Outcome Of Sperm Competition Research Articles

Influence of female reproductive anatomy on the outcome of sperm competition in Drosophila melanogaster.

Females as well as males can influence the outcome of sperm competition, and may do so through the anatomy of their reproductive tracts. Female Drosophila melanogaster store sperm in two morphologically distinct organs: a single seminal receptacle and, normally, two spermathecae. These organs have different temporal roles in sperm storage. To examine the association between sperm storage organ morphology and sperm competition, we used a mutant type of female with three spermathecae. Although the common measure of sperm competition, P(2), did not differ between females with two and three spermathecae, the pattern of sperm use over time indicated that female morphology did affect male reproductive success. The rate of offspring production by females with three spermathecae rose and fell more rapidly than by females with two spermathecae. If females remate or die before using up second male sperm, then second male reproductive success will be higher when they mate with females with three spermathecae. The results indicate that temporal patterns of sperm use as well as P(2) should be taken into account when measuring the outcome of sperm competition.

Female age and sperm competition: last-male precedence declines as female age increases

Until very recently, most studies of sperm competition have focused on variation in male competitive ability. However, we now know that a number of reproductive traits, including oviposition rate, use of stored sperm and receptivity to mating, vary with female condition. Because females can play an active part in the movement of sperm within their reproductive tract, sperm competition may be influenced by female condition. Existing studies of sperm competition in fruitflies ignore the effects of female condition, using females that are 3-4 days old and in their reproductive prime. But condition will decline as a female senesces. Here, we examine the effect of female age on the outcome of sperm competition in three strains of the fruitfly, Drosophila melanogaster. Previous studies have shown that female age influences preference for mates and male ejaculation strategies. In this study, we find that when males are mated to females that are older than 17 days, last-male sperm precedence decreases significantly. These results could lead to a greater understanding of the physiological mechanisms that regulate the outcome of sperm competition.

Badge size, paternity assurance behaviours and paternity losses in male house sparrows

Male quality may influence both the outcome of sperm competition and female faithfulness. In male house sparrows Passer domesticus, the size of the black throat patch (badge) signals dominance and perhaps attractiveness. So far, however, no study has reported any significant relationships between badge size, paternity and paternity assurance behaviours in this species. We found that the time mates spent together at the nest was positively correlated with badge size. Furthermore, although paternity losses were influenced by both the time spent at the nest and within‐pair copulation frequency, we found no relationship between copulation rate and badge size. It seems therefore that copulation frequency served as a paternity assurance behaviour, whereas the time mates stayed together at the nest may have reflected male attractiveness. Alternatively, females may have decided to stay with large‐badged males because they were better able to protect them from harassment by strange males. We also found that paternity losses were related to male badge size; average‐badged males cuckolded were more often than males with smaller or larger badges. We suggest that average‐badged males suffered higher paternity losses because they had different time allocation strategies than other males.

Sperm competitive ability and genetic relatedness in Drosophila melanogaster: similarity breeds contempt.

Offspring of close relatives often suffer severe fitness consequences. Previous studies have demonstrated that females, when given a choice, will choose to avoid mating with closely related males. But where opportunities for mate choice are limited or kin recognition is absent, precopulatory mechanisms may not work. In this case, either sex could reduce the risks of inbreeding through mechanisms that occur during or after copulation. During mating, males or females could commit fewer gametes when mating with a close relative. After mating, females could offset the effects of mating with a closely related male through cryptic choice. Few prior studies of sperm competition have examined the effect of genetic similarity, however, and what studies do exist have yielded equivocal results. In an effort to resolve this issue, we measured the outcome of sperm competition when female Drosophila melanogaster were mated to males of four different degrees of genetic relatedness and then to a standardized competitor. We provide the strongest evidence to date that sperm competitive ability is negatively correlated with relatedness, even after controlling for inbreeding depression.

Ovarian fluid enhances sperm movement in Arctic charr

Like the spermatozoa of most other fish species spawning in fresh water, Arctic charr Sahelinus alpinus sperm were short-lived (mean 42 s) after activation and their swimming speed declined rapidly during this period, e.g. from a mean speed of 106 um s−1 at 10 s after activation in fresh water to 21 μm s−1 only 20 s later. Ovarian fluid significantly influenced sperm longevity (duration of forward mobility), per cent motility, swimming speed and the linearity of sperm movement. All of these variables generally increased as the concentration of ovarian fluid increased from 0 to 50%, even though ovarian fluid is more than three times as viscous as fresh water. It is concluded that ovarian fluid enhances sperm movement in this species and thus has the potential to influence both fertilization success and the outcome of sperm competition.

