Variation In Sperm Length Research Articles

Extra-pair paternity and sperm length variation in a far northern Great Tit (Parus major) population

Extra-pair paternity and sperm length variation in a far northern Great Tit (Parus major) population

Tetrapod sperm length evolution in relation to body mass is shaped by multiple trade-offs

Sperm length is highly variable across species and many questions about its variation remain open. Although variation in body mass may affect sperm length evolution through its influence on multiple factors, the extent to which sperm length variation is linked to body mass remains elusive. Here, we use the Pareto multi-task evolution framework to investigate the relationship between sperm length and body mass across tetrapods. We find that tetrapods occupy a triangular Pareto front, indicating that trade-offs shape the evolution of sperm length in relation to body mass. By exploring the factors predicted to influence sperm length evolution, we find that sperm length evolution is mainly driven by sperm competition and clutch size, rather than by genome size. Moreover, the triangular Pareto front is maintained within endotherms, internal fertilizers, mammals and birds, suggesting similar evolutionary trade-offs within tetrapods. Finally, we demonstrate that the Pareto front is robust to phylogenetic dependencies and finite sampling bias. Our findings provide insights into the evolutionary mechanisms driving interspecific sperm length variation and highlight the importance of considering multiple trade-offs in optimizing reproductive traits.

A clear-cut difference in nuptial strategies may shape sperm traits in two paper wasps

Abstract Spermatozoa vary in quantity, quality and design across species and individuals. Here, we reported the first detailed analysis of sperm traits in two primitively eusocial paper wasps, Polistes dominula and Polistes gallicus, which differ in their nuptial strategies and body size as follows: lek-territoriality of the large P. dominula males, defending exclusive territories at landmarks; scramble competition of the small P. gallicus, where serial mating may occur because males interfere with rivals and replace them during copulation. We compared the number, viability, and length of sperm, and its coefficient of variation, between these sympatric paper wasps patrolling and marking the same landmarks during the same summer: a good opportunity to analyse sperm across species while controlling for environmental variables. Spermatozoa were more numerous and longer in P. dominula than in P. gallicus males. Viability was similar in both species and positively covaried with male body size. Intra-male variation in sperm length was significantly reduced in P. gallicus, as predicted in the case of selection for an optimal sperm design. We hypothesized that precopulatory sexual selection (lek-territoriality vs. scramble competition) may affect sperm traits.

Reproductive context of extremely short sperm in the parasitic waspCotesia congregata(Hymenoptera: Braconidae)

AbstractAmong adaptive traits under sexual selection, the length of spermatozoa shows high interspecific variation. In insects, extremes exist for both short and long sperm. The spermatozoa of the endoparasitic wasp Cotesia congregata (Say) are the shortest flagellated sperm described in animals, 6.6 µm in length. By comparison, the sperm of Drosophila bifurca are almost 6000 times longer. Thus, C. congregata has the potential to shed light on the selection pressures that drive variation in sperm length in relation to their production and use. The reproductive organs, sperm counts, controlled oviposition and sex ratios were investigated. The testes showed stratified differentiation stages of spermatogenesis, and sperm counts revealed continuous spermatogenesis in the late pupal stage. The small female spermatheca stored ~1000 sperm, resulting in an extremely high sperm concentration. The number of progeny per brood decreased over time until depletion of eggs. Females produced up to 370 daughters, corresponding to the effective use of 34% of the average sperm stock. Haploid males made up a greater proportion of broods in later parasitisms. Sperm miniaturization may be an adaptation to transfer increased quantities for the entire reproductive life of females in the absence of sperm competition but in the reduced space offered by the spermatheca.

