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Social polyandry shapes sperm morphology
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Data from: Dunnock social status correlates with sperm speed, but fast sperm does not always equal high fitness
<p>Sperm competition theory predicts that males should modulate sperm investment according to their social status. Sperm speed, one proxy of sperm quality, also influences the outcome of sperm competition because fast sperm cells may fertilize eggs before slow sperm cells. We evaluated whether the social status of males predicted their sperm speed in a wild population of dunnocks (<em>Prunella modularis</em>). In addition to the traditional analysis of the average speed of sperm cells per sample, we also analyzed subsamples of the fastest sperm cells per sample. In other words, we systematically evaluated the effects of including different numbers of the fastest sperm in our analyses, ranging from the 5-fastest sperm cells to the 100-fastest sperm cells in a sample. We further evaluated whether fitness, defined here as the number of chicks sired per male per breeding season, relates to the sperm speed in the same population. We found that males in monogamous pairings (i.e. low levels of sperm competition), produced the slowest sperm cells whereas subordinate males in polyandrous male-male coalitions, (i.e. high levels of sperm competition), produced the fastest sperm cells. This result was consistent regardless of the number of fastest sperm included in our analyses, but statistical support was conditional on the number of sperm cells included in the analysis. Interestingly, we found no significant relationship between fitness and sperm speed, which suggests that it is possible that the differential mating opportunities across social status leveled out any possible difference. Our study also suggests that it is important to identify biologically meaningful subsets of fastest sperm and cutoffs for inclusions for assessing sperm competition via sperm speed</p>
Data from: Repeated evidence that the accelerated evolution of sperm is associated with their fertilization function
<p><span><span><span><span><span><span><span><span><span><span><span>Spermatozoa are the most morphologically diverse cell type, leading to the widespread assumption that they evolve rapidly. However, there is no direct evidence that sperm evolve faster than other male traits. Such a test requires comparing male traits that operate in the same selective environment, ideally produced from the same tissue, yet vary in function. Here we examine rates of phenotypic evolution in sperm morphology using two insect groups where males produce fertile and non-fertile sperm types (<i>Drosophila </i>species from the <i>obscura </i>group and Lepidoptera), where these constraints are solved. Moreover, in <i>Drosophila </i>we test the relationship between rates of sperm evolution and the link with the putative selective pressures of fertilization function and postcopulatory sexual selection exerted by female reproductive organs.We find repeated evolutionary patterns across these insect groups – lengths of fertile sperm evolve faster than non-fertile sperm. In <i>Drosophila</i>, fertile sperm length evolved faster than body size, but at the same rate as female reproductive organ length. We also compare rates of evolution of different sperm components, showing that head length evolves faster in fertile sperm while flagellum length evolves faster in non-fertile sperm. Our study provides direct evidence that sperm length evolves more rapidly in fertile sperm, likely because of their functional role in securing male fertility and in response to selection imposed by female reproductive organs.</span></span></span></span></span></span></span></span></span></span></span></p>
Dataset used to map a stump tail sperm defect of Swiss Large White boars
<p>This dataset contains genotypes for 106 Swiss Large White boars that were used to map a stump tail sperm defect and a VCF file that contains genotypes of candiate variants for 87 boars.</p> <p>The subdirectories contain plink binaries, corresponding phased haplotypes (in MaCH format), the results of a haplotype-based GWAS, and a VCF file that contains genotypes at candidate causal variants.</p> <p>The affection status (case=2, control=1) of 106 boars is indicated in the file "pheno".</p> <p>The R script "haplo_linear.R" performs the haplotype-based association study.</p> <p>The README file provides instructions on how to run the GWAS as well as on how to create the Manhattan plot.</p>
Dataset accompanying: Echolocation click parameters and biosonar behaviour of the dwarf sperm whale (Kogia sima)
<p>This dataset accompanies the manuscript "Echolocation click parameters and biosonar behaviour of the dwarf sperm whale (<em>Kogia sima</em>)." All source parameters of on-axis clicks are available in MATLAB files, for both the deep water (n=46) and shallow harbour (n=870) datasets. The deep water dataset was collected using a 7-channel vertical hydrophone array in the Bahamas, and the shallow harbour dataset was collected using a single-channel recorder in South Africa. Metadeta explaining the variables are found within the MATLAB files under 'Comments'. Details on data collection, curation and analysis can be found in the Malinka et al., Kogia publication (https://jeb.biologists.org/content/224/6/jeb240689).</p> <p>For comments/questions, please contact chloe.e.malinka [at] bio.au.dk</p>
