Variation In Sperm Size Research Articles

Horn size is linked to Sertoli cell efficiency and sperm size homogeneity during sexual development in common eland (Taurotragus oryx).

Background: In polygynous species, the development of secondary sexual characters is usually decisive for male reproductive success. However, our understanding about the links between the growth of these traits and reproductive efficiency is still elusive. Most research efforts in this topic have been also focused on adult males, although the development of some secondary sexual characters, like bovid horns, typically starts after birth, continues during the puberty and in some species, such as the common eland, slows or even stops during adulthood. In this study, we investigated the relationships between horn size and testicular function during sexual development in common elands using a comprehensive approach that considers both spermatogenic and sperm parameters. Methods: Twenty-two non-sexually mature common elands were used for the present study. Horn size, body mass, testes mass, and gonadosomatic index were assessed. Spermatogenic activity was determined by cytological and histological analyses. Sperm concentration, morphology, morphometry, and intramale variation in sperm size were evaluated on epididymal sperm samples. Cluster analysis was performed to explore the influence of age on relationships between horn size and reproductive function. Results: We found that bigger horns are associated with increased Sertoli cell efficiency and reduced intramale variation in sperm size. Both parameters were not related to one another while they have shown to be associated with enhanced sperm quality in ungulates. Moreover, horn size was positively linked to the testis mass, sperm concentration, and testicular investment in the seminiferous epithelium. Spiral length and basal circumference were the horn traits most strongly correlated with spermatogenic and sperm parameters as well as those responsible for the sexual dimorphism in this species. Cluster analysis rendered two groups: the first one including males ≤30months old, while the second one those >30months old. Horn development and reproductive function were still correlated within age groups, with the strongest relationship found between horn size and sperm size homogeneity in males >30months old. Conclusion: Taken together, our results indicate that horn size can be regarded as a good index of male reproductive potential during sexual development and provide insights into the role of secondary sexual characters in sexual selection dynamics.

Variation of sperm size and evolution of giant spermatozoa in Lonchopteridae (Diptera)

Among species of the spear-winged flies (Lonchopteridae) there is remarkable variation in sperm size, with some species producing giant spermatozoa. With a length of 7500 μm and a width of 1.3 μm the spermatozoon of Lonchoptera fallax ranks among the largest known to date. In the present study body size, testis size, sperm size, and spermatid number per bundle and per testis were examined across 11 Lonchoptera species. Results are discussed in terms of how these characters are related with each other and how their evolution affects the resource allocation amongst spermatozoa. Based on some discrete morphological characters and a molecular tree derived from DNA barcodes a phylogenetic hypothesis of the genus Lonchoptera is proposed. The occurrence of giant spermatozoa in Lonchopteridae is compared to convergent occurrences reported in other taxa.

Age-related changes in sperm traits and evidence for aging costs of sperm production in a sexually promiscuous passerine

In many animal species, organismal performance declines with age in a process known as aging or senescence. Senescence typically leads to a deterioration of physiological functionality and can impact the development of primary sexual phenotypes. Sperm production is a complex and costly process that is sensitive to changes in individual physiological state, yet remarkably little is known about age-related changes in sperm performance and aging costs of sperm production. Here we use a non-linear generalized additive mixed models (GAMM) modelling to evaluate age-related changes in postcopulatory sexual traits in the European barn swallow (Hirundo rustica rustica), a relatively short lived sexually promiscuous passerine species, where male extra-pair fertilization success has been shown to increase with age. We confirmed a positive relationship between sperm midpiece length and sperm velocity in this species. Within-male changes in sperm morphology and sperm velocity were in general absent, with only sperm length decreasing linearly with increasing age, although this change was negligible compared to the overall variation in sperm size among males. In contrast, the cloacal protuberance (CP) size changed nonlinearly with age, with an initial increase between the first and third year of life followed by a plateau. The results further indicate the existence of a trade-off between investments in sperm production and survival as males with large CP tended to have a reduced lifespan. This seems consistent with the idea of expensive sperm production and survival aging costs associated with investments in post-copulatory traits in this sexually promiscuous species.