Sperm length variation among Afrotropical songbirds reflects phylogeny rather than adaptations to the tropical environment

Sperm cells vary tremendously in size and shape across the animal kingdom. In songbirds (Aves: Passeri), sperm have a characteristic helical form but vary considerably in size. Most of our knowledge about sperm morphology in this group stems from studies of species in the Northern temperate zone, while little is known about the numerous species in the tropics. Here we examined sperm size in 125 Afrotropical songbird species with emphasis on the length of the major structural components (head, midpiece, flagellum), and total sperm length measured using light microscopy. Mean total sperm length varied from 51 μm to 212 μm across species. Those belonging to the Corvoidea superfamily had relatively short sperm with a small midpiece, while those of the three major Passeridan superfamilies Passeroidea, Muscicapoidea and Sylvioidea showed large interspecific variation in total sperm length and associated variation in midpiece length. These patterns are consistent with previous findings for temperate species in the same major clades. A comparative analysis with songbird species from the Northern temperate zone (N = 139) showed large overlap in sperm length ranges although certain temperate families (e.g. Parulidae, Emberizidae) typically have long sperm and certain Afrotropical families (e.g. Cisticolidae, Estrildidae) have relatively short sperm. Afrotropical and temperate species belonging to the same families showed no consistent contrasts in sperm length. Sperm length variation among Afrotropical and Northern temperate songbirds exhibits a strong phylogenetic signal with little or no evidence for any directional latitudinal effect among closely related taxa.

Sperm morphology and evidence for sperm competition among parrots.

Sperm competition is an important component of post‐copulatory sexual selection that has shaped the evolution of sperm morphology. Previous studies have reported that sperm competition has a concurrently directional and stabilizing effect on sperm size. For example, bird species that show higher levels of extrapair paternity and larger testes (proxies for the intensity of sperm competition) have longer sperm and lower coefficients of variation in sperm length, both within and between males. For this reason, these sperm traits have been proposed as indexes to estimate the level of sperm competition in species for which other measures are not available. The relationship between sperm competition and sperm morphology has been explored mostly for bird species that breed in temperate zones, with the main focus on passerine birds. We measured sperm morphology in 62 parrot species that breed mainly in the tropics and related variation in sperm length to life‐history traits potentially indicative of the level of sperm competition. We showed that sperm length negatively correlated with the within‐male coefficient of variation in sperm length and positively with testes mass. We also showed that sperm is longer in sexually dichromatic and in gregarious species. Our results support the general validity of the hypothesis that sperm competition drives variation in sperm morphology. Our analyses suggest that post‐copulatory sexual selection is also important in tropical species, with more intense sperm competition among sexually dichromatic species and among species that breed at higher densities.

Postcopulatory sexual selection reduces Z-linked genetic variation and might contribute to the large Z effect in passerine birds.

The X and Z sex chromosomes play a disproportionately large role in intrinsic postzygotic isolation. The underlying mechanisms of this large X/Z effect are, however, still poorly understood. Here we tested whether faster rates of molecular evolution caused by more intense positive selection or genetic drift on the Z chromosome could contribute to the large Z effect in two closely related passerine birds, the Common Nightingale (Luscinia megarhynchos) and the Thrush Nightingale (L. luscinia). We found that the two species differ in patterns of molecular evolution on the Z chromosome. The Z chromosome of L. megarhynchos showed lower levels of within-species polymorphism and an excess of non-synonymous polymorphisms relative to non-synonymous substitutions. This is consistent with increased levels of genetic drift on this chromosome and may be attributed to more intense postcopulatory sexual selection acting on L. megarhynchos males as was indicated by significantly longer sperm and higher between-male variation in sperm length in L. megarhynchos compared to L. luscinia. Interestingly, analysis of interspecific gene flow on the Z chromosome revealed relatively lower levels of introgression from L. megarhynchos to L. luscinia than vice versa, indicating that the Z chromosome of L. megarhynchos accumulated more hybrid incompatibilities. Our results are consistent with the view that postcopulatory sexual selection may reduce the effective population size of the Z chromosome and thus lead to stronger genetic drift on this chromosome in birds. This can result in relatively faster accumulation of hybrid incompatibilities on the Z and thus contribute to the large Z effect.