Increased sperm production linked to competition in the maternal social environment
<p>Maternal or early life effects may prepare offspring for similar social conditions to those experienced by their mothers. For males, the ability to achieve mating and fertilisation success is a key social challenge. Competitive conditions may therefore favour increased body size or ejaculate production in male offspring. We tested this experimentally by comparing reproductive traits of adult male bank voles (<i>Myodes glareolus</i>), whose mothers had experienced contrasting encounter regimes with female conspecifics while breeding. We found that daily sperm production rates and epididymis mass were significantly higher when dams had experienced more frequent encounters with female conspecifics. This response to maternal and early life experience was specific to sperm production and storage, with no evidence for effects on male body mass or the size of testes and accessory reproductive glands. Our findings reveal a potentially adaptive effect of maternal and early-life experience on the development of sperm production, which is worthy of wider investigation.</p>
Costs and benefits of multiple mating in a species with first male sperm precedence
1. Different patterns of sperm precedence are expected to entail different costs and benefits of mating for each sex that translate into distinct predictions regarding mating system evolution. Still, most studies addressing these costs and benefits have focused on species with mixed paternity or last male precedence, neglecting first male sperm precedence. We attempted to understand whether this latter pattern of sperm precedence translates into different costs and benefits for each sex in the haplodiploid spider mite Tetranychus urticae, a species in which female multiple mating is prevalent but the majority of the offspring is sired by first males. 2. First, we assessed the stability of the sperm precedence pattern. To do so, we measured offspring paternity after exposing females to a different number of matings and mating intervals. Next, to determine the potential costs or benefits of multiple mating for females under different contexts, we measured the fecundity and survival of females that re-mated at different time points. To measure the potential costs of multiple mating for males, we analysed male survival in the presence of different numbers of virgin or mated females. We also tested whether males can reduce offspring production of their competitors, by reducing the production of fertilized offspring of mated females. 3. We found no change in the pattern of sperm precedence, independently of the mating interval between matings and the number of matings. Females paid a cost of mating, as multiply mated females laid fewer eggs than once-mated females. However, while males had reduced survival when exposed to an intermediate number of virgin females, they paid no additional costs of mating with mated females. Moreover, females that mated multiple times produced fewer fertilized offspring than females that mated once. Thus, males that copulated with mated females reduced the fitness of other males, potentially leading to a relative fitness benefit for themselves. 4. Our results show that complex costs and benefits may arise in males in species with first male sperm precedence. How these costs and benefits affect the maintenance of selection for polyandry remains an open question. 29-Nov-2019
Data from: The relationship of body condition, superoxide dismutase, and superoxide with sperm performance
Sperm competition theory predicts a negative correlation between somatic investment in traits that aid in pre- and postcopulatory sexual selection. Sperm performance is critical for postcopulatory success but are susceptible to damage by free radicals such as superoxide radicals generated during mitochondrial respiration (mtSOx). Males can ameliorate damage to spermatozoa by investing in the production of antioxidants, like superoxide dismutase (SOD), which may act as a mechanistic link for pre and postcopulatory trade-offs. Some male Australian, colour-polymorphic painted dragon lizards (Ctenophorus pictus) possess a yellow throat patch (bib) that females prefer over non-bibbed males and are also more likely to win male-male contests indicating that males with bibs are better at monopolizing females. We tested whether the sperm performance in non-bibbed males was superior to that of bibbed males as predicted by sperm competition theory. We show that blood cell mtSOx levels are negatively correlated with SOD activity in the plasma in all males early in the breeding season but SOD was lower in bibbed males. Non-bibbed males maintain a positive correlation between body condition and SOD activity over time while bibbed males do not. Overall sperm performance was not different between the bib-morphs, however, higher mtSOx levels were negatively correlated with sperm performance in bibbed males, but not of non-bibbed males. Together these data suggest physiological associations between body condition, SOD activity and sperm performance are linked to the expression of a yellow gular patch, which may be related to intrinsic differences in metabolism of bibbed versus non-bibbed males