Selection on sperm size in response to promiscuity and variation in female sperm storage organs.

Sperm cells are exceptionally morphologically diverse across taxa. However, morphology can be quite uniform within species, particularly for species where females copulate with many males per reproductive bout. Strong sexual selection in these promiscuous species is widely hypothesized to reduce intraspecific sperm variation. Conversely, we hypothesize that intraspecific sperm size variation may be maintained by high among-female variation in the size of sperm storage organs, assuming that paternity success improves when sperm are compatible in size with the sperm storage organ. We use individual-based simulations and an analytical model to evaluate how selection on sperm size depends on promiscuity level and variation in sperm storage organ size (hereafter, female preference variation). Simulations of high promiscuity (10 mates per female) showed stabilizing selection on sperm when female preference variation was low, and disruptive selection when female preference variation was high, consistent with the analytical model results. With low promiscuity (2-3 mates per female), selection on sperm was stabilizing for all levels of female preference variation in the simulations, contrasting with the analytical model. Promiscuity level, or mate sampling, thus has a strong impact on the selection resulting from female preferences. Furthermore, when promiscuity is low, disruptive selection on male traits will occur under much more limited circumstances (i.e. only with higher among-female variation) than many previous models suggest. Variation in female sperm storage organs likely has strong implications for intraspecific sperm variation in highly promiscuous species, but likely does not explain differences in intraspecific sperm variation for less promiscuous taxa.

Natural Variation and Genetic Determinants of Caenorhabditis elegans Sperm Size.

The diversity in sperm shape and size represents a powerful paradigm to understand how selection drives the evolutionary diversification of cell morphology. Experimental work on the sperm biology of the male-hermaphrodite nematode Caenorhabditis elegans has elucidated diverse factors important for sperm fertilization success, including the competitive superiority of larger sperm. Yet despite extensive research, the molecular mechanisms regulating C. elegans sperm size and the genetic basis underlying natural variation in sperm size remain unknown. To address these questions, we quantified male sperm size variation of a worldwide panel of 97 genetically distinct C. elegans strains, allowing us to uncover significant genetic variation in male sperm size. Aiming to characterize the molecular genetic basis of C. elegans male sperm size variation using a genome-wide association study, we did not detect any significant quantitative trait loci. We therefore focused on the genetic analysis of pronounced sperm size differences observed between recently diverged laboratory strains (N2 vs. LSJ1/2). Using mutants and quantitative complementation tests, we demonstrate that variation in the gene nurf-1 underlies the evolution of small sperm in the LSJ lineage. Given the previous discovery that this same nurf-1 variation was central for hermaphrodite laboratory adaptation, the evolution of reduced male sperm size in LSJ strains likely reflects a pleiotropic consequence. Together, our results provide a comprehensive quantification of natural variation in C. elegans sperm size and first insights into the genetic determinants of Caenorhabditis sperm size, pointing at an involvement of the NURF chromatin remodeling complex.

Convergent evolution of sperm gigantism and the developmental origins of sperm size variability in Caenorhabditis nematodes.

Sperm cells provide essential, if usually diminutive, ingredients to successful sexual reproduction. Despite this conserved function, sperm competition and coevolution with female traits can drive spectacular morphological change in these cells. Here, we characterize four repeated instances of convergent evolution of sperm gigantism in Caenorhabditis nematodes using phylogenetic comparative methods on 26 species. Species at the extreme end of the 50-fold range of sperm-cell volumes across the genus have sperm capable of comprising up to 5% of egg-cell volume, representing severe attenuation of the magnitude of anisogamy. Furthermore, we uncover significant differences in mean and variance of sperm size among genotypes, between sexes, and within and between individuals of identical genotypes. We demonstrate that the developmental basis of sperm size variation, both within and between species, becomes established during an early stage of sperm development at the formation of primary spermatocytes, while subsequent meiotic divisions contribute little further sperm size variability. These findings provide first insights into the developmental determinants of inter- and intraspecific sperm size differences in Caenorhabditis. We hypothesize that life history and ecological differences among species favored the evolution of alternative sperm competition strategies toward either many smaller sperm or fewer larger sperm.

