition) by accumulating and storing sperm.1 We now provide evidence that specific protein synthesized and secreted by the epididymis of the echidna plays a major role in sperm competition by binding spermatozoa into bundles of about a 100 sperm and consequently greatly enhancing their rate of motility, particularly in viscous medium. The epididymis of the echidna is structurally differentiated into a large caput epididymidis that is structurally similar to the ‘initial segment’ of other mammals, and a small cauda epididymidis. Using radiolabelling and 2-D electrophoresis we have shown that the caput epididymidis synthesises and secretes a similar pattern of proteins along most of its length where sperm are not associated with one another. The sperm form into bundles as they enter the cauda epididymidis where the pattern of protein secretion changes considerably, being characterised by a new band of about 80 kDa in reduced gels. Electron microscopy of the bundles shows electron dense material binding the sperm together in the bundles. The bundles persist for more than an hour after sperm are released into physiological media. (1)Jones, RC (1998). Evolution of the vertebrate epididymis. J. Reprod. Fertil. Suppl. 53, 163–182.

Sperm competition

Sperm competition

Sperm length influences fertilization success during sperm competition in the snail Viviparus ater.

Sperm form and size is tremendously variable within and across species. However, a general explanation for this variation is lacking. It has been suggested that sperm size may influence sperm competition, and there is evidence for this in some taxa but not others. In addition to normal fertilizing sperm, a number of molluscs and insects produce nonfertile sperm that are also extremely morphologically variable, and distinct from fertilizing forms. There is evidence that nonfertile sperm play an indirect role in sperm competition by decreasing female remating propensity in Lepidopterans, but in most taxa the function of parasperm is unknown. We investigated the role of nonfertile (oligopyrene) sperm during sperm competition in the fresh water snail Viviparus ater. Previous studies found that the proportion of oligopyrene sperm increased with the risk of sperm competition, and hence it seems likely that these sperm influence fertilization success during competitive matings. In mating experiments in which females were sequentially housed with males, we examined a range of male characteristics which potentially influence fertilization success. We found that the size of oligopyrene sperm was the best predictor of fertilization success, with males having the longer sperm siring the highest proportion of offspring. Furthermore, we found a positive shell size and sperm concentration effect on paternity, and females with multiply sired families produced more offspring than females mating with only one male. This result suggests polyandry is beneficial for female snails.

Understanding Reversals in the Relative Strength of Sexual Selection on Males and Females: A Role for Sperm Competition?

Sperm competition affects sexual selection intensity on males, but models suggest it cannot affect the relative intensity of sexual selection on males compared to females. However, if sperm competition depresses the payoff for male multiple mating, it could affect the relative intensity of sexual selection and even cause sexual selection to be more intense on females than males (reversal of typical pattern). To evaluate how sperm competition, energy availability, and parental investment affect the intensity of sexual selection on each sex, I constructed a simulation model using the relationship between fecundity and number of mates to estimate sexual selection gradients. Unlike earlier models, I include a trade-off between paternal investment and sperm competition ability. The amount of energy available for reproduction affects the sexual selection gradient for each sex. Reversals in the sex experiencing stronger sexual selection do occur when additional paternal investment reduces a male's ability to compete for fertilizations within females. The shape of the distribution of mates for each sex (determined by mate competition) is also important. Output from the model is qualitatively similar to empirical data from insects with paternal investment. This model challenges previous thinking about the role of sperm competition in sex-role reversal.

Sperm Quality as Reflected Through Morphology in Salmon Alternative Life Histories1

Male salmon exhibit alternative mating strategies, as both older anadromous adults and precocious juveniles (parr) participate in the spawning of a single female. This study tested the following hypotheses: 1) different intensities of sperm competition may reflect different sperm tail optima; 2) long spermatozoa are superior to short ones, with an associated cost on sperm longevity; and 3) a disfavored role in sperm competition selects for parr investing more in sperm quality. Comparisons included sperm morphological traits, whereas sperm quality was investigated by motility duration observations, measurement of the sperm adenylate system, and fertilization experiments. No evidence of different adaptive sperm dimensions between the male types was found. Positive association between spermatocrit and energy charge was, however, detected. Sperm length parameters correlated positively with ATP, energy charge, and fertilization success, whereas no evidence for an effect of sperm morphology on longevity was found. Male parr had greater spermatocrit than adults and fertilized equal proportions of eggs as adults despite a pronounced numerical subordinance in the fertilization experiments. It is concluded that a long sperm tail and midpiece may be selected to optimize energetic demands under conditions of increased sperm competition intensity.

