Micromotor-mediated sperm constrictions for improved swimming performance.
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ABSTRACT:
SUBMITTER: Striggow F
PROVIDER: S-EPMC8113191 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Mammals exhibit a tremendous amount of variation in sperm morphology and despite the acknowledgement of sperm structural diversity across taxa, its functional significance remains poorly understood. Of particular interest is the sperm of rodents. While most Eutherian mammal spermatozoa are relatively simple cells with round or paddle-shaped heads, rodent sperm are often more complex and, in many species, display a striking apical hook. The function of the sperm hook remains largely unknown, but it has been hypothesized to have evolved as an adaptation to inter-male sperm competition and thus has been implicated in increased swimming efficiency or in the formation of collective sperm movements. Here we empirically test these hypotheses within a single lineage of Peromyscus rodents, in which closely related species naturally vary in their mating systems, sperm head shapes, and propensity to form sperm aggregates of varying sizes. We performed sperm morphological analyses as well as in vitro analyses of sperm aggregation and motility to examine whether the sperm hook (i) morphologically varies across these species and (ii) associates with sperm competition, aggregation, or motility. We demonstrate inter-specific variation in the sperm hook and then show that hook width negatively associates with sperm aggregation and sperm swimming speed, signifying that larger hooks may be a hindrance to sperm movement within this group of mice. Finally, we confirmed that the sperm hook hinders motility within a subset of Peromyscus leucopus mice that spontaneously produced sperm with no or highly abnormal hooks. Taken together, our findings suggest that any adaptive value of the sperm hook is likely associated with a function other than inter-male sperm competition, such as interaction with ova or cumulous cells during fertilization, or migration through the complex female reproductive tract.
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Project description:From flocking birds to swarming insects, interactions of organisms large and small lead to the emergence of collective dynamics. Here, we report striking collective swimming of bovine sperm in dynamic clusters, enabled by the viscoelasticity of the fluid. Sperm oriented in the same direction within each cluster, and cluster size and cell-cell alignment strength increased with viscoelasticity of the fluid. In contrast, sperm swam randomly and individually in Newtonian (nonelastic) fluids of low and high viscosity. Analysis of the fluid motion surrounding individual swimming sperm indicated that sperm-fluid interaction was facilitated by the elastic component of the fluid. In humans, as well as cattle, sperm are naturally deposited at the entrance to the cervix and must swim through viscoelastic cervical mucus and other mucoid secretions to reach the site of fertilization. Collective swimming induced by elasticity may thus facilitate sperm migration and contribute to successful fertilization. We note that almost all biological fluids (e.g. mucus and blood) are viscoelastic in nature, and this finding highlights the importance of fluid elasticity in biological function.
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Project description:Seminal plasma (SP) plays a crucial role in reproduction and contains a large number of proteins, many of which may potentially modify sperm functionality. To evaluate the effects of SP identity and its protein composition on human sperm function, we treated the sperm of several males with either their own or multiple foreign SPs in all possible sperm-SP combinations (full-factorial design). Then we recorded sperm motility and viability in these combinations and investigated whether the sperm performance is dependent on sperm and SP identity (or their interaction). Finally, we studied whether the above-mentioned sperm traits are affected by the abundance of three SP proteins, dipeptidyl peptidase-4 (DPP4), neutral endopeptidase (NEP), and aminopeptidase N (APN). The identity of the SP donor affected sperm swimming velocity, viability, and the proportion of hyperactivated sperm, but males' own SP was not consistently more beneficial for sperm than foreign SPs. Furthermore, we show that sperm performance is also partly affected by the interaction between sperm and SP donor. Finally, we found that DPP4 and NEP levels in SP were positively associated with sperm swimming velocity and hyperactivation. Taken together, our results highlight the importance of seminal plasma as a potential source of biomarkers for diagnostics and therapeutic interventions for male-derived infertility.