Ovarian fluid enhances sperm movement in Arctic charr

Like the spermatozoa of most other fish species spawning in fresh water, Arctic charr Sahelinus alpinus sperm were short‐lived (mean 42 s) after activation and their swimming speed declined rapidly during this period, e.g. from a mean speed of 106 um s−1 at 10 s after activation in fresh water to 21 μm s−1 only 20 s later. Ovarian fluid significantly influenced sperm longevity (duration of forward mobility), per cent motility, swimming speed and the linearity of sperm movement. All of these variables generally increased as the concentration of ovarian fluid increased from 0 to 50%, even though ovarian fluid is more than three times as viscous as fresh water. It is concluded that ovarian fluid enhances sperm movement in this species and thus has the potential to influence both fertilization success and the outcome of sperm competition.

Sperm competition and the maintenance of polymorphism.

Sperm competition may occur whenever sperm from more than one male are present in the reproductive tract of the female. Studies of field-caught Drosophila reveal that a substantial fraction (80%) of females clearly have sperm from more than one male, and the figure is probably higher because only a small number of progeny are typically surveyed, so a strong skew in paternity can make multiply-mated females appear as singly mated unless appropriate models are applied. Examination of genetic variation in aspects of sperm competition has revealed some striking patterns, particularly in the implications for the maintenance of polymorphism. The magnitude of variation in sperm competitive ability is as great as that for other fitness components, and the males with the strongest displacement also appear to be the ones with the greatest positive effect on fertility. Why then does not the most competitive allele simply go to fixation? Such synergistic pleiotropy makes the polymorphism even more unexpected. Examination of patterns of competitive success of pairs of male genotypes, and of female-male interactions, demonstrate clearly that the outcome of sperm competition is not a simple property of each male. That is, sperm competitive ability of male genotypes cannot simply be ranked from best to worst. Rather, the outcome of each competitive bout depends on the particular pair of males. These results have intriguing implications for the molecular biology of genes involved in the determination of sperm competitive success, and on the opportunity for maintenance of polymorphism in those genes.

SPERM COMPETITIVE ABILITY AND GENETIC RELATEDNESS IN DROSOPHILA MELANOGASTER: SIMILARITY BREEDS CONTEMPT

Offspring of close relatives often suffer severe fitness consequences. Previous studies have demonstrated that females, when given a choice, will choose to avoid mating with closely related males. But where opportunities for mate choice are limited or kin recognition is absent, precopulatory mechanisms may not work. In this case, either sex could reduce the risks of inbreeding through mechanisms that occur during or after copulation. During mating, males or females could commit fewer gametes when mating with a close relative. After mating, females could offset the effects of mating with a closely related male through cryptic choice. Few prior studies of sperm competition have examined the effect of genetic similarity, however, and what studies do exist have yielded equivocal results. In an effort to resolve this issue, we measured the outcome of sperm competition when female Drosophila melanogaster were mated to males of four different degrees of genetic relatedness and then to a standardized competitor. We provide the strongest evidence to date that sperm competitive ability is negatively correlated with relatedness, even after controlling for inbreeding depression.

Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism.

The outcome of sperm competition in species with alternative male reproductive strategies may be determined by fair or loaded raffle mechanisms. The sperm production and quality of male Atlantic salmon using alternative reproductive tactics were investigated in order to determine the relative importance of sperm quality for male reproductive success. Sexually mature resident parr males produced greater numbers of spermatozoa per millilitre of ejaculate and invested more in their gonads as a percentage of body mass than their anadromous counterparts. Parr males had greater proportions of motile spermatozoa and a greater sperm ATP content as compared with anadromous males. Parr males invested relatively more in sperm quality and sperm numbers after the effect of body size was accounted for. In fertilization experiments, parr males fertilized greater proportions of eggs than anadromous males. A polynomial model exhibited a trade-off between testes mass and ejaculate expenditure and explained 60% of the variation. These results establish that, in sperm competition with dominant males, parr males may compensate for behavioural subordinance by producing physiologically superior spermatozoa.

Patterns of sperm precedence and predictors of paternity in the Trinidadian guppy.