Egg-induced changes to sperm phenotypes shape patterns of multivariate selection on ejaculates
<p class="MsoPlainText">Ejaculates exhibit extraordinary phenotypic diversity and rapid rates of evolution, yet the adaptive value of most sperm traits remains equivocal. Recent findings suggest that to understand how selection targets ejaculates we must recognize that female-imposed physiological conditions often alter ejaculate phenotypes. These phenotypic changes to ejaculates may influence the relationships among sperm traits and their association with fitness. Here, we show that chemical substances released by eggs (known to modify sperm physiology and behavior) alter patterns of selection on a suite of sperm traits in the mussel Mytilus galloprovincialis. We use multivariate selection analyses to characterize linear and nonlinear selection acting on sperm traits in (a) seawater alone, and (b) seawater containing egg-derived chemicals (egg water). Our analyses revealed that nonlinear selection on canonical axes of multiple traits (notably sperm velocity, sperm linearity and percentage of motile sperm) was the most important form of selection overall, but importantly these patterns were only evident when sperm phenotypes were measured in egg water. These findings reveal the subtle way that females can alter patterns of selection, with the implication that overlooking environmentally-moderated changes to ejaculate phenotypes may result in erroneous interpretations of how selection targets phenotypic (co)variation in ejaculate traits.</p>
Data from: Effects of condition and sperm competition risk on sperm allocation and storage in neriid flies
<p>Ejaculate traits can be sexually selected and often exhibit heightened condition-dependence. However, the influence of sperm competition risk in tandem with condition-dependent ejaculate allocation strategies is relatively unstudied. Because ejaculates are costly to produce, high-condition males may be expected to invest more in ejaculates when sperm competition risk is greater. We examined the condition-dependence of ejaculate size by manipulating nutrient concentration in the juvenile (larval) diet of the neriid fly Telostylinus angusticollis. Using a fully factorial design we also examined the effects of perceived sperm competition risk (manipulated by allowing males to mate first or second) on the quantity of ejaculate transferred and stored in the three spermathecae of the female reproductive tract. To differentiate male ejaculates, we fed males non-toxic rhodamine fluorophores (which bind to proteins in the body) prior to mating, labelling their sperm red or green. We found that high-condition males initiated mating more quickly and, when mating second, transferred more ejaculate to both of the female's posterior spermathecae. This suggests that males allocate ejaculates strategically, with high-condition males elevating their ejaculate investment only when facing sperm competition. More broadly, our findings suggest that ejaculate allocation strategies can incorporate variation in both condition and perceived risk of sperm competition.</p>
Data from: Sperm competitive advantage of a rare mitochondrial haplogroup linked to differential expression of mitochondrial oxidative phosphorylation genes
Maternal inheritance of mitochondria creates a sex-specific selective sieve through which mitochondrial mutations harmful to males but not females accumulate and contribute to sexual differences in longevity and disease susceptibility. Because eggs and sperm are under disruptive selection, sperm are predicted to be particularly vulnerable to the genetic load generated by maternal inheritance, yet evidence for mitochondrial involvement in male fertility is limited and controversial. Here, we exploit the coexistence of two divergent mitochondrial haplogroups (A and B2) in a Neotropical arachnid to investigate the role of mitochondria in sperm competition. DNA profiling demonstrated that B2-carrying males sired more than three times as many offspring in sperm competition experiments than A males, and this B2 competitive advantage cannot be explained by female mitochondrial haplogroup or male nuclear genetic background. RNA-Seq of testicular tissues implicates differential expression of mitochondrial oxidative phosphorylation (OXPHOS) genes in the B2 competitive advantage, including a 22-fold upregulation of <i>atp8</i> in B2 males. Previous comparative genomic analyses have revealed functionally significant amino acid substitutions in differentially expressed genes, indicating that the mitochondrial haplogroups differ not only in expression but also in DNA sequence and protein functioning. However, mitochondrial haplogroup had no effect on sperm number or sperm viability, and, when females were mated to a single male, neither male haplogroup, female haplogroup nor the interaction between male/female haplogroup significantly affected female reproductive success. Our findings therefore suggest that mitochondrial effects on male reproduction may often go undetected in noncompetitive contexts and may prove more important in nature than is currently appreciated.