Extensive variation in sperm morphology in a frog with no sperm competition.

BackgroundRecent comparative studies of several taxa have found that within-species variation in sperm size decreases with increasing levels of sperm competition, suggesting that male-male gamete competition selects for an optimal sperm phenotype. Previous studies of intraspecific sperm length variation have all involved internal fertilizers where some other factors—e.g., sperm storage and sperm movement along the walls of the female’s reproductive tract—probably also influence and reduce sperm size variation. Thus external fertilizers, where those factors are absent, might be expected to exhibit even more variation when there is little or no sperm competition. To test that idea, we studied the sperm morphology of a North American chorus frog, the spring peeper (Pseudacris crucifer), a species in which males encounter little or no sperm competition.ResultsAs expected, sperm size was highly variable in the spring peeper, largely due to variation in flagellum length within and among individual males, among populations and between mitochondrial lineages in southwestern Ontario. In addition, a large proportion of spermatozoa in all males was abnormal in such a way that the ability of abnormal spermatozoa to fertilize was probably compromised. There were no differences in the frequencies of abnormalities among populations or mitochondrial lineages.ConclusionsIn the absence of sperm competition, we suggest that genetic drift has probably played a role in the generation of diversity in sperm morphology in this species, potentially resulting in the observed differences among populations. Such interpopulation difference in sperm morphology might be expected to increase the degree of reproductive isolation between populations even before other isolating mechanisms evolve.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0601-8) contains supplementary material, which is available to authorized users.

Variation in sperm morphology among Afrotropical sunbirds

Birds show considerable variation in sperm morphology. Closely related species and subspecies can show diagnostic differences in sperm size. There is also variation in sperm size among males within a population, and recent evidence from passerine birds suggests that the coefficient of inter‐male variation in sperm length is negatively associated with the level of sperm competition. Here we examined patterns of inter‐ and intra‐specific variation in sperm length in 12 species of sunbird (Nectariniidae) from Nigeria and Cameroon, a group for which such information is extremely limited. We found significant variation among species in sperm total length, with mean values ranging from 74 μm to 116 μm, placing these species within the short to medium sperm length range for passerine birds. Most of this variation was explained by the length of the midpiece, which contains the fused mitochondria and is an important structure for sperm energetics. Relative midpiece length was negatively correlated with the coefficient of inter‐male variation in sperm total length across species, suggesting that sperm competition may have selected for greater midpiece length in this group. We also mapped sperm lengths onto a time‐calibrated phylogeny and found support for a phylogenetic signal in all sperm length components, except head length. A test of various evolutionary or tree transformation models gave strongest support for the Brownian motion model for all sperm components, i.e. divergences were best predicted by the phylogenetic distance between lineages. The coefficients of inter‐male variation in sperm total length indicate that sperm competition is high but variable among sunbird species, as is the case with passerine birds at large.

Intramale variation in sperm size: functional significance in a polygynous mammal.

Studies concerning the relationships between sperm size and velocity at the intraspecific level are quite limited and often yielded contradictory results across the animal kingdom. Intramale variation in sperm size may represent a meaningful factor to predict sperm velocity, due to its relationship with the level of sperm competition among related taxa. Because sperm phenotype is under post-copulatory sexual selection, we hypothesized that a reduced intramale variation in sperm size is associated with sperm competitiveness in red deer. Our results show that low variation in sperm size is strongly related to high sperm velocity and normal sperm morphology, which in turn are good predictors of male fertility in this species. Furthermore, it is well known that the red deer show high variability in testicular mass but there is limited knowledge concerning the significance of this phenomenon at intraspecific level, even though it may reveal interesting processes of sexual selection. Thereby, as a preliminary result, we found that absolute testes mass is negatively associated with intramale variation in sperm size. Our findings suggest that sperm size variation in red deer is under a strong selective force leading to increase sperm function efficiency, and reveal new insights into sexual selection mechanisms.