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Project description:Over the last 50 years, sperm competition has become increasingly recognised as a potent evolutionary force shaping male ejaculate traits. One such trait is sperm swimming speed, with faster sperm associated with increased fertilisation success in some species. Consequently, sperm are often thought to have evolved to be longer in order to facilitate faster movement. However, despite the intrinsic appeal of this argument, sperm operate in a different biophysical environment than we are used to, and instead increasing length may not necessarily be associated with higher velocity. Here, we test four predictive models (ConstantPower Density, Constant Speed, Constant Power Transfer, Constant Force) of the relationship between sperm length and speed. We collated published data on sperm morphology and velocity from 141 animal species, tested for structural clustering of sperm morphology and then compared the model predictions across all morphologically similar sperm clusters. Within four of five morphological clusters of sperm, we did not find a significant positive relationship between total sperm length and velocity. Instead, in four morphological sperm clusters we found evidence for the Constant Speed model, which predicts that power output is determined by the flagellum and so is proportional to flagellum length. Our results show the relationship between sperm morphology (size, width) and swimming speed is complex and that traditional models do not capture the biophysical interactions involved. Future work therefore needs to incorporate not only a better understanding of how sperm operate in the microfluid environment, but also the importance of fertilising environment, i.e., internal and external fertilisers. The microenvironment in which sperm operate is of critical importance in shaping the relationship between sperm length and form and sperm swimming speed.
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Project description:We investigated the hypothesis that intra ejaculate sperm competition screens against the transmission of deleterious alleles, including new mutants, from male parent to offspring. Recent investigations have established that sperm haploid genotypes can have major effects on sperm traits such as cellular robustness, longevity, and fertilization success. However, there is no evidence that new mutations can meaningfully affect sperm phenotypes. We tested this directly by comparing sperm from mutagenized and non-mutagenized control males in Astyanax fish. We used N-ethyl-N-nitrosourea (ENU) to induce single base substitutions in spermatogonial stem cells. We looked at swimming velocity, an important factor contributing to fertilization success, and flagellar length. Variability in swimming velocity was significantly higher in sperm from mutagenized males than in control sperm, reflecting their increased allelic diversity. In contrast, flagellar length, which is fixed during diploid stages of spermatogenesis, was unaffected by ENU treatment. We briefly discuss the implications of intra-ejaculate screening for maintenance of anisogamy and for outcomes of assisted reproductive technology.
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Project description:The selection of high-quality sperm is essential to the success of in vitro fertilization (IVF). As human cervical mucus has a high viscosity, without enough swimming persistence, human sperm clouds cannot arrive at the ampulla to fertilize the egg. In this study, we used swimming capability and motion characteristics that are known to be associated with fertilization ability to evaluate the quality of sperm. Here, a clinically applicable polymethyl methacrylate (PMMA)-based microdevice was designed and fabricated for sperm evaluation and screening for swimming capability and persistence in a viscous environment. In this study, we applied methylcellulose (MC) to mimic the natural properties of mucus in vivo to achieve the selection of motile sperm. Sperm motion was recorded by an inverted microscope. The statistical features were extracted and analyzed. Hundreds of sperm in two treated groups with different concentrations of MC and one control group with human tubal fluid (HTF) media were video recorded. This device can achieve a one-step procedure of high-quality sperm selection and achieve the quantitative evaluation of sperm swimming capability and persistence. Sperm with good swimming capability and persistence may be more suitable for fertilization in a viscous environment. This microdevice and methods could be used to guide the evaluation of sperm motility and screening in the future.
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Project description:Despite evidence that variation in male-female reproductive compatibility exists in many fertilization systems, identifying mechanisms of cryptic female choice at the gamete level has been a challenge. Here, under risks of genetic incompatibility through hybridization, we show how salmon and trout eggs promote fertilization by conspecific sperm. Using in vitro fertilization experiments that replicate the gametic microenvironment, we find complete interfertility between both species. However, if either species' ova were presented with equivalent numbers of both sperm types, conspecific sperm gained fertilization precedence. Surprisingly, the species' identity of the eggs did not explain this cryptic female choice, which instead was primarily controlled by conspecific ovarian fluid, a semiviscous, protein-rich solution that bathes the eggs and is released at spawning. Video analyses revealed that ovarian fluid doubled sperm motile life span and straightened swimming trajectory, behaviors allowing chemoattraction up a concentration gradient. To confirm chemoattraction, cell migration tests through membranes containing pores that approximated to the egg micropyle showed that conspecific ovarian fluid attracted many more spermatozoa through the membrane, compared with heterospecific fluid or water. These combined findings together identify how cryptic female choice can evolve at the gamete level and promote reproductive isolation, mediated by a specific chemoattractive influence of ovarian fluid on sperm swimming behavior.
