Sperm design and sperm function

Spermatozoa vary enormously in their form and dimensions, both between and within species, yet how this variation translates into fertilizing efficiency is not known. Sperm swimming velocity is a key determinant of male fertilization success, but previous efforts to identity which sperm phenotypic traits are associated with swimming velocity have been unsuccessful. Here, we examine the relationship between the size of several sperm components and sperm swimming velocity in natural populations of red deer (Cervus elaphus hispanicus) where selective pressures to enhance male reproductive success are expected to be strong. Our results show that there is little within-male and considerable between-male variation in sperm dimensions. Spermatozoa with longer midpieces swim more slowly, a finding which does not support the hypothesis that the size of the midpiece determines the amount of energy which is translated into swimming speed. In contrast, spermatozoa with elongated heads, and those in which the relative length of the rest of the flagellum is longer, swim faster. Thus, the hydrodynamic shape of the head and the forces generated by the relative size of the rest of the flagellum seem to be the key determinants of sperm swimming velocity.     

Non-invasive collection and analysis of semen in wild macaques

Assessments of primate male fertility via semen analyses are so far restricted to captivity. This study describes a non-invasive method to collect and analyse semen in wild primates, based on fieldwork with Yakushima macaques (Macaca fuscata yakui). Over nine mating seasons between 1993 and 2010, 128 masturbatory ejaculations were recorded in 21 males of 5 study troops, and in 11 non-troop males. In 55 %, ejaculate volume was directly estimated, and in 37 %, pH-value, sperm vitality, numbers, morphology and swimming velocity could also be determined. This approach of assessing semen production rates and individual male fertility can be applied to other primate taxa, in particular to largely terrestrial populations where males masturbate frequently, such as macaques and baboons. Furthermore, since explanations of male reproductive skew in non-human primate populations have until now ignored the potential role of semen quality, the method presented here will also help to answer this question.     

Long sperm fertilize more eggs in a bird

Sperm competition, in which the ejaculates of multiple males compete to fertilize a female''s ova, results in strong selection on sperm traits. Although sperm size and swimming velocity are known to independently affect fertilization success in certain species, exploring the relationship between sperm length, swimming velocity and fertilization success still remains a challenge. Here, we use the zebra finch (Taeniopygia guttata), where sperm size influences sperm swimming velocity, to determine the effect of sperm total length on fertilization success. Sperm competition experiments, in which pairs of males whose sperm differed only in length and swimming speed, revealed that males producing long sperm were more successful in terms of (i) the number of sperm reaching the ova and (ii) fertilizing those ova. Our results reveal that although sperm length is the main factor determining the outcome of sperm competition, complex interactions between male and female reproductive traits may also be important. The mechanisms underlying these interactions are poorly understood, but we suggest that differences in sperm storage and utilization by females may contribute to the outcome of sperm competition.     

No evidence of inbreeding depression in sperm performance traits in wild song sparrows

Inbreeding is widely hypothesized to shape mating systems and population persistence, but such effects will depend on which traits show inbreeding depression. Population and evolutionary consequences could be substantial if inbreeding decreases sperm performance and hence decreases male fertilization success and female fertility. However, the magnitude of inbreeding depression in sperm performance traits has rarely been estimated in wild populations experiencing natural variation in inbreeding. Further, the hypothesis that inbreeding could increase within‐ejaculate variation in sperm traits and thereby further affect male fertilization success has not been explicitly tested. We used a wild pedigreed song sparrow (Melospiza melodia) population, where frequent extrapair copulations likely create strong postcopulatory competition for fertilization success, to quantify effects of male coefficient of inbreeding (f) on key sperm performance traits. We found no evidence of inbreeding depression in sperm motility, longevity, or velocity, and the within‐ejaculate variance in sperm velocity did not increase with male f. Contrary to inferences from highly inbred captive and experimental populations, our results imply that moderate inbreeding will not necessarily constrain sperm performance in wild populations. Consequently, the widely observed individual‐level and population‐level inbreeding depression in male and female fitness may not stem from reduced sperm performance in inbred males.     

