Sperm competition when transfer is dangerous.
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ABSTRACT:
SUBMITTER: Tuni C
PROVIDER: S-EPMC7661443 | biostudies-literature | 2020 Dec
REPOSITORIES: biostudies-literature
Publications
Sperm competition when transfer is dangerous.
Tuni Cristina C Schneider Jutta J Uhl Gabriele G Herberstein Marie E ME
Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20201019 1813
Aggressive and cannibalistic female spiders can impose strong selection on male mating and fertilization strategies. Furthermore, the distinctive reproductive morphology of spiders is predicted to influence the outcome of sperm competition. Polyandry is common in spiders, leading to defensive male strategies that include guarding, plugging and self-sacrifice. Paternity patterns are highly variable and unlikely to be determined solely by mating order, but rather by relative copulation duration, d ...[more]
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Project description:Sperm competition favors increases in relative testes mass and production efficiency, and changes in sperm phenotype that result in faster swimming speeds. However, little is known about its effects on traits that contribute to determine the quality of a whole ejaculate (i.e., proportion of motile, viable, morphologically normal and acrosome intact sperm) and that are key determinants of fertilization success. Two competing hypotheses lead to alternative predictions: (a) sperm quantity and quality traits co-evolve under sperm competition because they play complementary roles in determining ejaculate's competitive ability, or (b) energetic constraints force trade-offs between traits depending on their relevance in providing a competitive advantage. We examined relationships between sperm competition levels, sperm quantity, and traits that determine ejaculate quality, in a comparative study of 18 rodent species using phylogenetically controlled analyses. Total sperm numbers were positively correlated to proportions of normal sperm, acrosome integrity and motile sperm; the latter three were also significantly related among themselves, suggesting no trade-offs between traits. In addition, testes mass corrected for body mass (i.e., relative testes mass), showed a strong association with sperm numbers, and positive significant associations with all sperm traits that determine ejaculate quality with the exception of live sperm. An "overall sperm quality" parameter obtained by principal component analysis (which explained 85% of the variance) was more strongly associated with relative testes mass than any individual quality trait. Overall sperm quality was as strongly associated with relative testes mass as sperm numbers. Thus, sperm quality traits improve under sperm competition in an integrated manner suggesting that a combination of all traits is what makes ejaculates more competitive. In evolutionary terms this implies that a complex network of genetic and developmental pathways underlying processes of sperm formation, maturation, transport in the female reproductive tract, and preparation for fertilization must all evolve in concert.
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Project description:Multiple paternity is ubiquitous within the polyphyletic group called 'reptiles', especially within the lizards and snakes. Therefore, the probability of sperm competition occurring, and being intense, is high. Squamates exhibit a diversity of tactics to ensure fertilization success in the face of sperm competition. The duration of female sperm storage, which can be many months and even years in some species, remains an enigma. Here, we emphasize some mechanisms that might affect patterns of paternity, the source and function of ejaculates and features of the female reproductive tract that may aid in long-term sperm storage. In doing so, we present a new analysis of the relationship between sperm size, the strength of sperm competition and the duration of female sperm storage. Lizards and snakes are a diverse group that has provided many excellent models for the study of an array of life-history strategies. However, when it comes to postcopulatory sexual selection, there is much left to discover. This article is part of the theme issue 'Fifty years of sperm competition'.
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Project description: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.
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Project description:BackgroundThe influence of sperm competition upon sperm size has been a controversial issue during the last 20 years which remains unresolved for mammals. The hypothesis that, when ejaculates compete with rival males, an increase in sperm size would make sperm more competitive because it would increase sperm swimming speed, has generated contradictory results from both theoretical and empirical studies. In addition, the debate has extended to which sperm components should increase in size: the midpiece to accommodate more mitochondria and produce more energy to fuel motility, or the principal piece to generate greater propulsion forces.ResultsIn this study we examined the influence of sperm competition upon sperm design in mammals using a much larger data set (226 species) than in previous analyses, and we corrected for phylogenetic effects by using a more complete and resolved phylogeny, and more robust phylogenetic control methods. Our results show that, as sperm competition increases, all sperm components increase in an integrated manner and sperm heads become more elongated. The increase in sperm length was found to be associated with enhanced swimming velocity, an adaptive trait under sperm competition.ConclusionsWe conclude that sperm competition has played an important role in the evolution of sperm design in mammals, and discuss why previous studies have failed to detect it.