Sperm size evolution in African greenbuls (Passeriformes: Pycnonotidae)

Sperm morphology is highly diversified across the animal kingdom and recent comparative evidence from passerine birds suggests that postcopulatory sexual selection is a significant driver of sperm evolution. In the present study, we describe sperm size variation among 20 species of African greenbuls and one bulbul (Passeriformes: Pycnonotidae) and analyze the evolutionary differentiation of sperm size within a phylogenetic framework. We found significant interspecific variation in sperm size; with some genera exhibiting relatively long sperm (e.g. Eurillas) and others exhibiting short sperm head lengths (e.g. Phyllastrephus). However, our results suggest that contemporary levels of sperm competition are unlikely to explain sperm diversification within this clade: the coefficients of inter-male variation (CVbm) in sperm length were generally high, suggesting relatively low and homogeneous rates of extra-pair paternity. Finally, in a comparison of six evolutionary or tree transformation models, we found support for both the Kappa (evolutionary change primarily at nodes) and Lambda (lineage-specific evolutionary rates along branches) models in the evolutionary trajectories of sperm size among species. We therefore conclude that African greenbuls have more variable rates of sperm size evolution than expected from a neutral model of genetic drift. Understanding the evolutionary dynamics of sperm diversification remains a future challenge.

Variability in sperm form and function in the context of sperm competition risk in two Tupinambis lizards.

In polyandrous species, sperm morphometry and sperm velocity are under strong sexual selection. Although several hypotheses have been proposed to explain the role of sperm competition in sperm trait variation, this aspect is still poorly understood. It has been suggested that an increase in sperm competition pressure could reduce sperm size variation or produce a diversity of sperm to maximize male fertilization success. We aim at elucidating the variability of sperm morphometric traits and velocity in two Tupinambis lizards in the context of sperm competition risk. Sperm traits showed substantial variation at all levels examined: between species, among males within species, and within the ejaculate of individual males. Sperm velocity was found to be positively correlated with flagellum: midpiece ratio, with relatively longer flagella associated with faster sperm. Our results document high variability in sperm form and function in lizards.

Postcopulatory sexual selection results in spermatozoa with more uniform head and flagellum sizes in rodents.

Interspecific comparative studies have shown that, in most taxa, postcopulatory sexual selection (PCSS) in the form of sperm competition drives the evolution of longer and faster swimming sperm. Work on passserine birds has revealed that PCSS also reduces variation in sperm size between males at the intraspecific level. However, the influence of PCSS upon intra-male sperm size diversity is poorly understood, since the few studies carried out to date in birds have yielded contradictory results. In mammals, PCSS increases sperm size but there is little information on the effects of this selective force on variations in sperm size and shape. Here, we test whether sperm competition associates with a reduction in the degree of variation of sperm dimensions in rodents. We found that as sperm competition levels increase males produce sperm that are more similar in both the size of the head and the size of the flagellum. On the other hand, whereas with increasing levels of sperm competition there is less variation in head length in relation to head width (ratio CV head length/CV head width), there is no relation between variation in head and flagellum sizes (ratio CV head length/CV flagellum length). Thus, it appears that, in addition to a selection for longer sperm, sperm competition may select more uniform sperm heads and flagella, which together may enhance swimming velocity. Overall, sperm competition seems to drive sperm components towards an optimum design that may affect sperm performance which, in turn, will be crucial for successful fertilization.

Patterns of sperm damage in Chernobyl passerine birds suggest a trade-off between sperm length and integrity

Interspecific variation in sperm size is enigmatic, but generally assumed to reflect species-specific trade-offs in selection pressures. Among passerine birds, sperm length varies sevenfold, and sperm competition risk seems to drive the evolution of longer sperm. However, little is known about factors favouring short sperm or constraining the evolution of longer sperm. Here, we report a comparative analysis of sperm head abnormalities among 11 species of passerine bird in Chernobyl, presumably resulting from chronic irradiation following the 1986 accident. Frequencies of sperm abnormalities varied between 15.7 and 77.3% among species, more than fourfold higher than in uncontaminated areas. Nonetheless, species ranked similarly in sperm abnormalities in unpolluted areas as in Chernobyl, pointing to intrinsic factors underlying variation in sperm damage among species. Scanning electron microscopy of abnormal spermatozoa revealed patterns of acrosome damage consistent with premature acrosome reaction. Sperm length, but not sperm competition risk explained variation in sperm damage among species. This suggests that longer spermatozoa are more susceptible to premature acrosome reaction. Therefore, we hypothesize a trade-off between sperm length and sperm integrity affecting sperm evolution in passerine birds.