Despite its widespread occurrence in animals, sperm competition has been studied in a limited range of taxa. Among the most neglected groups in this respect are internally fertilizing fish in which virtually nothing is known about the dynamics of sperm competition. In this study, we examined the outcome of sperm competition when virgin female guppies mated with two males. Behavioural cues were used to ensure that each male mated once (with female cooperation) and that sperm were successfully inseminated at copulation. Two polymorphic microsatellite loci were used to estimate the proportion of offspring sired by the second male (P2) and the results revealed a bimodal distribution with either first or (more often) second male priority The observed P2 distribution differed from that expected under the 'fair raffle' model of sperm competition. Random sperm mixing is therefore unlikely to account for the observed variance in P2 in this study. A further aim of our study was to identify predictors of male reproductive success. Using logistic linear modelling, we found that the best predictors of paternity were time to remating and the difference in courtship display rate between first and second males. Males that mated quickly and performed relatively high numbers of sigmoid displays obtained greater parentage than their slower and less vigorous counterparts. Since females are attracted to high-displaying males, our results suggest that female choice may facilitate sperm competition and/or sperm choice in guppies.

Females receive a life-span benefit from male ejaculates in a field cricket.

Mating has been found to be costly for females of some species because of toxic products that males transfer to females in their seminal fluid. Such mating costs seem paradoxical, particularly for species in which females mate more frequently than is necessary to fertilize their eggs. Indeed, some studies suggest that females may benefit from mating more frequently. The effect of male ejaculates on female life span and lifetime fecundity was experimentally tested in the variable field cricket, Gryllus lineaticeps. In field crickets, females will mate repeatedly with a given male and mate with multiple males. Females that were experimentally mated either repeatedly or multiply lived more than 32% longer than singly mated females. In addition, multiply mated females produced 98% more eggs than singly mated females. Because females received only sperm and seminal fluid from males in the experimental matings, these life-span and fecundity benefits may result from beneficial seminal fluid products that males transfer to females during mating. Mating benefits rather than mating costs may be common in many animals, particularly in species where female mate choice has a larger effect on male reproductive success than does the outcome of sperm competition.

Paternity in horseshoe crabs when spawning in multiple-male groups

Unpaired or satellite male horseshoe crabs, Limulus polyphemus, are attracted to and often form a group around a pair (a female with an attached male) that is nesting in the high intertidal zone. These males are engaged in sperm competition. We observed nesting pairs and their associated satellites in the wild, collected and reared their eggs and used genetic markers to examine paternity. We found that the unpaired, satellite males are highly successful at fertilizing eggs; two satellites can leave the attached male with few fertilizations. Two satellites together are each as successful as one spawning with a pair. A satellite's location around the female greatly affects his success, and males compete for access to a position over the dorsal canal between the prosoma and opisthosoma of the female and under the front margin of the paired male where they are most likely to fertilize eggs. Although eggs and sperm retain their viability for some time after spawning, nearly all eggs are fertilized by the satellites that are around the nesting pair at the time of egg laying and by the attached male. A number of factors including beach current, female size and male behaviour affect the outcome of sperm competition in this externally fertilizing species.

The role of male accessory gland protein Acp36DE in sperm competition in Drosophila melanogaster.

A crucial factor determining sperm fertilization success in multiply mated Drosophila melanogaster females is the efficiency with which sperm are stored. This process is modulated by the accessory gland protein Acp36DE. In this study, we show that the effect of Acp36DE on sperm storage itself alters the outcome of sperm competition. As second-mating males, Acp36DE1 (null) males had significantly lower P2-values than Acp36DE2 (truncation) or Acp36DE+ (control) males, as might be expected as the null males' sperm are poorly stored. We used spermless males, which are null for Acp36DE, to show that, in the absence of sperm co-transfer, Acp36DE itself could not displace first-male sperm. The results therefore suggest that males null for Acp36DE suffer in sperm displacement because fewer sperm are stored or retained, not because Acp36DE itself displaces sperm. Acp36DE1 (null) males also gained significantly fewer fertilizations than controls when they were the first males to mate. Using spermless males, we also showed that significantly more second-male offspring were produced following the transfer of Acp36DE by spermless first-mating males. This implies that the transfer of Acp36DE itself by the first male facilitated the storage or use of the second male's sperm and that co-transfer with sperm is not necessary for Acp36DE effects on second-male sperm storage. Acp36DE may persist in the reproductive tract and aid the storage of any sperm including those of later-mating males or prime the female for future efficient sperm storage. Our results indicate that mutations in genes that affect sperm storage can drastically affect the outcome of sperm competition.