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Project description:BackgroundUsing information from physics, biomechanics and evolutionary biology, we explore the implications of physical constraints on sperm performance, and review empirical evidence for links between sperm length and sperm competition (where two or more males compete to fertilize a female's eggs). A common theme in the literature on sperm competition is that selection for increased sperm performance in polyandrous species will favour the evolution of longer, and therefore faster swimming, sperm. This argument is based on the common assumption that sperm swimming velocity is directly related to sperm length, due to the increased thrust produced by longer flagella.ResultsWe critically evaluate the evidence for links between sperm morphology and swimming speed, and draw on cross-disciplinary studies to show that the assumption that velocity is directly related to sperm length will rarely be satisfied in the microscopic world in which sperm operate.ConclusionWe show that increased sperm length is unlikely to be driven by selection for increased swimming speed, and that the relative lengths of a sperm's constituent parts, rather than their absolute lengths, are likely to be the target of selection. All else being equal, we suggest that a simple measure of the ratio of head to tail length should be used to assess the possible link between morphology and speed. However, this is most likely to be the case for external fertilizers in which females have relatively limited opportunity to influence a sperm's motility.
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Project description:Interactions among eggs and sperm are often assumed to generate intraspecific variation in reproductive fitness, but the specific gamete-level mechanisms underlying competitive fertilization success remain elusive in most species. Sperm chemotaxis-the attraction of sperm by egg-derived chemicals-is a ubiquitous form of gamete signaling, occurring throughout the animal and plant kingdoms. The chemical cues released by eggs are known to act at the interspecific level (e.g., facilitating species recognition), but recent studies have suggested that they could have roles at the intraspecific level by moderating sperm competition. Here, we exploit the experimental tractability of a broadcast spawning marine invertebrate to test this putative mechanism of gamete-level sexual selection. We use a fluorescently labeled mitochondrial dye in mussels to track the real-time success of sperm as they compete to fertilize eggs, and provide the first direct evidence in any species that competitive fertilization success is moderated by differential sperm chemotaxis. Furthermore, our data are consistent with the idea that egg chemoattractants selectively attract ejaculates from genetically compatible males, based on relationships inferred from both nuclear and mitochondrial genetic markers. These findings for a species that exhibits the ancestral reproductive strategy of broadcast spawning have important implications for the numerous species that also rely on egg chemoattractants to attract sperm, including humans, and have potentially important implications for our understanding of the evolutionary cascade of sexual selection.
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Project description:Appropriate timing of mating is crucial for the success of individuals. However, we know little about factors that explain variation in mating time in unicellular organisms. Unicellular eukaryotes often have facultative sexuality, that is, the less frequent sex is occasionally induced after long clonal reproduction. Thus, males originated from clonemates could be non-negligible mating rivals. Using a centric diatom whose clonal cells differentiate into either male or female, we analysed whether males (spermatogonium) compete or cooperate with each other. By analysing differentiation timing with hypotheses based on evolutionary game theory, we estimated that a substantial part of the variation in the mating timing of the diatom can be explained by results of optimization through interactions among selfish individuals rather than cooperation among clonemates. However, the competition is fiercer than expected owing to excessive synchronization, which was realized by adjustment of meiotic duration: cells completed mitotic division in the earlier mating phase took longer to enter into meiosis, whereas late-dividing cells entered into meiosis more quickly. Adjacent cells tended to synchronize, and model analyses suggest that cell-cell interaction can create a gap between the optimal and actual decisions. Our results provide insights into the evolution of cellular decision making and its restriction.
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Project description:Ejaculate attributes are important factors driving the probability of fertilizing eggs. When females mate with several males, competition between sperm to fertilize eggs should accentuate selection on ejaculate attributes. We tested this hypothesis in the North African houbara bustard ( Chlamydotis undulata undulata) by comparing the strength of selection acting on two ejaculate attributes when sperm from single males or sperm from different males were used for insemination. In agreement with the prediction, we found that selection on ejaculate attributes was stronger when sperm of different males competed for egg fertilization. These findings provide the first direct comparison of the strength of selection acting on ejaculate attributes under competitive and non-competitive fertilizations, confirming that sperm competition is a major selective force driving the evolution of ejaculate characteristics.
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Project description:Sperm competition is a powerful selective force that has shaped sexual traits throughout animal evolution. Yet, how fertilization mode (i.e. external versus internal fertilization) influences the scope and potential for sperm competition to act on ejaculates remains unclear. Here, I examine how fertilization mode shapes ejaculatory responses to sperm competition in fishes, a diverse group that constitute the majority of vertebrate biological diversity. Fishes are an ideal group for this examination because they exhibit a wide range of reproductive behaviours and an unparalleled number of transitions in fertilization mode compared to any other vertebrate group. Drawing on data from cartilaginous and bony fishes, I first show that rates of multiple paternity are higher in internally than externally fertilizing fishes, contrary to the prevailing expectation. I then summarize how sperm competition acts on sperm number and quality in internally and externally fertilizing fishes, highlighting where theoretical predictions differ between these groups. Differences in how ejaculates respond to sperm competition between fertilization modes are most apparent when considering sperm size and swimming performance. Clarifying how fertilization mode influences evolutionary responses in ejaculates will inform our understanding of ejaculate evolution across the animal tree of life. This article is part of the theme issue 'Fifty years of sperm competition'.
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Project description: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.
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