No association between sperm competition and sperm length variation across dung flies (Scathophagidae)

Sperm length is extremely variable across species, but a general explanation for this variation is lacking. However, when the risk of sperm competition is high, sperm length is predicted to be less variable within species, and there is some evidence for this in birds and social insects. Here, we examined intraspecific variation in sperm length, both within and between males, and its potential associations with sperm competition risk and variation in female reproductive tract morphology across dung flies. We used two measures of variation in sperm size, and testis size was employed as our index of sperm competition risk. We found no evidence of associations between sperm length variation and sperm competition or female reproductive tract variation. These results suggest that variation in sperm competition risk may not always be associated with variation in sperm morphology, and the cause(s) of sperm length variation in dung flies remains unclear.

Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations

Spermatozoa vary greatly in size and shape among species across the animal kingdom. Postcopulatory sexual selection is thought to be the major evolutionary force driving this diversity. In contrast, less is known about how sperm size varies among populations of the same species. Here, we investigate geographic variation in sperm size in barn swallows Hirundo rustica, a socially monogamous passerine with a wide Holarctic breeding distribution. We included samples from seven populations and three subspecies: five populations of ssp. rustica in Europe (Czech, Italy, Norway, Spain, and Ukraine), one population of ssp. transitiva in Israel, and one population of ssp. erythrogaster in Canada. All sperm traits (head length, midpiece length, tail length, and total length) varied significantly among populations. The variation among the European rustica populations was much lower than the differences among subspecies, indicating that sperm traits reflect phylogenetic distance. We also performed a test of the relationship between the coefficient of between-male variation in total sperm length and extrapair paternity levels across different populations within a species. Recent studies have found a strong negative relationship between sperm size variation and extrapair paternity among species. Here, we show a similar negative relationship among six barn swallow populations, which suggests that the variance in male sperm length in a population is shaped by the strength of stabilizing postcopulatory sexual selection.

Mass-Specific Metabolic Rate and Sperm Competition Determine Sperm Size in Marsupial Mammals

Two complementary hypotheses have been proposed to explain variation in sperm size. The first proposes that post-copulatory sexual selection favors an increase in sperm size because it enhances sperm swimming speed, which is an important determinant of fertilization success in competitive contexts. The second hypothesis proposes that mass-specific metabolic rate acts as a constraint, because large animals with low mass-specific metabolic rates will not be able to process resources at the rates needed to produce large sperm. This constraint is expected to be particularly pronounced among mammals, given that this group contains some of the largest species on Earth. We tested these hypotheses among marsupials, a group in which mass-specific metabolic rates are roughly 30% lower than those of eutherian mammals of similar size, leading to the expectation that metabolic rate should be a major constraint. Our findings support both hypotheses because levels of sperm competition are associated with increases in sperm size, but low mass-specific metabolic rate constrains sperm size among large species. We also found that the relationship between sperm size and mass-specific metabolic rate is steeper among marsupials and shallower among eutherian mammals. This finding has two implications: marsupials respond to changes in mass-specific metabolic rate by modifying sperm length to a greater extent, suggesting that they are more constrained by metabolic rate. In addition, for any given mass-specific metabolic rate, marsupials produce longer sperm. We suggest that this is the consequence of marsupials diverting resources away from sperm numbers and into sperm size, due to their efficient sperm transport along the female tract and the existence of mechanisms to protect sperm.

