Sex ratio distorter reduces sperm competitive ability in an insect

Selfish genetic elements (SGEs) are ubiquitous in animals and often associated with low male fertility due to reduced sperm number in male carriers. In the fruit fly Drosophila pseudoobscura , the meiotic driving X chromosome "sex ratio" kills Y-bearing sperm in carrier males (SR males), resulting in female only broods. We competed SR males against the ejaculates of noncarrying standard males (ST males), and quantified the number of sperm transferred by SR and ST males to females. We show that SR males are very poor sperm competitors, which is partly related to transfer of fewer sperm during mating. However, sperm numbers alone cannot explain the observed paternity reduction, indicating SR males' sperm may be of reduced quality, possibly due to damage during the killing of the noncarrying Y-sperm. The reduction in sperm competitive ability due to SR is large enough to potentially stabilize the spread of sex ratio drive through populations. The poor sperm competitive ability of SR males coupled with their low fitness as mates could favor increased remating by females to reduce paternity by SR males. Given the generally poor performance of SGE-carrying males in sperm competition, this may generate strong selective pressure favoring polyandry in many species.     

Age-related sperm transfer and sperm competitive ability in the male hide beetle

The influence of male age on reproductive success after a singlemating has been explored widely; however, few studies have investigatedwhether quantitative or qualitative differences in male spermare responsible for the observed patterns. Moreover, the roleof male age on sperm competitive ability has been largely ignored.We examined the importance of male age on the probability andamount of sperm transferred during a single mating and exploredwhether sperm competitive ability varies with male age in thehide beetle Dermestes maculatus, a species where sperm viabilitydoes not vary with male age. We also investigated whether spermtransfer rates varied with female age. We found that the probabilityof sperm transfer and the amount of sperm transferred variedwith male, but not female, age. All males performed behaviorallysuccessful copulations, but intermediate-age and old males weremore likely to transfer sperm successfully and also transferreda greater quantity of sperm than young males. Old males wereless likely to transfer sperm than intermediate-age males, butif they did transfer sperm successfully, they transferred comparableamounts. Sperm competitive ability varied with male age andreflected the quantity of sperm transferred. On average, intermediate-agemales achieved greater fertilization success when competingagainst young or old males than when competing against otherintermediate-age males. Old males were poor competitors againstintermediate-age males, but they achieved significantly higherrates of fertilization when competing against young males. Ourfindings suggest that quantitative differences in the amountof sperm transferred determine male success in sperm competitionin the hide beetle.     

Nontransitivity of sperm precedence in Drosophila

Abstract.— Sperm competition is an important component of fitness in Drosophila , but we still do not have a clear understanding of the unit of selection that is relevant to sperm competition. Here we demonstrate that sperm competitive ability is not a property of the sperm haplotype, but rather of the diploid male's genotype. Then we test whether the relative sperm competitive ability of males can be ranked on a linear array or whether competitive ability instead depends on particular pairwise contests among males. Sperm precedence of six chromosome-extracted lines was tested against three different visible marker lines ( cn bw, bw^D , and Cy ), and the rank order of the six lines differed markedly among the mutant lines. Population genetic theory has shown that departures from transitivity of sperm precedence may be important to the maintenance of polymorphism for genes that influence sperm competitive ability. The non-transitivity seen in sperm precedence should theoretically increase the opportunity for polymorphism in genes that influence this phenotype.     

Autosomal variation for male body size and sperm competition phenotypes is uncorrelated in Drosophila melanogaster

Correlations between male body size and phenotypes impacting post-copulatory sexual selection are commonly observed during the manipulation of male body size by environmental rearing conditions. Here, we control for environmental influences and test for genetic correlations between natural variation in male body size and phenotypes affecting post-copulatory sexual selection in Drosophila melanogaster. Dry weights of virgin males from 90 second-chromosome and 88 third-chromosome substitution lines were measured. Highly significant line effects (p<0.001) documented a genetic basis to variation in male body size. No significant correlations were identified between male body size and the components of sperm competitive ability. These results suggest that natural autosomal variation for male body size has little impact on post-copulatory sexual selection. If genetic correlations exist between male body size and post-copulatory sexual selection then variation in the sex chromosomes are likely candidates, as might be expected if sexually antagonistic coevolution was responsible.     

