Sperm competition in mammals

Female promiscuity can lead to the spermatazoa of several males 'competing' to fertilize the ova of a single female. Such promiscuity is relatively common among mammals and has resulted in a suite of adaptations associated with sperm competition. In the last decade, laboratory scientists using experimental techniques have clarified the physiological and behavioural mechanisms that result from sperm competition. Field biologists have collected data on a variety of mammals to test predictions of sperm competition theory. Unfortunately, theories developed and tested in laboratory situations do not always explain variation in behaviour observed in field studies.     

Copula in yellow dung flies (Scathophaga stercoraria): investigating sperm competition models by histological observation

While sperm competition has been extensively studied, the mechanisms involved are typically not well understood. Nevertheless, awareness of sperm competition mechanisms is currently recognised as being of fundamental importance for an understanding of many behavioural strategies. In the yellow dung fly, a model system for studies of sperm competition, second male sperm precedence appears to result from a combination of sperm displacement and sperm mixing. Displacement was until recently thought to be directly from the female's sperm stores, the spermathecae (i.e. males were thought to ejaculate directly into these stores), and under male control. However, recent work indicates displacement is indirect (i.e. males do not ejaculate directly into the sperm stores) and that it is female-aided, although the evidence was not based on direct observation. Here, we used histological techniques to directly determine interactions during copula and sperm transfer. Our results are consistent with inference and clearly show that males ejaculate into the bursa copulatrix. Our data are also consistent with active female involvement in sperm displacement, which is indirect, and indicate the aedeagus may remove some spermatozoa from the bursa at the end of copula. In addition, evidence suggests females aid sperm transport to and from the spermathecae, possibly by muscular movement of a spermathecal invagination.     

THE EVOLUTION OF EUTHERIAN SPERMATOZOA AND UNDERLYING SELECTIVE FORCES: FEMALE SELECTION AND SPERM COMPETITION

We have examined sperm morphology and dimensions in Eutherian mammals. In most Eutherians, sperm heads are round or oval and spermatozoa have short tails (average sperm length about 65 microns; range = 33-121 microns). Rodents, however, clearly depart from the typical Eutherian pattern in that they show a broad array of head morphs and an extreme range of sperm dimensions (35-250 microns). In order to trace the evolutionary changes that rodent sperm have undergone, we have used phylogenetic relationships based on biogeographical, morphological, chromosomal and genic data, and we have superimposed onto them the information available on sperm traits. Analyses were carried out for five rodent groups on which enough information was available. The evolutionary trends which emerged from these studies have two main points in common: throughout evolution spermatozoa have become enlarged and morphologically more complex, and this process seems to have taken place independently in different lineages. A general model was developed which outlines the different evolutionary pathways that rodent sperm have undergone. The adaptive significance of the increase in head complexity and the elongation of the sperm tail remains obscure. We have integrated information from evolutionary, physiological and behavioural studies to address this issue. We argue that two main selective forces may have favoured these changes: female selection within the reproductive tract and sperm competition. The female tract represents a formidable barrier for spermatozoa and its provides an environment where numerous interactions take place. The extent of these barriers and the complexity of these poorly understood interactions suggest that females may be exercising a strong selection, which may enable them to favour particular types of spermatozoa or ejaculates from particular males. Throughout their evolution males must have evolved adaptations to overcome these barriers, and the conflicting interests of choosy females. Sperm competition is a potent evolutionary force among mammals, which has influenced not only the evolution of sperm numbers but also changes in sperm dimensions. Thus, sperm competition has favoured the elongation of the sperm tail, which has led to the attainment of faster swimming speed, an important factor when sperm from rival males compete to reach the ova first.     

Mechanisms of sperm competition: Linking physiology and behavioural ecology

Sperm competition has received a great deal of attention from behavioural ecologists because it is the ultimate form of male-male competition, and may also be important for female choice. It is becoming clear that the adaptive value of the behavioural strategies of males and females will not be fully understood until we have a better understanding of the physiological mechanisms that come into play after copulation. We now have enough information to compare the underlying mechanisms in birds and mammals and to relate these to the way in which sperm competition operates in both groups. To integrate this knowledge, the boundaries between behavioural ecology and physiology will have to be crossed in what promises to be a most fruitful enterprise.     