Altitudinal variation in somatic condition and reproductive investment of male Yunnan pond frogs (Dianrana pleuraden)

Comparisons between populations that differ in resource availability and in environmental variables affecting the intensity of male–male competition allow insights into the mechanisms shaping reproductive allocation. Here, we studied inter-population variation in male investments in testis size and sperm length across four populations of the Yunnan pond frog (Dianrana pleuraden) along an altitudinal gradient in western China. Male body condition, relative testis size and sperm length did not increase with altitude despite an increasing male bias in the operational sex ratio (OSR) in high altitude was recorded. Our results were inconsistent with previous prediction that increasing latitude and/or altitude should lead to a declining male reproductive investment in anurans due to shortening breeding seasons and declining resource availability. We found a positive correlation between body condition and testes mass along the altitudinal gradient, which was indicative of a condition-dependent expression of testis size. By contrast, we recorded a non-significant correlation between testes mass and OSR, suggesting that male–male competition did not result in increasing levels of sperm competition. A non-significant correlation between sperm length and testis mass suggested that the intensity of sperm competition can account for the variation in sperm length.

Competitive males have higher quality sperm in a monogamous social bee.

BackgroundReproductive success is determined by the interplay between mating and fertilization success. In social insect species with male-biased sex ratios and queen monogamy, males face particularly strong pre-copulatory sexual selection since they must compete with thousands of other males for a unique mating opportunity. Ejaculate quality is also expected to be under selection, because queens are long-lived and store sperm for life, so males with higher quality ejaculates are expected to provide queens with larger and longer-lived colonies, which in turn may produce more daughter queens (the only direct fitness gains of haplodiploid males). Considering the action of pre and post-copulatory sexual selection on male traits, three scenarios might thus be expected: positive, negative or no association between male mating ability and fertilization success. Here we explored these scenarios in the stingless bee Scaptotrigona aff. depilis, where males gather in large aggregations and queens mate with a single male. Male mating ability was assessed through the capacity of a male to reach an aggregation and persist on it; while sperm viability, sperm number, and sperm morphology were used as proxies for sperm quality.ResultsSperm viability was associated with persistence time in the aggregation, and males that persisted longer presented shorter spermatozoa and higher variation in sperm length than recently arrived males. However, sperm traits of males that reached aggregations did not differ from those of males collected inside their colonies. In addition, males that persisted longer in aggregations were smaller than other males. Male size and sperm viability were not correlated, suggesting that the observed patterns were not due to trade-offs in male resource allocation.ConclusionsPersistence in male aggregations thus seems to select more competitive males with higher quality sperm. Our work is the first one to reveal an association between male competitive ability and fertilization success in a monogamous social insect. This finding sheds important light on the evolution of male traits in social insects and the general mechanisms of sexual selection.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0765-2) contains supplementary material, which is available to authorized users.

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.

Parasitic mites influence intra- and interpopulational variation in sperm length in a simultaneous hermaphrodite land snail (Gastropoda: Helicidae)

Sperm morphology can be highly variable among species, but less is known about patterns of population differentiation within species. Sperm morphology is under strong sexual selection, may evolve rapidly, and often co-varies with other reproductive traits that differ between populations. We investigated variation in sperm morphology in the simultaneous hermaphrodite land snail Arianta arbustorum in relation to parasitic mite infection. Variation in total sperm length and sperm head length was assessed in 23 populations sampled across the distributional range of the species in Central and Northern Europe. We found a pronounced variation in total sperm length among the populations studied, with a difference of 11.0% of total sperm length between the shortest and longest population means. Differences among populations explained 62.9% of the variance in total sperm length, differences among individual snails within population 23.4% and differences within individual snail 13.7%. Mantel tests showed that interpopulation differences in total sperm length increased significantly with geographical distance between populations. A minimal adequate model revealed that parasitic infection had a positive effect and longitude a negative effect on total sperm length. Thus, independent of the population examined, mite-infected individuals of A. arbustorum produced larger sperm than uninfected snails and total sperm length decreased from west to east. Sperm head length also varied among populations, but it was not influenced by any of the factors examined. In a subsample of 12 populations restricted to the mountains of Switzerland (elevational range 440–2485 m a.s.l.), total sperm length decreased with increasing elevation. Our results suggest that selection pressures acting among populations may differ from those acting within. Stabilizing selection might be a possible mechanism for producing the reduced variation observed in sperm length within a population. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 1036–1046.