Antlers honestly advertise sperm production and quality

Evolutionary theory proposes that exaggerated male traits have evolved via sexual selection, either through female mate choice or male-male competition. While female preferences for ornamented males have been amply demonstrated in other taxa, among mammals sexual characters are commonly regarded as weapons whose main function is to enhance male competitiveness in agonistic encounters. One particularly controversial hypothesis to explain the function of male sexual characters proposes that they advertise male fertility. We test this hypothesis in red deer (Cervus elaphus), a species where sexual characters (antlers) reach an extreme degree of elaboration. We find that a global measure of relative antler size and complexity is associated with relative testes size and sperm velocity. Our results exclude the possibility that condition dependence, age or time of culling, drive these associations. Red deer antlers could signal male fertility to females, the ability to avoid sperm depletion throughout the reproductive season and/or the competitive ability of ejaculates. By contrast, male antlers could also signal to other males not only their competitive ability at the behavioural level (fighting ability) but also at the physiological level (sperm competition).     

Implications of diversity in sperm size and function for sperm competition and fertility

Sperm competition is now recognised as a potent selective force shaping many male reproductive traits. While the influence of sperm competition on sperm number is widely accepted, its effects upon sperm size remain controversial. It had been traditionally assumed that there is a trade-off between sperm number and sperm size, so that an increase in sperm number would result in a decrease in sperm size, under conditions of sperm competition. Contrary to this prediction, we proposed some time ago that sperm competition favours an increase in sperm size, because longer sperm swim faster and are more likely to win the race to fertilize ova. Comparative studies between species show that in many taxa such a relationship exists, but the consequences of an increase in sperm size may vary between taxa depending on the environment in which spermatozoa have to compete. We present new evidence showing that in mammals longer sperm swim at higher speeds. We also show that mean swimming speed is highly correlated with maximum swimming speed, so even if the fastest swimming sperm are more likely to fertilize, both measures are informative. When individuals of the same species are compared, ratios between the dimensions of different sperm components, as well as the shape of the head, seem better at explaining sperm swimming velocity. Finally, we show that mean and maximum sperm swimming speed determine male fertility. Other studies have shown that in competitive contexts, males with faster swimming sperm have higher fertilization success. We conclude that the available evidence supports our original hypothesis.     

Between‐male variation in sperm size,velocity and longevity in sand martins Riparia riparia

Sperm mobility is known to be an important determinant of a male's sperm competitive ability. Although more debated, sperm length and its relation to sperm swimming ability has also been proposed to determine a male's fertilisation potential. Furthermore, both mobility and length may covary with a male's phenotype, either positively (the phenotype‐linked fertility hypothesis) or negatively if, for instance, low‐quality males have less access to females but invest more in sperm production. Using dummy females, we collected sperm samples from wild sand martins Riparia raparia males. We investigated the relationship between sperm length and sperm swimming speed as measured by sperm straight line velocity (VSL), and determined whether sperm traits are correlated with male body size and condition. We found that total sperm length is repeatable within‐ejaculate and shows substantial inter‐male variation. Sperm length was associated with sperm velocity: males with short sperm have sperm that swim initially faster but die sooner, whereas males with longer sperm have sperm that swim more slowly but for a longer time. Smaller males produced sperm with higher overall velocity. This correlation between male size and sperm behaviour may reflect alternative fertilisation strategies where small males having less mating opportunities invest more in sperm competitive ability. The existence of such alternative strategies would participate in maintaining variation in sperm length and velocity in this species.     

Sperm Swimming Velocity Predicts Competitive Fertilization Success in the Green Swordtail Xiphophorus helleri

Sperm competition is expected to favour the evolution of traits that influence the performance of sperm when they compete to fertilize a female''s eggs. While there is considerable evidence that selection favours increases in sperm numbers, much less is known about how sperm quality contributes towards competitive fertilization success. Here, we determine whether variation in sperm quality influences competitive fertilization success in the green swordtail Xiphophorus helleri, a highly promiscuous livebearing fish. We use artificial insemination as a method of controlled sperm delivery and show that sperm swimming velocity is the primary determinant of fertilization success when ejaculates from two males compete to fertilize a female''s eggs. By contrast, we found no evidence that sperm length had any effect on siring success. We also found no evidence that pre- and postcopulatory sexual traits were phenotypically integrated in this species, suggesting that the previous observation that reproductive skew favours males with high mating rates is unlikely to be due to any direct association between sperm quality and male sexual ornamentation.     

Early determinants of lifetime reproductive success differ between the sexes in red deer.