Pitfalls in experiments testing predictions from sperm competition theory

As females of many species mate with more than one male, ejaculates often face competition from the sperm of other males. In recent years, numerous papers have been published on theoretical predictions of evolutionary, behavioural and physiological responses to variation in the strength of sperm competition (SC). These theoretical predictions have also been extensively tested. However, although predictions from SC theory are relatively straightforward, extra caution has to be paid in the design of experiments testing them. One difficulty is for example to disentangle immediate and mean SC risk and intensity. Without carefully designed experiments, it is also very easy to simultaneously increase SC risk and the probability of intense SC--a situation for which we currently have no clear predictions, as the theoretical models to date only assume variation in either SC risk or intensity. In this paper, we discuss these and some other pitfalls related to manipulations of SC risk and intensity and suggest how to avoid them.     

Female control of paternity

Of the two components of sexual selection, female choice is much less obvious than male-male competition, and hence has always been considered to be of secondary importance. However, recent field observations and new theory have brought about a radical change of emphasis. It now appears that although a female's choice of who fathers her offspring often occurs in a subtle manner, it may be widespread and take place through a variety of behavioural and physiological mechanisms, including the manipulation of male behaviour and the selection of sperm within the female reproductive tract.     

Sperm storage and utilization in female Queensland fruit flies (Bactrocera tryoni)

Abstract.  Female animals that use sperm from a single mating to fertilize eggs over an extended period require efficient mechanisms for sperm storage and use. There have been few studies of these mechanisms in tephritid flies. Mating, copula duration, sperm storage and sperm usage patterns are assessed in an Australian tephritid, the Queensland fruit fly ( Bactrocera tryoni ; a.k.a. 'Q-fly'). In particular, the present study investigates whether each of these aspects of mating varies in relation to female size or male size, whether sperm storage patterns change over time after mating (1, 5, 10 and 15 days), and the relative roles of the ventral receptacle and the two spermathecae as sperm storage organs. Large females are more likely to mate than are small females, and are also more fecund in the first 5 days after mating. Females are more likely to store some sperm and, among those that store some sperm, store more sperm if their mate is large. Most sperm are stored in the spermathecae (median = 97%), often with high levels of asymmetry between the two spermathecae. Asymmetry of sperm storage is related to number of sperm stored, but not to male or female size. Total number of stored sperm declines over the 15 days after mating, but this decrease in sperm numbers only reflects changes in the spermathecae; numbers of sperm in the ventral receptacle remain unchanged over this period. As a consequence, the proportion of total sperm stored in the spermathecae declines relative to the ventral receptacle. These results are consistent with a system in which small numbers of sperm are maintained in the ventral receptacle for fertilizations, and are replenished by sperm from the spermathecae as required. Sperm distribution and usage patterns in Q-flies are comparable with recent findings in medflies, Ceratitis capitata , but differ markedly from patterns found in several Anastrepha species.     

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.     

The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism

When females are inseminated by more than one male (polyandry) sexual selection continues after insemination in the form of sperm competition and cryptic female choice. The sexually-selected sperm hypothesis proposes that, under the risk of sperm competition, additive variation in male traits determining fertilising efficiency will select for female propensity to be polyandrous in order to increase the probability of producing sons with superior fertilising efficiency. Two factors complicate this prediction: sex-biased transmission of male fertilising efficiency traits and sexual antagonism of sex-limited traits, fostered by sex-biased inheritance. Here, we (i) review the evidence that male traits contributing towards fertilising efficiency are heritable through sex-biased mechanisms, and (ii) explore the evolutionary implications for male and female reproductive strategies caused by both sex-biased transmission and sexual antagonism of fertilising efficiency traits. Many male fertilising efficiency traits are heritable through sex-biased mechanisms and may not necessarily increase female fitness. The predictions of the sexually-selected sperm hypothesis change dramatically under these different mechanisms of inheritance of fertilising efficiency traits, and different fitness pay-offs derived by females from the expression of such traits. Both sex-biased control of fertilising efficiency and sexual antagonism may also be important in explaining the maintenance of the genetic variance and selection potential of fertilising efficiency. We propose that a useful approach to test the sexually-selected sperm hypothesis is to combine studies which identify behavioural and physiological mechanisms explaining variation in reproductive success with artificial selection experiments to infer the underlying evolutionary patterns.     