Offspring phenotype is shaped by the non-sperm fraction of semen
<p>In a large majority of animal species, the only contribution of males to the next generation has been assumed to be their genes (sperm). However, along with sperm, seminal plasma contains a wide array of extracellular factors that have many important functions in reproduction. Yet, the potential intergenerational effects of these factors are virtually unknown. We investigated these effects in European whitefish (<i>Coregonus lavaretus</i>) by experimentally manipulating the presence and identity of seminal plasma and by fertilizing the eggs of multiple females with the manipulated and unmanipulated semen of several males in a full-factorial breeding design. Presence of both own and foreign seminal plasma inhibited sperm motility and removal of own seminal plasma decreased embryo survival. Embryos hatched significantly earlier after both semen manipulations than in control fertilizations; foreign seminal plasma also increased offspring aerobic swimming performance. Given that our experimental design allowed us to control potentially confounding sperm-mediated (sire) effects and maternal effects, our results indicate that seminal plasma may have direct intergenerational consequences for offspring phenotype and performance. This novel source of offspring phenotypic variance may provide new insights into the evolution of polyandry and mechanisms that maintain heritable variation in fitness and associated female mating preferences.</p>
Sequential_Sperm_Competition: Mathematica Code
<p>Mathematica code for the study "Female sperm use and storage between fertilization events drive sperm competition and male ejaculate allocation"</p>
Dataset from 'Size Distribution of Sperm Whales Acoustically Identified During Long Term Deep-Sea Monitoring in the Ionian Sea'
<p>This dataset is from the study:</p> <p>Caruso Francesco, Virginia Sciacca, Giorgio Bellia, Emilio De Domenico, Giuseppina Larosa, Elena Papale, Carmelo Pellegrino, Sara Pulvirenti, Giorgio Riccobene, Francesco Simeone, Fabrizio Speziale, Salvatore Viola and Gianni Pavan. “Size Distribution of Sperm Whales Acoustically Identified During Long Term Deep-Sea Monitoring in the Ionian Sea.”</p> <p>The archive named NEMO-OvDE Dataset.zip contains the results of an automatic analysis developed and applied to the data acquired by the Ocean noise Detection Experiment. In detail, a subsample of the large dataset was processed to assess the size of the recorded sperm whales, by measuring the structure of their acoustic signals. The dataset consists in several plots generated by the algorithm described in the cited research article. The files are in PNG format. These data were used to study the size distribution of the sperm whale recorded during the OvDE Passive Acoustic Monitoring.</p> <p>For further information: riccobene@lns.infn.it (Principal Investigator of the Ocean noise Detection Experiment)</p>
Application of flow cytometry using advanced chromatin analyses for assessing changes in the sperm structure and DNA integrity in a porcine model
<p><span>Chromatin status is critical for sperm fertility. We tested a multivariate approach for studying pig sperm chromatin, aiming to capture the chromatin structure's complexity with a set of quick and simple techniques, not only DNA damage. Sperm doses from 36 boars (3 ejaculates/boar) were analyzed at days 0 and 11 (cooled storage). Analyses were: CASA (motility) and flow cytometry to assess sperm functionality and chromatin structure by SCSA (DNA fragmentation %DFI and chromatin maturity %HDS), monobromobimane (mBBr, tiol status/disulfide bridges between protamines), chromomycin A3 (CMA3, protamination) and 8-hydroxy-2'-deoxyguanosine (8-oxo-dG, DNA oxidative damage). Data were analyzed by linear models for effects of boar and storage, correlations, and multivariate analysis as hierarchical clustering and principal component analysis (PCA). Storage reduced sperm quality parameters, mainly motility, with no critical oxidative stress increases, while chromatin status worsened slightly (%DFI and 8-oxo-dG increased while mBBr MFI and disulfide bridges decreased). Boar significantly affected most chromatin variables except for CMA3, with storage affecting most except %HDS. At day 0, sperm chromatin variables clustered