In polygynous, sexually dimorphic species, sexual selection should be stronger in males than in females. Although this prediction extends to the effects of early development on fitness, few studies have documented early determinants of lifetime reproductive success in a natural mammal population. In this paper, we describe factors affecting the reproductive success of male and female red deer (Cervus elaphus) on the island of Rum, Scotland. Birthweight was a significant determinant of total lifetime reproductive success in males, with heavier-born males being more successful than lighter ones. In contrast, birthweight did not affect female reproductive success. High population density and cold spring temperatures in the year of birth decreased several components of fitness in females, but did not affect the breeding success of males. The results confirm the prediction that selection on a sexually dimorphic trait should be greater in males than in females, and explain the differential maternal expenditure between sons and daughters observed in red deer. Differences between the sexes in the effects of environmental and phenotypic variation on fitness may generate differences in the amount of heritable genetic variation underlying traits such as birthweight.     

Taking advantage of the use of supervised learning methods for characterization of sperm population structure related with freezability in the Iberian red deer

Using Iberian red deer as a model, this study presents a supervised learning method, the Support Vector Machines (SVM), to characterize sperm population structure related with freezability. Male freezability was assessed by evaluating motility, membrane status and mitochondrial membrane potential of sperm after a freezing-thawing procedure. The SVM model was generated using sperm motility information captured by computer-assisted sperm analysis (CASA) from thawed semen, belonging to six stags with marked differences on their freezability. A total of 1369 sperm tracks were recorded for seven kinematic parameters and assigned to four motility patterns based on them: weak motile, progressive, transitional and hyperactivated-like. Then, these data were split in two sets: the training set, used to train the SVM model, and the testing set, used to examine how the SVM method and three other unsupervised methods, a non-hierarchical, a hierarchical and a multistep clustering procedures, performed the sperm classification into subpopulations. The SVM was revealed as the most accurate method in the characterization of sperm subpopulations, showing all the sperm subpopulations obtained in this way high significant correlations with those sperm parameters used to characterize freezability of males. Given its superiority, the SVM method was used to characterize the sperm motile subpopulations in Iberian red deer. Sperm motile data from frozen-thawed semen belonging to 25 stags were recorded and loaded into the SVM model. The sperm population structure revealed that those males showing poor freezability were characterized by high percentages of sperm with a weak motility pattern. In opposite, males showing good freezability were characterized by higher percentages of sperm with a progressive and hyperactivated-like motility pattern and lower percentages of sperm with a weak motile pattern. We also identified a sperm subpopulation with a transitional motility pattern. This subpopulation increased as the freezability of males improved, and may be used as indicative of overall sperm motility.     

圈养猞猁多雄交配雄性的成功繁殖

研究了笼养猞猁多雄交配的结果以及雄性的成功繁殖。雄兽与发情雌兽随机配对,其繁殖成功(所产生的后代数量)不取决于与雌兽的交配顺序、交配次数与持续时间、遗传关系或雄兽的行为特征,但似乎取决于精子质量,特别是取决于形态正常精子的百分率。繁殖成功的雄兽比其竞争对手具有更多的形态正常的精子,似乎更能成功地诱发交配雌兽的排卵。证实了4窝(占总窝数的20%)幼兽的双重父亲身份。在所有情形下, 2雄1雌的交配间隔为24h 。     

Male sexual ornament size is positively associated with reproductive morphology and enhanced fertility in the stalk-eyed fly <Emphasis Type="Italic">Teleopsis dalmanni</Emphasis>

Background  

Exaggerated male ornaments and displays often evolve in species where males only provide females with ejaculates during reproduction. Although "good genes" arguments are typically invoked to explain this phenomenon, a simpler alternative is possible if variation in male reproductive quality (e.g. sperm number, ejaculate content, mating rate) is an important determinant of female reproductive success. The "phenotype-linked fertility hypothesis" states that female preference for male ornaments or displays has been selected to ensure higher levels of fertility and has driven the evolution of exaggerated male traits. Females of the stalk-eyed fly Teleopsis dalmanni must mate frequently to maintain high levels of fertility and prefer to mate with males exhibiting large eyespan, a condition-dependent sexual ornament. If eyespan indicates male reproductive quality, females could directly increase their reproductive success by mating with males with large eyespan. Here we investigate whether male eyespan indicates accessory gland and testis length, and then ask whether mating with large eyespan males affects female fertility.     