Female sperm use and storage between fertilization events drive sperm competition and male ejaculate allocation

Sperm competition theory has traditionally focused on how male allocation responds to female promiscuity, when males compete to fertilize a single clutch of eggs. Here, we develop a model to ask how female sperm use and storage across consecutive reproductive events affect male ejaculate allocation and patterns of mating and paternity. In our model, sperm use (a single parameter under female control) is the main determinant of sperm competition, which alters the effect of female promiscuity on male success and, ultimately, male reproductive allocation. Our theory reproduces the general pattern predicted by existing theory that increased sperm competition favors increased allocation to ejaculates. However, our model predicts a negative correlation between male ejaculate allocation and female promiscuity, challenging the generality of a prevailing expectation of sperm competition theory. Early models assumed that the energetic costs of precopulatory competition and the level of sperm competition are both determined by female promiscuity, which leads to an assumed covariation between these two processes. By modeling precopulatory costs and sperm competition independently, our theoretical framework allows us to examine how male allocation should respond independently to variation in sperm competition and energetic trade‐offs in mating systems that have been overlooked in the past.     

Effect of male age on sperm traits and sperm competition success in the guppy (Poecilia reticulata)

Deleterious mutations can accumulate in the germline with age, decreasing the genetic quality of sperm and imposing a cost on female fitness. If these mutations also affect sperm competition ability or sperm production, then females will benefit from polyandry as it incites sperm competition and, consequently, minimizes the mutational load in the offspring. We tested this hypothesis in the guppy (Poecilia reticulata), a species characterized by polyandry and intense sperm competition, by investigating whether age affects post‐copulatory male traits and sperm competition success. Females did not discriminate between old and young males in a mate choice experiment. While old males produced longer and slower sperm with larger reserves of strippable sperm, compared to young males, artificial insemination did not reveal any effect of age on sperm competition success. Altogether, these results do not support the hypothesis that polyandry evolved in response to costs associated with mating with old males in the guppy.     

Similar mating and sperm displacement patterns in two highly divergent D. simulans populations from Africa and Europe

The frequency of remating in Drosophila melanogaster is affected by both genetic and ecological factors. We studied the remating behaviour in one European (Italy) and one African (Uganda) Drosophila simulans population using six highly polymorphic microsatellite markers. Despite that the populations were genetically distinct (F(ST) = 0.18) and originated from very dissimilar ecological settings with different population densities, we inferred a very similar mating pattern. The remating parameter alpha was similar in both populations (a = 1.3-1.4). No more than two distinct paternal genotypes per family were detected in each population.     

The Y chromosomes of Drosophila simulans are highly polymorphic for their ability to suppress sex-ratio drive

The sex-ratio trait, known in several species of Drosophila including D. simulans, results from meiotic drive of the X chromosome against the Y. Males that carry a sex-ratio X chromosome produce strongly female-biased progeny. In D. simulans, drive suppressors have evolved on the Y chromosome and on the autosomes. Both the frequency of sex-ratio X and the strength of the total drive suppression (Y-linked and autosomal) vary widely among geographic populations of this worldwide species. We have investigated the pattern of Y-linked drive suppression in six natural populations representative of this variability. Y-linked suppressors were found to be a regular component of the suppression, with large differences between populations in the mean level of suppression. These variations did not correspond to differences in frequency of discrete types of Y chromosomes, but to a more or less wide continuum of phenotypes, from nonsuppressor to partial or total suppressor. We concluded that a large diversity of Y-linked suppressor alleles exists in D. simulans and that some populations are highly polymorphic. Our results support the hypothesis that a Y-chromosome polymorphism can be easily maintained by a balance between meiotic drive and the cost of drive suppression.     

Multiple paternity and sperm competition in the sibling species Drosophila buzzatii and Drosophila koepferae

Sperm competition (SC) is a major component of sexual selection that enhances intra‐ and intersexual conflicts and may trigger rapid adaptive evolution of sexual characters. The actual role of SC on rapid evolution, however, is poorly understood. Besides, the relative contribution of distinctive features of the mating system to among species variation in the strength of SC remains unclear. Here, we assessed the strength of SC and mating system factors that may account for it in the closely related species Drosophila buzzatii and Drosophila koepferae. Our analyses reveal higher incidence of multiple paternity and SC risk in D. buzzatii wild‐inseminated females. The estimated number of fathers per brood was 3.57 in D. buzzatii and 1.95 in D. koepferae. In turn, the expected proportion of females inseminated by more than one male was 0.89 in D. buzzatii and 0.58 in D. koepferae. Laboratory experiments show that this pattern may be accounted for by the faster rate of stored sperm usage observed in D. koepferae and by the greater female remating rate exhibited by D. buzzatii. We also found that the male reproductive cost of SC is also higher in D. buzzatii. After a female mated with a second male, first‐mating male fertility was reduced by 71.4% in D. buzzatii and only 33.3% in D. koepferae. Therefore, we may conclude that postmating sexual selection via SC is a stronger evolutionary force in D. buzzatii than in its sibling.     