closely, except for CMA3, and %HDS and 8-oxo-dG correlated with many variables (notably, mBBr). After storage, the relation between %HDS and 8-oxo-dG remained, but correlations among other techniques disappeared, and mBBr variables clustered separately. The PCA suggested a considerable influence of mBBr on sample variance, especially regarding storage, with SCSA and 8-oxo-dG affecting between-sample variability. Overall, CMA3 was the least informative, in contrast with results in other species. The combination of DNA fragmentation, DNA oxidation, chromatin compaction, and tiol status seems a good candidate for obtaining a complete picture of the pig sperm nucleus status, raising many questions for future molecular studies and deserving further research to establish its usefulness as fertility predictors in multivariate models. The meaning of CMA3 should be clarified.</span></p>
Sperm production and allocation in response to risks of sperm competition in the black soldier fly Hermetia illucens
<p>Dataset and R script used in the study: "Sperm production and allocation in response to risks of sperm competition in the black soldier fly Hermetia illucens".</p>
Data supporting: Molecular, behavioural and morphological comparisons of sperm adaptations in a fish with alternative mating tactics
<p>In species with alternative reproductive tactics, there is much empirical support that sneaker males have larger testes size and greater sperm numbers. However, support for higher sperm performance by sneakers is inconsistent. We used the sand goby (Pomatoschistus minutus) to test whether sperm performance differed between breeding-coloured males (small testes, but large mucus-filled sperm-duct glands; builds a nest lined with a sperm-containing mucus, provides care) and sneaker-morph males (no breeding colouration, large testes, rudimentary sperm-duct glands; no nest, no care). We compared motility (proportion motile sperm), velocity and longevity of sperm, between the two morphs. Furthermore, we compared gene expression of testes, and tested if the sperm-duct gland contents affected sperm performance, and if sperm morphometrics differed between male morphs. We found a clear difference in gene expression of testes between the male morphs with 109 transcripts differentially expressed between the morphs. Notably, several mucin genes were upregulated in breeding-coloured males and two ATP-related genes were upregulated in sneaker-morph males. There was some evidence of higher sperm velocity in sneaker-morph males, but no difference in sperm motility. Presence of the sperm-duct gland contents significantly increased sperm velocity, but equally so for the two morphs. The same was true for sperm motility although the difference was not significant. The sand goby has remarkably long-lived sperm, with only small or no decline in motility and velocity over time (5 min vs. 22 hours), but again, this was equally true for both morphs. Sperm length (head, tail, total) did not differ between morphs, and did not correlate with sperm velocity for either morph. Thus, other than a clear difference in testes gene expression, we found only modest differences between the two male morphs, confirming previous findings that high sperm performance as an adaptation to sperm competition is not a primary target of evolution.</p>
Sperm competition experiment with lake char (Lake Geneva 2017/18)
<p><span>Male and female wild lake char (</span><em>Salvelinus umbla</em>) <span>were sampled from Lake Geneva in December 2017 and December 2018. Male size and colouration (all samples, N = 34) were compared to milt characteristics. For the 2017 samples, m</span><span>ilt characteristics were also determined after sperm activation in diluted ovarian fluid or </span><span>water only, and the gametes were used in sperm competition trials:</span><span> Equal numbers of sperm competed for fertilization in the presence or absence of ovarian fluids. The resulting embryos were raised singly in an environment that supports symbiotic microbes (sublethal stress) or in a clean environment, and microsatellite markers were used to assign in total 1,464 embryos (from 70 experimental trials) to their fathers. Overall, the sperm of more colourful males were faster and reached higher fertilization success than the sperm of pale males. These differences were enhanced by the presence of ovarian fluids. The primary sex ratio did not differ among families and was about 1:1. Female embryos hatched on average later and showed lower stress tolerance than male embryos. There were significant parental effects on offspring growth and mortality, but the sex differences in embryo performance were not family-specific. Offspring of yellow males seemed less stress-tolerant than those of pale males, and embryo development was slowed down with increasing genetic similarity between the parents.</span></p>