The dynamic relationship between polyandry and selfish genetic elements

Selfish genetic elements (SGEs) are ubiquitous in eukaryotes and bacteria, and make up a large part of the genome. They frequently target sperm to increase their transmission success, but these manipulations are often associated with reduced male fertility. Low fertility of SGE-carrying males is suggested to promote polyandry as a female strategy to bias paternity against male carriers. Support for this hypothesis is found in several taxa, where SGE-carrying males have reduced sperm competitive ability. In contrast, when SGEs give rise to reproductive incompatibilities between SGE-carrying males and females, polyandry is not necessarily favoured, irrespective of the detrimental impact on male fertility. This is due to the frequency-dependent nature of these incompatibilities, because they will decrease in the population as the frequency of SGEs increases. However, reduced fertility of SGE-carrying males can prevent the successful population invasion of SGEs. In addition, SGEs can directly influence male and female mating behaviour, mating rates and reproductive traits (e.g. female reproductive tract length and male sperm). This reveals a potent and dynamic interaction between SGEs and polyandry highlighting the potential to generate sexual selection and conflict, but also indicates that polyandry can promote harmony within the genome by undermining the spread of SGEs.     

Sexual ornamentation reflects antibacterial activity of ejaculates in mallards

Bacteria present in ejaculates can impair sperm function and reduce male reproductive success. Thus, selection should favour the evolution of antimicrobial defences to limit the detrimental effects of sperm-associated bacteria. Additionally, current hypotheses suggest that ornamental traits may signal information about the infection status of an individual or the ability of an individual to resist bacterial-induced sperm damage. However, despite the evolutionary implications of ejaculate antimicrobials, and the putative importance of pathogens for the evolution of male ornamentation, tests of these hypotheses are lacking. We examined the antibacterial activity of semen from mallard ducks (Anas platyrhynchos) and tested whether the bactericidal capacity of semen was associated with bill coloration, a sexually selected trait. We show that mallard semen exhibits significant antibacterial activity, as measured by the in vitro capacity to kill Escherichia coli and Staphylococcus aureus. Furthermore, we demonstrate that males with more colourful bills have semen with superior bacterial-killing ability. These results suggest that females could use male phenotypic traits to avoid sexually transmitted pathogens and acquire partners whose sperm suffer less bacteria-induced damage.     

Wear Fast,Die Young: More Worn Teeth and Shorter Lives in Iberian Compared to Scottish Red Deer

Teeth in Cervidae are permanent structures that are not replaceable or repairable; consequently their rate of wear, due to the grinding effect of food and dental attrition, affects their duration and can determine an animal''s lifespan. Tooth wear is also a useful indicator of accumulative life energy investment in intake and mastication and their interactions with diet. Little is known regarding how natural and sexual selection operate on dental structures within a species in contrasting environments and how these relate to life history traits to explain differences in population rates of tooth wear and longevity. We hypothesised that populations under harsh environmental conditions should be selected for more hypsodont teeth while sexual selection may maintain similar sex differences within different populations. We investigated the patterns of tooth wear in males and females of Iberian red deer (Cervus elaphus hispanicus) in Southern Spain and Scottish red deer (C. e. scoticus) across Scotland, that occur in very different environments, using 10343 samples from legal hunting activities. We found higher rates of both incisor and molar wear in the Spanish compared to Scottish populations. However, Scottish red deer had larger incisors at emergence than Iberian red deer, whilst molars emerged at a similar size in both populations and sexes. Iberian and Scottish males had earlier tooth depletion than females, in support of a similar sexual selection process in both populations. However, whilst average lifespan for Iberian males was 4 years shorter than that for Iberian females and Scottish males, Scottish males only showed a reduction of 1 year in average lifespan with respect to Scottish females. More worn molars were associated with larger mandibles in both populations, suggesting that higher intake and/or greater investment in food comminution may have favoured increased body growth, before later loss of tooth efficiency due to severe wear. These results illustrate how independent selection in both subspecies, that diverged 11,700 years BP, has resulted in the evolution of different longevity, although sexual selection has maintained a similar pattern of relative sex differences in tooth depletion. This study opens interesting questions on optimal allocation in life history trade-offs and the independent evolution of allopatric populations.     