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.

Sperm length variation in House Wrens Troglodytes aedon

It is well documented that sperm size and structure varies considerably among avian species, but we know much less about the extent of intraspecific variation in sperm morphometry and its possible co-variation with somatic traits like body size and condition. Here, we investigate patterns of sperm length variation and co-variation in a population of House Wrens (Troglodytes aedon). Total sperm length showed considerable between-male variation, with high repeatability between seasons indicative of a strong genetic basis for this trait. However, we also detected a seasonal increase in the flagellum:head length ratio, which might indicate phenotypic plasticity or adjustment in the relative size of sperm components. The variation in total sperm length within an ejaculate sample was higher for males sampled very early in the season, which may reflect more heterogeneity in the size of seminiferous tubules when testes are growing. None of the studied sperm morphometry traits correlated significantly with any measures of male body size or physiological condition. Further studies are needed to reveal if the observed individual variation in sperm morphology plays any functional or adaptive role.

No Evidence for Pre-Copulatory Sexual Selection on Sperm Length in a Passerine Bird

There is growing evidence that post-copulatory sexual selection, mediated by sperm competition, influences the evolution of sperm phenotypes. Evidence for pre-copulatory sexual selection effects on sperm traits, on the other hand, is rather scarce. A recent paper on the pied flycatcher, Ficedula hypoleuca, reported phenotypic associations between sperm length and two sexually selected male traits, i.e. plumage colour and arrival date, thus invoking pre-copulatory sexual selection for longer sperm. We were unable to replicate these associations with a larger data set from the same and two additional study populations; sperm length was not significantly related to either male plumage colour or arrival date. Furthermore, there was no significant difference in sperm length between populations despite marked differences in male plumage colour. We also found some evidence against the previously held assumption of longer sperm being qualitatively superior; longer sperm swam at the same speed as shorter sperm, but were less able to maintain speed over time. We argue that both empirical evidence and theoretical considerations suggest that the evolution of sperm morphology is not primarily associated with pre-copulatory sexual selection on male secondary sexual traits in this or other passerine bird species. The relatively large between-male variation in sperm length in this species is probably due to relaxed post-copulatory sexual selection.

Sperm competition leads to functional adaptations in avian testes to maximize sperm quantity and quality

The outcome of sperm competition (i.e. competition for fertilization between ejaculates from different males) is primarily determined by the relative number and quality of rival sperm. Therefore, the testes are under strong selection to maximize both sperm number and quality, which are likely to result in trade-offs in the process of spermatogenesis (e.g. between the rate of spermatogenesis and sperm length or sperm energetics). Comparative studies have shown positive associations between the level of sperm competition and both relative testis size and the proportion of seminiferous (sperm-producing) tissue within the testes. However, it is unknown how the seminiferous tissue itself or the process of spermatogenesis might evolve in response to sperm competition. Therefore, we quantified the different germ cell types and Sertoli cells (SC) in testes to assess the efficiency of sperm production and its associations with sperm length and mating system across 10 species of New World Blackbirds (Icteridae) that show marked variation in sperm length and sperm competition level. We found that species under strong sperm competition generate more round spermatids (RS)/spermatogonium and have SC that support a greater number of germ cells, both of which are likely to increase the maximum sperm output. However, fewer of the RS appeared to elongate to mature spermatozoa in these species, which might be the result of selection for discarding spermatids with undesirable characteristics as they develop. Our results suggest that, in addition to overall size and gross morphology, testes have also evolved functional adaptations to maximize sperm quantity and quality.