A nonsemen copulatory fluid influences the outcome of sperm competition in Japanese quail

Sperm competition is a powerful and widespread evolutionary force that drives the divergence of behavioural, physiological and morphological traits. Elucidating the mechanisms governing differential fertilization success is a fundamental question of sperm competition. Both sperm and nonsperm ejaculate components can influence sperm competition outcomes. Here, we investigate the role of a nonsemen copulatory fluid in sperm competition. Male Japanese quail possess a gland that makes meringue‐like foam. Males produce and store foam independent of sperm and seminal fluid, yet transfer foam to females during copulation. We tested whether foam influenced the outcome of sperm competition by varying foam state and mating order in competitive matings. We found that the presence of foam from one male decreased the relative fertilization success of a rival, and that foam from a given male increased the probability he obtained any fertilizations. Mating order also affected competitive success. Males mated first fertilized proportionally more eggs in a clutch and had more matings with any fertilizations than subsequent males. We conclude that the function of foam in sperm competition is mediated through the positive interaction of foam with a male's sperm, and we speculate whether the benefit is achieved through improving sperm storage, fertilizing efficiency or retention. Our results suggest males can evolve complex strategies to gain fertilizations at the expense of rivals as foam, a copulatory fluid not required for fertilization, nevertheless, has important effects on reproductive performance under competition.     

Do Fig Wasps Produce Mixed Paternity Clutches?

Pollinating fig wasps (Hymenoptera, Agaonidae) have been the focus of numerous studies examining sex ratio evolution. Recently, molecular genetic techniques have been introduced that assume single matings in fig wasps, yet their mating biology has not been investigated genetically. We used recently developed microsatellite markers to investigate whether a pollinating fig wasp (Liporrhopalum tentacularis Grandi) produces single or mixed paternity clutches. The clutches of 12 females which had had the opportunity to mate with males of different genotypes were investigated. The results suggest that, at least in this species of fig wasp, single paternity clutches are the norm. Based on our behavioural observations, this appears to be due to mating with a single male rather than sperm competition.     

Female genotype affects male success in sperm competition

The central question addressed by most studies of sperm competition is: ''what determines which male''s sperm are used at fertilization?'' Empirical and theoretical studies that address this question have traditionally focused on adaptations which enhance male fertilization success while treating the female as a receptacle in which sperm competition is played out. Here we provide evidence which suggests that female genotype strongly influences the outcome of sperm competition. When the sperm of two males are in competition the proportion of offspring fathered by the second male to mate (P₂) was found to be highly repeatable only if the male pair were mated to three different, but genetically similar females (full-sisters to each other; unrelated to either of the males). In contrast, if a male pair were mated to three females that were unrelated then P₂ was either non-repeatable or marginally repeatable. We also show that male success in sperm competition is determined, to a large extent, by gamete and/or male–female compatibility. This conclusion is derived from the observation that P₂ was repeatable among full-sisters mated to different, yet genetically similar male pairings, whilst P₂ was non-repeatable among full-sisters mated to different, genetically distinct male pairings.     

Structure and allometry of genitalia in males and females of a social African ground squirrel with high polygynandry

The few studies that have looked at genital allometry in mammals have typically shown a positively allometric relationship with body size and high coefficients of variation. Cryptic female choice, sexual conflict or sperm competition are mechanisms underlying genital evolution and as these are not mutually exclusive, they are often difficult to disentangle. In addition, these mechanisms are affected by both male and female social structure and/or mating strategies and, as such, pre- and post-copulatory behaviours have been shown to alter selection on genitalia. We examined genital traits and allometry in a polygynandrous and social ground squirrel Xerus inauris . We found that male testes are positively allometric and account for 1.5% of their body weight, one of the highest percentages known for sciurids. The penis, at 42.4% of head/body length, was isometric while the female reproductive tract, 22.4% head/body length, demonstrated no such relationship. Based on the allometric relationships of both males and females presented here, in conjunction with high levels of competition for females and lack of male aggression and territoriality, we suggest that sperm competition is the most likely mechanism for the evolution of the extremely large genitalia in this species.     