Determinants of sperm precedence in a noctuid mothHeliothis virescens: a role for male age

Summary1. Females of the noctuid mothHeliothis virescensF. mate more than once. Thus, sperm from two or more males normally compete for fertilisations within the female reproductive tract. The eggs are typically fertilised by sperm from only one male, either the female's last mate or an earlier mate. Twice‐mated females store only one ejaculate's worth of fertilising sperm (eupyrene) but nearly two ejaculates' worth of a nonfertilising sperm morph (apyrene), which is thought to play a role in sperm competition.2. The mechanism of sperm use inH. virescenswas investigated by examining factors that vary with paternity, which was assigned based on allozyme variation. The factors included male and female body masses and ages, male genital characters, the size of the sperm package, and the number of sperm stored by the female.3. One male typically gained sperm precedence; this was nearly twice as likely to be the second male as it was to be the first. Two factors were found to vary significantly with paternity: female mass and male age. The second male to mate was more likely to gain sperm precedence if the female was larger and if the male was older than the female's first mate.4. The significance of male age and female mass to several hypothetical models of the mechanism of sperm use is discussed.

Sperm storage by females of the polyandrous noctuid moth Heliothis virescens

Female tobacco budworm moths, Heliothis virescens, generally mate with more than one male, receiving from each mate both fertilizing sperm (eupyrene) and nonfertilizing anucleate sperm (apyrene), which is thought to play a role in sperm competition. One male typically gains sperm precedence, but it is not consistently the last or the first male to mate. I investigated the mechanism of this variable pattern of paternity by examining the patterns of storage of both types of sperm in the female's spermatheca as a function of multiple mating and male phenotype. The number of stored apyrene sperm varied with mating history, being greatest in twice-mated females and least in females mated to one nonvirgin male. In contrast, only one ejaculate's worth of eupyrene sperm was stored regardless of female mating history (once or twice mated). Thus, while they store two complements of apyrene sperm, twice-mated females apparently store only one ejaculate's worth of eupyrene sperm. This biased pattern of sperm storage may contribute to the variable pattern of paternity observed in this species. Eupyrene sperm storage also correlated positively with female size, male age and spermatophore size. Finally, a new sperm storage site was identified and described. It is a bulged region in the seminal duct.

Snail sperm production characteristics vary with sperm competition risk

Sperm competition is widespread and influences both male investment in spermatogenic tissue and ejaculate characteristics. Sperm competition models assume trade-offs between sperm size and number, although such trade-offs may be difficult to detect. This study examines the effects of sperm competition risk on the sperm production characteristics of the freshwater snail Viviparus ater. In this prosobranch, females mate frequently and store sperm, generating sperm competition. Males produce two sperm morphs, fertile eupyrene sperm and non-fertilizing oligopyrene sperm. Non-fertilizing sperm may play a role in sperm competition and therefore, like fertilizing sperm, the number produced could vary relative to sperm competition risk. In addition, trade-offs between sperm number and sperm size may be expected. We manipulated the sex ratio of sexually mature snails and found the presence of rivals affected the ratio of oligopyrene/eupyrene sperm males produced. In experimental and natural populations, the number of oligopyrene sperm produced, but not the number of eupyrene sperm, was significantly higher when the sex ratio was male biased. Testis mass did not vary between experimental treatments. We also found a negative relationship between the number and size of oligopyrene sperm produced, which is consistent with evolutionary models of sperm competition, and is, to our knowledge, the first intraspecific demonstration of a trade-off between these traits.

THE EVOLUTION OF SPERM SIZE IN BIRDS.

Sperm size varies enormously among species, but the reasons for this variation remain obscure. Since it has been suggested that swimming velocity increases with sperm length, earlier studies proposed longer (and therefore faster) sperm are advantageous under conditions of intense sperm competition. Nonetheless, previous work has been equivocal, perhaps because the intensity of sperm competition was measured indirectly. DNA profiling now provides a more direct measure of the number of offspring sired by extrapair males, and thus a more direct method of assessing the potential for sperm competition. Using a sample of 21 species of passerine birds for which DNA profiling data were available, we found a positive relation between sperm length and the degree of extrapair paternity. A path analysis, however, revealed that this relationship arises only indirectly through the positive relationship between the rate of extrapair paternity and length of sperm storage tubules (SSTs) in the female. As sperm length is correlated positively with SST length, an increase in the intensity of sperm competition leads to an increase in sperm length only through its effect on SST length. Why females vary SST length with the intensity of sperm competition is not clear, but one possibility is that it increases female control over how sperm are used in fertilization. Males, in turn, may respond on an evolutionary time scale to changes in SST size by increasing sperm length to prevent displacement from rival sperm. Previous theoretical analyses predicting that sperm size should decrease as sperm competition becomes more intense were not supported by our findings. We suggest that future models of sperm-size evolution consider not only the role of sperm competition, but also how female control and manipulation of ejaculates after insemination selects for different sperm morphologies.