Developmental temperature affects the expression of ejaculatory traits and the outcome of sperm competition in Callosobruchus maculatus

The outcome of post‐copulatory sexual selection is determined by a complex set of interactions between the primary reproductive traits of two or more males and their interactions with the reproductive traits of the female. Recently, a number of studies have shown the primary reproductive traits of both males and females express phenotypic plasticity in response to the thermal environment experienced during ontogeny. However, how plasticity in these traits affects the dynamics of sperm competition remains largely unknown. Here, we demonstrate plasticity in testes size, sperm size and sperm number in response to developmental temperature in the bruchid beetle Callosobruchus maculatus. Males reared at the highest temperature eclosed at the smallest body size and had the smallest absolute and relative testes size. Males reared at both the high‐ and low‐temperature extremes produced both fewer and smaller sperm than males reared at intermediate temperatures. In the absence of sperm competition, developmental temperature had no effect on male fertility. However, under conditions of sperm competition, males reared at either temperature extreme were less competitive in terms of sperm offence (P₂), whereas those reared at the lowest temperature were less competitive in terms of sperm defence (P₁). This suggests the developmental pathways that regulate the phenotypic expression of these ejaculatory traits are subject to both natural and sexual selection: natural selection in the pre‐ejaculatory environment and sexual selection in the post‐ejaculatory environment. In nature, thermal heterogeneity during development is commonplace. Therefore, we suggest the interplay between ecology and development represents an important, yet hitherto underestimated component of male fitness via post‐copulatory sexual selection.     

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.     

Changes in sperm quality and numbers in response to experimental manipulation of male social status and female attractiveness

In promiscuous species, male reproductive success is determined by the interaction between the ability to access and choose females of the highest reproductive quality and, after copulation, the ability to outcompete the ejaculates of rival males. Disentangling the factors regulating the interplay between traits conferring a reproductive advantage before and after copulation is therefore crucial to understanding how sexual strategies evolve. Here we show in the fowl Gallus gallus, where social status determines copulation success, that dominant males produce more sperm than subordinates but that the quality of dominant males' sperm decreases over successive copulations, whereas that of subordinates remains constant. Experimentally manipulating male social status confirmed that ejaculate quality (the number and quality of sperm produced) was a response to the social environment rather than the result of intrinsic differences between dominant and subordinate males. We further show that dominant males responded to variation in female sexual ornamentation, which signals reproductive quality, by adjusting the number and quality of sperm they transferred, whereas subordinate males did not: they transferred ejaculates of similar quality to females with different ornament sizes. These results indicate that trade-offs between traits influencing reproductive success before and after copulation, combined with variation in social dynamics and female quality, may favor the evolution of phenotypically plastic alternative reproductive strategies.     

Team swimming in ant spermatozoa

In species where females mate promiscuously, competition between ejaculates from different males to fertilize the ova is an important selective force shaping many aspects of male reproductive traits, such as sperm number, sperm length and sperm–sperm interactions. In eusocial Hymenoptera (bees, wasps and ants), males die shortly after mating and their reproductive success is ultimately limited by the amount of sperm stored in the queen''s spermatheca. Multiple mating by queens is expected to impose intense selective pressure on males to optimize the transfer of sperm to the storage organ. Here, we report a remarkable case of cooperation between spermatozoa in the desert ant Cataglyphis savignyi. Males ejaculate bundles of 50–100 spermatozoa. Sperm bundles swim on average 51% faster than solitary sperm cells. Team swimming is expected to increase the amount of sperm stored in the queen spermatheca and, ultimately, enhance male posthumous fitness.     

Insecticide resistance enhances male reproductive success in a beetle

Abstract.— Malathion-specific resistance in the red flour beetle, Tribolium castaneum , is widespread and stable in natural populations even in the absence of pesticide exposure. To understand this stability, both resistant and susceptible males were placed in competition for susceptible female fertilization. Females were then isolated and their progeny was tested for malathion susceptibility. Male reproductive success was estimated for populations originating from different geographic areas and for isogenic strains. In most cases, resistant males had a greater reproductive success rate than susceptibles. The results suggest that male reproductive success is not traded against the selection for malathion resistance, even resistant individuals are at an advantage for this fitness trait. This absence of fitness cost may be the result of postselection of (1) modifier gene which ameliorate the fitness of resistant individuals or (2) nondeleterious resistance gene. Resistant phenotype superiority could be due to increased male mating success, improved ability of resistant males in sperm competition, female mate choice, and/or cryptic female choice of resistance gene(s). The effect of male phenotypic frequency on male reproductive success was also examined. We observed that male fertilization success is frequency dependent and inversely related to their frequency. However, this "rare male" advantage did not counteract the superiority of the resistant males.