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

Abstract.— 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.     

Changes in sperm stores, ejaculate size, fertilization success, and sexual motivation over repeated matings in the common toad, Bufo bufo (Anura: Bufonidae)

Fertilization is of central importance in the determination of reproductive success for both males and females. In species where males have the chance to mate repeatedly within a short period of time, sperm stocks may become depleted and males may have to carefully economize on their sperm reserves. Also, intensive intrasexual competition for females and repeated matings may lead to exhaustion on the behavioural level. To determine whether the reproductive potential of males is limited and if such a limitation is due to behavioural exhaustion or sperm depletion, we experimentally investigated changes in sperm stores, sperm expenditure, fertilization success, and sexual motivation over three repeated matings in the common toad, Bufo bufo , where the breeding season is short and sequential polygyny occurs. At the end of the breeding season, the number of sperm stored in the testes of males mated repeatedly was close to 50% lower than in testes of unmated males. Ejaculate size, which was estimated by applying a novel method allowing direct quantification, decreased by 88% from first to third matings. We also observed a drop in fertilization success from the first two to third matings by 65%, which was largest in males that had started the reproductive season in bad body condition. Some of these males also showed a decreased interest in females in the third mating round. Our results suggest that sperm depletion and loss of sexual motivation may together set a limit to the reproductive potential of common toad males. The present study draws attention to a limitation in reproductive potential, which may occur more often than currently anticipated and has the potential to strongly influence several aspects of reproductive behaviour.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 361–371.     

The Effect of Female Quality on Male Ejaculatory Expenditure and Reproductive Success in a Praying Mantid

Strategic ejaculation is a behavioural strategy shown by many animals as a response to sperm competition and/or as a potential mechanism of cryptic male choice. Males invest more mating resources when the risk of sperm competition increases or they invest more in high quality females to maximize their reproductive output. We tested this hypothesis in the false garden mantid Pseudomantis albofimbriata, where females are capable of multiply mating and body condition is an indicator of potential reproductive fitness. We predicted male mantids would ejaculate strategically by allocating more sperm to high quality females. To determine if and how males alter their ejaculate in response to mate quality, we manipulated female food quantity so that females were either in good condition with many eggs (i.e. high quality) or poor condition with few eggs (i.e. low quality). Half of the females from each treatment were used in mating trials in which transferred sperm was counted before fertilisation occurred and the other half of females were used in mating trials where fertilisation occurred and ootheca mass and total eggs in the ootheca were recorded. Opposed to our predictions, the total number of sperm and the proportion of viable sperm transferred did not vary significantly between female treatments. Male reproductive success was entirely dependent on female quality/fecundity, rather than on the number of sperm transferred. These results suggest that female quality is not a major factor influencing postcopulatory male mating strategies in P. albofimbriata, and that sperm number has little effect on male reproductive success in a single mating scenario.     

Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success

Sperm competition occurs when sperm from more than one male compete for fertilizations. This form of post-copulatory sexual selection is recognized as a significant and widespread force in the evolution of male reproductive biology and as a key determinant of differential male reproductive success. Despite its importance, however, detailed mechanisms of sperm competition at the gamete level remain poorly understood. Here, we use natural variation in spermatozoal traits among wild Atlantic salmon (Salmo salar), a species naturally adapted to sperm competition, to examine how the relative influences of sperm (i) number, (ii) velocity, (iii) longevity, and (iv) total length determine sperm competition success. Atlantic salmon fertilize externally, and we were therefore able to conduct controlled in vitro fertilization competitions while concurrently measuring spermatozoal traits within the aqueous micro-environment to which salmon gametes are naturally adapted. Microsatellite DNA fingerprinting revealed that a male's relative sperm velocity was the primary determinant of sperm competition success. There was no significant relationship between fertilization success and either relative sperm number or total length; sperm longevity showed an inverse relationship with competition success. These relationships were consistent for two experimental repeats of the in vitro fertilization competitions. Our results therefore show, under the natural microenvironment for salmon gametes, that relative sperm velocity is a key spermatozoal component for sperm competition success. Atlantic salmon sperm can be considered to enter a competition analogous to a race in which the fastest sperm have the highest probability of success.     