Variation in spermathecal morphology and amount of sperm stored in populations of the simultaneously hermaphroditic land snail Arianta arbustorum

AbstractThe morphology of the sperm storage organ (spermatheca) may influence the outcome of sperm competition in a variety of invertebrate species. Simultaneously hermaphroditic pulmonates show considerable inter‐ and intraspecific variation in the structure of the spermatheca. The morphological variation in the spermatheca (number of spermathecal tubules and tubule length) and the amount of sperm stored in the tubules in 115 individuals of the simultaneously hermaphroditic land snail Arianta arbustorum (L.) from six natural populations in the Eastern Alps (Gesäuse, Austria) was examined. The populations differed in snail density, therefore in the number of potential mating partners (range: 0.9–39.8 individuals/m2) and thus in the sperm competition risk. The number of spermathecal tubules ranged from two to nine. However, the six populations did not differ in either the mean number of spermathecal tubules, the length of the main tubule (range 0.9–3.4 mm), or in the cumulative length of the tubules (range 1.5–7.8 mm). The number of tubules and tubule length were not correlated with either shell height and shell breadth or with population density. The amount of sperm stored in the spermathecal tubules was estimated. Individuals from different populations did not differ in the amount of sperm stored, and the amount of sperm stored was not correlated with population density. Results indicate that the risk of sperm competition does not affect the complexity of the spermatheca (number of spermathecal tubules) in this snail. However, the possibility that individuals in high‐density populations store sperm from more different mating partners than those in low‐density populations remains to be examined.

Sperm mobility determines the outcome of sperm competition in the domestic fowl

The aim of this study was to establish whether the mobility of sperm of the domestic fowl, as measured by an in vitro assay, predicted the outcome of sperm competition. Thirteen pairs of New Hampshire roosters, comprising one male categorized as having high-mobility sperm and the other as having average-mobility sperm, were used. Each male provided 25 x 10(6) sperm, which were mixed and artificially inseminated into between four and seven New Hampshire hens, each of which produced 2-11 offspring. The experiment was conducted twice, such that the same pair of males inseminated the same females. Paternity was assigned by using microsatellite markers. There was a clear effect of sperm-mobility phenotype on the outcome of sperm competition: in all 13 pairs the high-mobility male fathered the majority of offspring (75.3% overall; p < 0.0001). The proportion of offspring fathered by the high-mobility male within pairs varied significantly between male pairs (p < 0.0005). This effect was associated with the difference in sperm-mobility scores between males within pairs; there was a significant positive relationship between the proportion of offspring fathered by the high-mobility male and the ratio of mobility scores between males (p < 0.05). In addition, compared with their success predicted from the non-competitive situation, in the competitive situation high-mobility males were disproportionately successful in fertilizing eggs compared with average-mobility males. This may occur because female sperm storage is limited in some way and a greater proportion of high-mobility sperm gain access to the female's sperm storage tubules. There was no evidence that female effects accounted for any of the variation in paternity.

VARIATION OF SPERM PRECEDENCE IN THE ROVE BEETLE ALEOCHARA CURTULA (COLEOPTERA: STAPHYLINIDAE)

Abstract In order to quantify the outcome of sperm competition in the mating system of the rove beetle Aleochara curtula we performed three different mating experiment series. Paternity was established by DNA fingerprinting with oligonucleotide probes. We found a precedence of the last male with a proportion of eggs fathered by the last male of 87% (median). Nevertheless, we observed a large variation of P2-values in A. curtula and cases of mixed paternity were documented as well as cases of 100% or 0% paternity of the last male. The variation of P2-values correlates with the efficiency of spermatophore and sperm transfer.

Sperm competition in birds.

Sperm competition in birds occurs when a female is inseminated by more than one male during a single breeding cycle. Despite most birds being socially monogamous, sperm competition is widespread and results in frequent extra-pair paternity. Sperm competition is a fundamental part of sexual selection since it results in differential reproductive success among males. Male adaptations to sperm competition include relatively large testes, large sperm stores and long spermatozoa, mate guarding and frequent pair copulations. Females show no obvious morphological adaptations to sperm competition but, by controlling whether copulations are successful, they probably determine its frequency and extent. Despite this, the evolutionary benefits females acquire from extra-pair fertilizations are poorly understood. Experiments in which females are inseminated with equal numbers of spermatozoa from two males usually show last male sperm precedence. Understanding the mechanism of sperm competition requires understanding of why the last male to inseminate a female fertilizes a disproportionate number of eggs. The data from sperm competition studies on the domestic fowl, turkeys and zebra finches are consistent only with a passive sperm loss model of sperm competition. The mechanism is as follows: after insemination, spermatozoa enter the sperm storage tubules located in the oviduct, from which they are lost at a constant rate over days or weeks. All else being equal, the interval between two inseminations determines the probability of fertilization: the second of two inseminations fertilizes most eggs simply because, by the time fertilization occurs, fewer of these spermatozoa have been lost. Other factors also affect the outcome of sperm competition: the timing of insemination relative to oviposition, the differential fertilizing capacity of males and differences in the numbers of spermatozoa inseminated; as a consequence, last male sperm precedence is not automatic. On the basis of the mechanism of sperm competition, the optimal strategy for both males and females to maximize their likelihood of extra-pair fertilization is to copulate with an extra-pair partner as close as possible to the onset of oviposition.