Divergent natural selection alters male sperm competition success in Drosophila melanogaster

Sexually selected traits may also be subject to non‐sexual selection. If optimal trait values depend on environmental conditions, then “narrow sense” (i.e., non‐sexual) natural selection can lead to local adaptation, with fitness in a certain environment being highest among individuals selected under that environment. Such adaptation can, in turn, drive ecological speciation via sexual selection. To date, most research on the effect of narrow‐sense natural selection on sexually selected traits has focused on precopulatory measures like mating success. However, postcopulatory traits, such as sperm function, can also be under non‐sexual selection, and have the potential to contribute to population divergence between different environments. Here, we investigate the effects of narrow‐sense natural selection on male postcopulatory success in Drosophila melanogaster. We chose two extreme environments, low oxygen (10%, hypoxic) or high CO₂ (5%, hypercapnic) to detect small effects. We measured the sperm defensive (P1) and offensive (P2) capabilities of selected and control males in the corresponding selection environment and under control conditions. Overall, selection under hypoxia decreased both P1 and P2, while selection under hypercapnia had no effect. Surprisingly, P1 for both selected and control males was higher under both ambient hypoxia and ambient hypercapnia, compared to control conditions, while P2 was lower under hypoxia. We found limited evidence for local adaptation: the positive environmental effect of hypoxia on P1 was greater in hypoxia‐selected males than in controls. We discuss the implications of our findings for the evolution of postcopulatory traits in response to non‐sexual and sexual selection.     

Male sperm donation consequences in single and double matings in Anisopteromalus calandrae

Abstract. The number of spermatozoa that a male transfers to the female during copulation is a main component of its individual fitness, especially under the pressure of sperm competition. This paper presents experimental results on the direct relationship between the male's sperm investment and its paternity in the offspring of dual-mated females. An eye colour mutant (red-eyed) is used to study the differences in the mating and fertilization abilities of males through observation of single and dual matings of females in Anisopteromalus calandrae (Hymenoptera, Chalcidoidea, Pteromalidae). Experimentally, females accept dual matings only in the simultaneous presence of two males. Counts of spermatozoa in the seminal vesicles of virgin males show that red-eyed males have more sperm than wild-eyed ones (approximately 1.46-fold greater). Red- and wild-eyed males do not differ in their mating behaviour and females mate indifferently with both phenotypes. Compared with once-mated females, double-mated females increase neither sperm storage nor lifetime fecundity, and the offspring sex ratio is female-biased. Females mated with two males of different phenotypes produce offspring of both phenotypes throughout their reproductive life, whatever the order of males in the copulation sequence. Any mating pattern appears to produce more red- than wild-eyed offspring (between 1.45- and 1.88-fold greater). Thus, proportions of offspring of each male match the proportions of their sperm potential. With no preference of female for red-eye or wild-eye males being demonstrated at either behavioural or physiological levels, a male's investment in sperm quantity appears to determine its individual reproductive success, at least in these experimental conditions.     

Sperm competition and sperm precedence in the dragonfly Nanophya pygmaea

Abstract. The libellulid dragonfly, Nanophya pygmaea Rambur, has an average ejaculate volume of 0.16 mm³. During successive copulations the volume of sperm stored in the female's sperm storage organs increases in steps equivalent to this volume, suggesting that the sperm competition mechanism in this species is sperm repositioning, i.e. adding an ejaculate to what is already present in the female's sperm storage organ. By using sterile/normal males in double matings with females we have shown that this mechanism results in last male sperm precedence (P²= 0.979).     