Sperm dimensions differ between two Coal Tit Periparus ater populations

The evolutionary forces that shape and maintain variation in sperm traits across species in birds have recently attracted increased attention. Much less is known about the patterns, the causes and the consequences of variation in sperm traits within and, in particular, between populations of the same species. We here analyse intraspecific variation in sperm dimensions within and between two populations of the Coal Tit Periparus ater, a socially monogamous passerine with a high frequency of extra-pair paternity. Spermatozoa from a Norwegian population had a greater mean total length compared to those from a German population, mainly as a result of longer sperm heads. Sperm head length in the Norwegian population also accounted for a larger percentage of sperm total length suggesting differences in sperm proportions between populations. Furthermore, spermatozoa from the Norwegian population showed lower mean within-male variation in sperm length and there was significant between-male variation in sperm total length within each of the two populations. We discuss these results in the light of recent comparative evidence suggesting relationships between sperm length, and variation in sperm length, and the frequency of extra-pair paternity across passerine birds.

Sperm Length Variation as a Predictor of Extrapair Paternity in Passerine Birds

BackgroundThe rate of extrapair paternity is a commonly used index for the risk of sperm competition in birds, but paternity data exist for only a few percent of the approximately 10400 extant species. As paternity analyses require extensive field sampling and costly lab work, species coverage in this field will probably not improve much in the foreseeable future. Recent findings from passerine birds, which constitute the largest avian order (∼5 900 species), suggest that sperm phenotypes carry a signature of sperm competition. Here we examine how well standardized measures of sperm length variation can predict the rate of extrapair paternity in passerine birds.Methodology/Principal FindingsWe collected sperm samples from 55 passerine species in Canada and Europe for which extrapair paternity rates were already available from either the same (n = 24) or a different (n = 31) study population. We measured the total length of individual spermatozoa and found that both the coefficient of between-male variation (CVbm) and within-male variation (CVwm) in sperm length were strong predictors of the rate of extrapair paternity, explaining as much as 65% and 58%, respectively, of the variation in extrapair paternity among species. However, only the CVbm predictor was independent of phylogeny, which implies that it can readily be converted into a currency of extrapair paternity without the need for phylogenetic correction.Conclusion/SignificanceWe propose the CVbm index as an alternative measure to extrapair paternity for passerine birds. Given the ease of sperm extraction from male birds in breeding condition, and a modest number of sampled males required for a robust estimate, this new index holds a great potential for mapping the risk of sperm competition across a wide range of passerine birds.

Inbreeding depresses sperm competitiveness, but not fertilization or mating success in male Tribolium castaneum

As populations decline to levels where reproduction among close genetic relatives becomes more probable, subsequent increases in homozygous recessive deleterious expression and/or loss of heterozygote advantage can lead to inbreeding depression. Here, we measure how inbreeding across replicate lines of the flour beetle Tribolium castaneum impacts on male reproductive fitness in the absence or presence of male-male competition. Effects on male evolution from mating pattern were removed by enforcing monogamous mating throughout. After inbreeding across eight generations, we found that male fertility in the absence of competition was unaffected. However, we found significant inbreeding depression of sperm competitiveness: non-inbred males won 57 per cent of fertilizations in competition, while inbred equivalents only sired 42 per cent. We also found that the P(2) 'offence' role in sperm competition was significantly more depressed under inbreeding than sperm 'defence' (P(1)). Mating behaviour did not explain these differences, and there was no difference in the viability of offspring sired by inbred or non-inbred males. Sperm length variation was significantly greater in the ejaculates of inbred males. Our results show that male ability to achieve normal fertilization success was not depressed under strong inbreeding, but that inbreeding depression in these traits occurred when conditions of sperm competition were generated.

Sperm length is not influenced by haploid gene expression in the flies Drosophila melanogaster and Scathophaga stercoraria

Recent theoretical models have postulated a role for haploid-diploid conflict and for kin selection favouring sperm cooperation and altruism in the diversification and specialization of sperm form. A critical assumption of these models-that haploid gene expression contributes to variation in sperm form-has never been demonstrated and remains contentious. By quantifying within-male variation in sperm length using crosses between males and females from populations that had been subjected to divergent experimental selection, we demonstrate that haploid gene expression does not contribute to variation in sperm length in both Drosophila melanogaster and Scathophaga stercoraria. This finding casts doubt on the importance of haploid-diploid conflict and kin selection as evolutionary influences of sperm phenotypes.