Sperm competition in birds

Sperm competition in birds occurs when a female is inseminated by more than one male during a single breeding cycle. Despite most birds being socially monogamous, sperm competition is widespread and results in frequent extra-pair paternity. Sperm competition is a fundamental part of sexual selection since it results in differential reproductive success among males. Male adaptations to sperm competition include relatively large testes, large sperm stores and long spermatozoa, mate guarding and frequent pair copulations. Females show no obvious morphological adaptations to sperm competition but, by controlling whether copulations are successful, they probably determine its frequency and extent. Despite this, the evolutionary benefits females acquire from extra-pair fertilizations are poorly understood. Experiments in which females are inseminated with equal numbers of spermatozoa from two males usually show last male sperm precedence. Understanding the mechanism of sperm competition requires understanding of why the last male to inseminate a female fertilizes a disproportionate number of eggs. The data from sperm competition studies on the domestic fowl, turkeys and zebra finches are consistent only with a passive sperm loss model of sperm competition. The mechanism is as follows: after insemination, spermatozoa enter the sperm storage tubules located in the oviduct, from which they are lost at a constant rate over days or weeks. All else being equal, the interval between two inseminations determines the probability of fertilization: the second of two inseminations fertilizes most eggs simply because, by the time fertilization occurs, fewer of these spermatozoa have been lost. Other factors also affect the outcome of sperm competition: the timing of insemination relative to oviposition, the differential fertilizing capacity of males and differences in the numbers of spermatozoa inseminated; as a consequence, last male sperm precedence is not automatic. On the basis of the mechanism of sperm competition, the optimal strategy for both males and females to maximize their likelihood of extra-pair fertilization is to copulate with an extra-pair partner as close as possible to the onset of oviposition.

A Possible Explanation for Cryptic Female Choice in the Yellow Dung Fly, Scathophaga stercoraria (L.)

AbstractCryptic, or post‐copulatory, female choice could markedly affect the outcome of sperm competition, i.e. a female could differentially manipulate ejaculates within her own body, affecting the fertilization successes of her mating partners. Female yellow dung flies, Scathophaga (Scatophaga) stercoraria, have three spermathecae, the sperm‐storage organs, and can to some extent store the sperm of different males in different places. I show that a female's body size, as well as those of her mates, influences the process of sperm storage. Furthermore, females lay eggs of different genotypes under different environmental conditions. Females use both cues correlated with single locus variation (at the locus for the enzyme phosphoglucomutase, PGM) and quantitative trait variation (in body size and development time) when using sperm to fertilize their eggs. It is proposed that this allows a female to match the genotypes of her offspring to the conditions in which the larvae must grow, thus increasing their subsequent fitness. I describe an experiment where larvae of different PGM genotypes were raised in different environments and the most successful genotype was different in different environments. The complexity of the female reproductive system may therefore have evolved because the best father for a female's offspring, from the female's viewpoint, is different under different environmental conditions. The effect interacts with the established male‐determined effects to influence the outcome of sperm competition.

Complex Female Reproductive Tract Morphology: Its Possible Use in Postcopulatory Female Choice

Sperm competition has traditionally been modelled exclusively from the male perspective with females as passive participants. However females of many species have a physiologically and morphologically complex reproductive system (e.g. multiple sperm stores), which could enable them to control or influence offspring paternity by postcopulatory sperm selection. Previously the female reproductive tract has been modelled using a single sperm store. The model here describes the effects of a hostile site of insemination and two (or more) sperm stores in the outcome of sperm competition. If there was mortality of sperm directly after insemination, the main difference between having one or two stores was the number of possible choices. One-store females could choose the storage rates for different males and thereby influence paternity. Two-store females could choose the storage rates for different males differently in each store and later by choosing sperm from a particular store could favour a male at fertilisation. Without sperm mortality females with one store could hardly influence paternity. It was determined by female storage capacity relative to male ejaculate size. In contrast, females with two stores still achieved a clear separation of competing ejaculates, despite counteracting sperm displacement favouring last mates. This could give females the ultimate control over paternity through the selective use of sperm from each storage site, e.g. depending on environmental factors. As females of many animal groups may be able to spatially separate competing sperm in their multiple sperm stores (e.g. flies, spiders, birds) these results could have general significance for the evolution of female control of paternity.