Sexual Strategies of a North American ‘Tarantula’ (Araneae: Theraphosidae)

Despite their general notoriety and popularity as pets, little is known of the behavioural ecology of ‘tarantulas’ or theraphosid spiders. We studied a theraphosid of the Arizona deserts, Aphonopelma sp., to determine behavioural events crucial to successful courtship and mating. Males search for spatially scattered females and, at short range, may detect females by substrate-borne cues. When two males are present with a single female, no direct competition such as aggression is observed. Both males may mate with a single female in rapid succession, with no evidence of post-copulatory mate guarding. Despite the potential for sexual cannibalism, courtship and mating behaviour patterns exhibit few aggressive elements and males nearly always survive sexual encounters with females. The mating system of this Aphonopelma species may best be described as a type of scramble-competition polygyny, in which the ability of males to locate receptive females is an important determinant of mating success in males. Multiple mating by females renders predictions concerning fertilization success uncertain, due to the possibility of sperm competition and ‘cryptic’ female mate choice.     

Sperm competition and ejaculate economics

Sperm competition was identified in 1970 as a pervasive selective force in post‐copulatory sexual selection that occurs when the ejaculates of different males compete to fertilise a given set of ova. Since then, sperm competition has been much studied both empirically and theoretically. Because sperm competition often favours large ejaculates, an important challenge has been to understand the evolution of strategies through which males invest in sperm production and economise sperm allocation to maximise reproductive success under competitive conditions. Sperm competition mechanisms vary greatly, depending on many factors including the level of sperm competition, space constraints in the sperm competition arena, male mating roles, and female influences on sperm utilisation. Consequently, theoretical models of ejaculate economics are complex and varied, often with apparently conflicting predictions. The goal of this review is to synthesise the theoretical basis of ejaculate economics under sperm competition, aiming to provide empiricists with categorised model assumptions and predictions. We show that apparent contradictions between older and newer models can often be reconciled and there is considerable consensus in the predictions generated by different models. We also discuss qualitative empirical support for some of these predictions, and detail quantitative matches between predictions and observations that exist in the yellow dung fly. We argue that ejaculate economic theory represents a powerful heuristic to explain the diversity in ejaculate traits at multiple levels: across species, across males and within individual males. Future progress requires greater understanding of sperm competition mechanisms, quantification of trade‐offs between ejaculate allocation and numbers of matings gained, further knowledge of mechanisms of female sperm selection and their associated costs, further investigation of non‐sperm ejaculate effects, and theoretical integration of pre‐ and post‐copulatory episodes of sexual selection.     

How the sperm lost its tail: the evolution of aflagellate sperm

The typical sperm is comprised of a head, midpiece and flagellum. Around this theme there is an enormous diversity of form--giant sperm, multi-flagellate sperm and also sperm that lack flagella entirely. Explaining this diversity in sperm morphology is a challenging question that evolutionary biologists have only recently engaged in. Nonetheless, one of the selective forces identified as being an important factor in the evolution of sperm form is sperm competition, which occurs when the sperm of two or more males compete to fertilize a female's ova. In species with a truly monandrous mating system, the absence of sperm competition means that the selection pressure on males to produce motile sperm may be relaxed. Potentially aflagellate sperm are less costly to produce, both in terms of energy and time. Thus, selection may therefore favour the loss of the sperm flagellum and any other motile mechanisms in monandrous taxa. A review of the literature revealed that 36 taxonomic groups, from red algae to fish, were found independently to have evolved aflagellate sperm. I review what is known about the mating systems of each of these taxa and their nearest sister taxa. A sister-group analysis using this information provided weak evidence suggesting that the evolution of aflagellate sperm could be linked to the removal of selective pressures generated by sperm competition.