Data from: Sperm metabolic rate predicts female mating frequency across Drosophila species
<p>Female mating rates vary widely, even among closely related species, but the reasons for this variation are not fully understood. Across <i>Drosophila </i>species, female mating frequencies are positively associated with sperm length. This association may be due in part to sperm limitation, with longer-spermed species transferring fewer sperm, or to cryptic female choice. However, a previously overlooked factor is sperm metabolic rate, which may correlate with sperm length. If faster-metabolizing sperm accumulate age-related cellular damage more quickly, then females should remate sooner to obtain fresh sperm. Alternatively, frequent female mating may select for increased sperm competitiveness via increased metabolism. Here, we measure sperm metabolism across 13 <i>Drosophila </i>species and compare these measures to published data on female mating rate and on sperm length. Using fluorescent lifetime imaging microscopy, we quantify NAD(P)H metabolism ex vivo, in intact organs. Phylogenetically controlled regression reveals that sperm metabolic rate is positively associated with sperm length and with female mating frequency. Path analysis shows sperm length driving sperm metabolism and sperm metabolism either driving or being driven by female mating rate. While the causal directionality of these relationships remains to be fully resolved, and the effect of sperm metabolism on sperm aging and/or sperm competitiveness remains to be established, our results demonstrate the importance of sperm metabolism in sexual selection.</p>
Supplementary data to "Alternative reproductive tactics are associated with sperm performance in invasive round goby from two different salinity environments"
<p>During male-male competition, evolution can favor alternative reproductive tactics. This often results in a dominant morph that holds a resource, such as a nest for egg laying, competes with a smaller sneaker morph that reproduces by stealing fertilizations. The salinity environment can influence male growth rates, e.g. via osmoregulatory costs, which in turn may influence the use of sneaker tactics for small males competing for mating opportunities. Salinity can also affect sperm directly; however, little is known of how salinity influences sneaker tactics through sperm performance. We sampled males of the invasive round goby (<i>Neogobius melanostomus</i>) from two environments, a freshwater river and a brackish estuary. This fish has two male morphs: nest-holding dark males and non-nest-holding light males. We examined the role of water salinity of 0, 8 and 16 on sperm performance and found that in estuarine males, a salinity of 0 reduced sperm velocity compared to a salinity of 8 and 16. Riverine males had low velocity in all salinities. Sperm viability also decreased by over 30 % in 0 salinity, compared to 8 and 16, for fish from both environments. Gobies produce ejaculate contents in specialized glands that could in theory shield sperm in an adverse environment. However, gland contents did not improve sperm performance in our tests. Body mass and age estimates indicate that riverine males invested more in somatic growth compared to estuarine males. Estuarine light morph males had a high enough gonadosomatic index to indicate sneaker tactics. We propose that when sperm performance is low, such as for the riverine males, sneaker tactics are ineffective, and will be selected against or phenotypically suppressed. Instead, we interpret the increased investment in somatic growth found in riverine males as a life-history decision that is advantageous when defending a nest in the next reproductive season.</p>
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