Resolving variation in the reproductive tradeoff between sperm size and number

Spermatozoa are amongst the most variable cells, and three factors are thought to account for this variation in design: fertilization mode, phylogeny, and postcopulatory sexual selection. In addition, it has long been assumed that a tradeoff exists between sperm size and number, and although postcopulatory sexual selection affects both traits, empirical evidence for a tradeoff has so far been elusive. Our recent theoretical model predicts that the nature of a direct tradeoff between sperm size and number varies with sperm competition mechanism and sperm competition risk. We test these predictions using a comparative approach in two very different taxa with different sperm competition mechanisms: passerine birds (mechanism: simple raffle) and Drosophila fruit flies (sperm displacement). We show that in both groups, males increase their total ejaculate investment with increasing sperm competition risk, but whereas passerine birds allocate disproportionately to sperm number, drosophilids allocate disproportionately to sperm size. This striking difference between the two groups can be at least partly explained by sperm competition mechanisms depending on sperm size relative to the size of the female reproductive tract: in large animals (passerines), sperm numbers are advantageous in sperm competition owing to dilution inside the female tract, whereas in small animals (drosophilids), large sperm are advantageous for physical competition (sperm displacement). Our study provides two important results. First, we provide convincing evidence for the existence of a sperm size-number tradeoff. Second, we show that by considering both sperm competition mechanism and dilution, can we account for variation in sperm size between different taxa.

Repeatability of sperm size in outbred and inbred Scathophaga stercoraria (Diptera: Scathophagidae)

AbstractVariability in male gametic traits can depend on several genetic and environmental factors such as developmental instability as a consequence of inbreeding, developmental noise during spermatogenesis, or age- or condition-dependent changes in allocation to sperm cells. Variation in sperm size is particularly evident in species that produce more than one sperm morph but also occurs among males in sperm-monomorphic species. Both discrete and continuous sperm size variation have been implicated in male fertilization success when the sperm of several males directly compete for fertilization of the same set of ova. In this study, we investigated among-male variation in sperm length in field-collected, outbred male Scathophaga stercoraria (L.) flies, as well as in flies from the same natural population that had been subjected to 15 and 16 generations of inbreeding under laboratory conditions. Among-male variation in sperm length was significant and repeatable over subsequent matings in both inbred and outbred flies. We conclude that sperm length can be used as an individual male marker in sperm competition studies and that significant repeatability of sperm length supports heritability for this trait.

Variation in sperm size within and between ejaculates in a cockroach

Summary Interspecific diversity in the morphology of animal sperm suggests adaptive evolutionary changes in size and structure. Little attention has been directed at patterns of intraspecific phenotypic variation in sperm morphology, although such variation is a prerequisite for the extreme diversity seen among male gametes. Despite well‐developed sperm competition theory providing a basis for exploring how variation in sperm morphology may affect male fitness, the patterns of variation in sperm morphology remain unclear for most species. We report systematic size variation in sperm length among different males and between successive ejaculates within the same male in the cockroach Nauphoeta cinerea. Both flagellum length and mid‐piece length decreased between the first and second ejaculate. However, within the same ejaculate the sperm head (acrosome and nucleus), midpiece (centriole adjunct region) and tail length exhibited less variation than that present between males for both first and second ejaculates. Our findings, combined with previous studies, suggest a focus on episodes of selection and lifetime selection on ejaculates may be instructive in understanding the selective forces influencing sperm evolution in a predictive framework.

Extraordinarily long sperm in the socially monogamous cichlid fish Pelvicachromis taeniatus

The main function of the spermatozoon is the transfer of the male haploid genome during fertilisation. In animals in general and in fishes in particular, there is huge variation in sperm size. In fishes, sperm size ranges from 13 microm in Mugil cephlus to nearly 100 microm in the channel catfish Ictalurus punctatus. We examined intra-specific variation in sperm morphometry in the socially monogamous cichlid Pelvicachromis taeniatus using scanning electron microscopy. The mean total sperm length of nearly 70 microm was extraordinarily large for cichlids. Furthermore, within-male variation was remarkably high. To our knowledge, P. taeniatus produces the longest cichlid sperm ever documented. Several hypotheses concerning the adaptive significance of these results are presented.