Intraspecific sperm competition genes enforce post-mating species barriers in Drosophila

Sexual selection and sexual conflict are considered important drivers of speciation, based on both theoretical models and empirical correlations between sexually selected traits and diversification. However, whether reproductive isolation between species evolves directly as a consequence of intrapopulation sexual dynamics remains empirically unresolved, in part because knowledge of the genetic mechanisms (if any) connecting these processes is limited. Here, we provide evidence of a direct mechanistic link between intraspecies sexual selection and reproductive isolation. We examined genes with known roles in intraspecific sperm competition (ISC) in D. melanogaster and assayed their impact on conspecific sperm precedence (CSP). We found that two such genes (Acp36DE and CG9997) contribute to both offensive sperm competition and CSP; null/knockdown lines both had lower competitive ability against D. melanogaster conspecifics and were no longer able to displace heterospecific D. simulans sperm in competitive matings. In comparison, Sex Peptide (Acp70A)—another locus essential for ISC—does not contribute to CSP. These data indicate that two loci important for sperm competitive interactions have an additional role in similar interactions that enforce post-mating reproductive isolation between species, and show that sexual selection and sexual isolation can act on the same molecular targets in a gene-specific manner.     

Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

Sex-ratio distortion in Drosophila simulans: co-occurence of a meiotic drive and a suppressor of drive

A sex-ratio distortion factor was found at high frequency in D. simulans strains from Seychelles and New Caledonia. This factor is poorly or not expressed within those strains which are resistant to it. Its presence was detected by crossing females from New Caledonia or the Seychelles with males from a different geographic origin. Most of the F1 males obtained produced an excess of females (up to 99%) in their progeny. The two strains are infected with Wolbachia, but these micro-organisms are not involved in the sex-ratio distortion. The sex-ratio factor is shown to be an X-linked meiotic driver; nuclear resistance factor(s) act by suppressing the drive. It is likely that the same X-located driver invaded the two populations, which subsequently developed resistance factor(s) against it.     

Fitness consequences of redundant cues of competition in male Drosophila melanogaster

Phenotypic plasticity can allow animals to adapt their behavior, such as their mating effort, to their social and sexual environment. However, this relies on the individual receiving accurate and reliable cues of the environmental conditions. This can be achieved via the receipt of multimodal cues, which may provide redundancy and robustness. Male Drosophila melanogaster detect presence of rivals via combinations of any two or more redundant cue components (sound, smell, and touch) and respond by extending their subsequent mating duration, which is associated with higher reproductive success. Although alternative combinations of cues of rival presence have previously been found to elicit equivalent increases in mating duration and offspring production, their redundancy in securing success under sperm competition has not previously been tested. Here, we explicitly test this by exposing male D. melanogaster to alternative combinations of rival cues, and examine reproductive success in both the presence and absence of sperm competition. The results supported previous findings of redundancy of cues in terms of behavioral responses. However, there was no evidence of reproductive benefits accrued by extending mating duration in response to rivals. The lack of identifiable fitness benefits of longer mating under these conditions, both in the presence and absence of sperm competition, contrasted with some previous results, but could be explained by (a) damage sustained from aggressive interactions with rivals leading to reduced ability to increase ejaculate investment, (b) presence of features of the social environment, such as male and female mating status, that obscured the fitness benefits of longer mating, and (c) decoupling of behavioral investment with fitness benefits.     

Pattern of sperm transfer in redback spiders: implications for sperm competition and male sacrifice

Many sperm competition studies have identified copulation durationas an important predictor of paternity. This result is ofteninterpreted as a sperm transfer effect—it is assumed thatsperm transfer is limited by copulation duration. Here we testthe assumption of duration-dependent sperm transfer in the Australianredback spider, Latrodectus hasselti, in which a correlationbetween copulation duration and paternity has been implicatedin the evolution of a rare male self-sacrifice behavior. Maleredbacks facilitate sexual cannibalism by females during copulation.Sexual cannibalism is apparently adaptive for redback males,in part because it results in longer copulations (25 versus11 min.), and copulation duration is positively correlated withpaternity. We assessed sperm transfer in normal copulationsand in copulations that we terminated at 5, 10, or 20 min. Ourresults show that the paternity advantage of sexual cannibalismis not owing to time-dependent sperm transfer, as redback malestransfer the majority of their sperm within the first 5 minof copulation. This suggests that the link between copulationduration and paternity may instead be owing to cryptic femalechoice or the transfer of nongametic ejaculatory substances.Results further indicate that the act of cannibalism itselfmight play a role in mediating sperm transfer. This study highlightsthe importance of understanding mechanisms of sperm transferwhen attempting to interpret the outcome of sperm competitionstudies.