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Project description:The diploid genotypes of males are widely thought to determine sperm phenotypes, yet recent work shows that the haploid genetics of the individual sperm cell also contributes significantly. We tested seven sperm phenotypes, flagellar length and six behaviors, looking for correlations between genetic and phenotypic variability. While flagellar length appears to be controlled by the diploid genotype of the source, variation in three of the behavioral phenotypes, linearity, wobble, and progression are significantly correlated with the heterozygosity of the male producer. Because males that are more genetically variable produce a sperm set that is more diverse in its haploid genotypes, we suggest that the correlations may reflect significant haploid genetic control of sperm swimming behaviors.
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Project description:Collective swimming is evident in the sperm of several mammalian species. In bull (Bos taurus) sperm, high viscoelasticity of the surrounding fluid induces the sperm to form dynamic clusters. Sperm within the clusters swim closely together and align in the same direction, yet the clusters are dynamic because individual sperm swim into and out of them over time. As the fluid in part of the mammalian female reproductive tract contains mucus and, consequently, is highly viscoelastic, this mechanistic clustering likely happens in vivo. Nevertheless, it has been unclear whether clustering could provide any biological benefit. Here, using a microfluidic in vitro model with viscoelastic fluid, we found that the collective swimming of bull sperm in dynamic clusters provides specific biological benefits. In static viscoelastic fluid, clustering allowed sperm to swim in a more progressive manner. When the fluid was made to flow in the range of 2.43-4.05 1/sec shear rate, clustering enhanced the ability of sperm to swim upstream. We also found that the swimming characteristics of sperm in our viscoelastic fluid could not be fully explained by the hydrodynamic model that has been developed for sperm swimming in a low-viscosity, Newtonian fluid. Overall, we found that clustered sperm swam more oriented with each other in the absence of flow, were able to swim upstream under intermediate flows, and better withstood a strong flow than individual sperm. Our results indicate that the clustering of sperm can be beneficial to sperm migrating against an opposing flow of viscoelastic fluid within the female reproductive tract.
| S-EPMC9535079 | biostudies-literature
Project description:BackgroundCompetition between spermatozoa from rival males for success in fertilization (i.e., sperm competition) is an important selective force driving the evolution of male reproductive traits and promoting positive selection in genes related to reproductive function. Positive selection has been identified in reproductive proteins showing rapid divergence at nucleotide level. Other mutations, such as insertions and deletions (indels), also occur in protein-coding sequences. These structural changes, which exist in reproductive genes and result in length variation in coded proteins, could also be subjected to positive selection and be under the influence of sperm competition. Catsper1 is one such reproductive gene coding for a germ-line specific voltage-gated calcium channel essential for sperm motility and fertilization. Positive selection appears to promote fixation of indels in the N-terminal region of CatSper1 in mammalian species. However, it is not known which selective forces underlie these changes and their implications for sperm function.ResultsWe tested if length variation in the N-terminal region of CatSper1 is influenced by sperm competition intensity in a group of closely related rodent species of the subfamily Murinae. Our results revealed a negative correlation between sequence length of CatSper1 and relative testes mass, a very good proxy of sperm competition levels. Since CatSper1 is important for sperm flagellar motility, we examined if length variation in the N-terminus of CatSper1 is linked to changes in sperm swimming velocity. We found a negative correlation between CatSper1 length and several sperm velocity parameters.ConclusionsAltogether, our results suggest that sperm competition selects for a shortening of the intracellular region of CatSper1 which, in turn, enhances sperm swimming velocity, an essential and adaptive trait for fertilization success.
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