Intensity Of Sperm Competition Research Articles

Attempted copulatory behaviour between two phylogenetically unrelated alien species (Coypu, Myocastor coypus, and Pond slider, Trachemys scripta): first evidence

We report the first case of sexual interaction between two phylogenetically unrelated species (coypu Myocastor coypus and pond slider Trachemys scripta, a freshwater pond turtle), both of them non-native in the study area, a remnant coastal wetland of Tyrrhenian, central Italy (41°57'34.0''N 12°02'58.0''E). We inductively propose two different hypotheses (masturbatory act due to intense sperm competition, or behaviour induced by female pheromones) to explain this peculiar observation.

Within-population sperm competition intensity does not predict asymmetry in conpopulation sperm precedence.

Postcopulatory sexual selection can generate evolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilization success diverge between populations, postmating prezygotic (PMPZ) barriers to gene flow may evolve. Conspecific sperm precedence is a form of PMPZ isolation thought to evolve early during speciation yet has mostly been studied between species. Here, we show conpopulation sperm precedence (CpSP) between Drosophila montana populations. Using Pool-seq genomic data we estimate divergence times and ask whether PMPZ isolation evolved in the face of gene flow. We find models incorporating gene flow fit the data best indicating populations experienced considerable gene flow during divergence. We find CpSP is asymmetric and mirrors asymmetry in non-competitive PMPZ isolation, suggesting these phenomena have a shared mechanism. However, we show asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilization success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of PMPZ isolation. We suggest that instead cryptic female choice or mutation-order divergence may drive divergence of postcopulatory phenotypes resulting in PMPZ isolation.This article is part of the theme issue ‘Fifty years of sperm competition’.

Male body size does not affect the refractory period of females in the West Indian sweet potato weevil Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae) and the seed bug Togo hemipterus (Scott) (Heteroptera: Lygaeidae)

Multiple mating by females increases both the risk and intensity of sperm competition for males. The ability to temporarily or permanently inhibit female receptivity to further mating represents a highly adaptive strategy to reduce the risk of sperm competition. Males of the West Indian sweet potato weevil Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae) and the seed bug Togo hemipterus (Scott) (Heteroptera: Lygaeidae) use accessory gland substances to inhibit remating in females. It is known that there is variance in the length of the female refractory period (i.e., the effectiveness of male ejaculate substances that inhibit female remating) within a species. However, it is unclear what types of male traits affect the length of the female refractory period. The mechanism of the female refractory period is not sufficiently revealed. We focused on male body size, which is often a target of sexual selection, and investigated the relationship between male body size and both the refractory period of females and mating duration. Contrary to our thought, male body size did not significantly influence the refractory period of females or mating duration in either species. Smaller male body size was not particularly favored by post-copulatory sexual selection in either species.

Trade-offs of strategic sperm adjustments and their consequences under phenotype–environment mismatches in guppies

In polyandrous species males invest significant resources in producing large and high-quality ejaculates. As ejaculates are costly, males are expected to modulate their investment in response to social cues associated with the expected level of sperm competition or mating opportunity, to anticipate future mating conditions. Another consequence of ejaculate costs is that the increase in ejaculate production may be traded against traits linked to mate acquisition. In such cases, the effect of this anticipatory plasticity in ejaculate investment on a male's reproductive success will depend on the balance between postcopulatory benefits and precopulatory costs in the sociosexual context subsequently encountered. Here, we used the guppy, Poecilia reticulata, a live-bearing fish characterized by intense sperm competition, to investigate how mismatches between anticipatory phenotypes and the social conditions subsequently experienced affect male reproductive success. Male guppies kept in visual contact with females, a social stimulus predicting high mating opportunities, increase their sperm production compared to female-deprived males which foresee fewer opportunities to mate, but simultaneously reduce their courtship rate. Using a paired experimental design, we manipulated the male's perceived mating opportunities by housing them in the presence (FP) or in the absence (FA) of females. We then measured male mating and insemination success under two conditions: (1) a female-biased sex ratio, matching expected FP cues; and (2) a male-biased sex ratio, matching expected FA cues. Under a female-biased sex ratio, mating and insemination success were not affected by previous exposure to females, although FP males experienced a lower risk of sperm depletion after several copulations. However, FP males showed a small, but significant, reduction in their mating success under a male-biased sex ratio, when directly competing with an FA male. Males showed significant repeatability in mating and insemination success within a sex ratio context, suggesting that the costs of mismatching anticipatory ejaculate responses are probably low in this species.

Effects of two seminal fluid transcripts on post-mating behaviour in the simultaneously hermaphroditic flatworm Macrostomum lignano.

The seminal fluid proteins (SFPs) transferred to mating partners along with sperm often play crucial roles in mediating post-mating sexual selection. One way in which sperm donors can maximize their own reproductive success is by modifying the partner's (sperm recipient's) post-copulatory behaviour to prevent or delay re-mating, thereby decreasing the likelihood or intensity of sperm competition. Here, we adopted a quantitative genetic approach combining gene expression and behavioural data to identify candidates that could mediate such a response in the simultaneously hermaphroditic flatworm Macrostomum lignano. We identified two putative SFPs-Mlig-pro46 and Mlig-pro63-linked to both mating frequency and 'suck' frequency, a distinctive behaviour, in which, upon ejaculate receipt, the worm places its pharynx over its female genital opening and apparently attempts to remove the received ejaculate. We, therefore, performed a manipulative experiment using RNA interference-induced knockdown to ask how the loss of Mlig-pro46 and Mlig-pro63 expression, singly and in combination, affects mating frequency, partner suck propensity and sperm competitive ability. None of the knockdown treatments impacted strongly on the mating frequency or sperm competitive ability, but knockdown of Mlig-pro63 resulted in a significantly decreased suck propensity of mating partners. This suggests that Mlig-pro63 may normally act as a cue in the ejaculate to trigger recipient suck behaviour and-given that other proteins in the ejaculate have the opposite effect-could be one component of an ongoing arms race between donors and recipients over the control of ejaculate fate. However, the adaptive significance of Mlig-pro46 and Mlig-pro63 from a donor perspective remains enigmatic.

Differential gene regulation in selected lines for high and low sperm production in male guppies.

In species where females mate with more than one male during the same reproductive event, males typically increase the number of sperm produced to boost their fertilization share. Sperm is not limitless, however, and theory predicts that their production will come at the cost of other fitness-related traits, such as body growth or immunocompetence, although these evolutionary trade-offs are notoriously difficult to highlight. To this end, we combined artificial selection for sperm production with a transcriptome analysis using Poecilia reticulata, a fish characterized by intense sperm competition in which the number of sperm transferred during mating is the most important predictor of fertilization success, yet sperm production is highly variable among males. We compared the brain and testes transcriptome in male guppies of lines artificially selected for high and low sperm production by identifying pivotal differentially expressed gene sets that may regulate spermatogenesis and immune function in this species. Despite the small differences in single genes' expression, gene set enrichment analysis showed coordinated gene expression differences associated with several pathways differentially regulated in the two selection lines. High sperm production males showed an upregulation of pathways related to immunosuppression and development of spermatozoa indicating a possible immunological cost of sperm production.

Estimating a Key Parameter of Mammalian Mating Systems: The Chance of Siring Success for a Mated Male.

Studies of multiple paternity in mammals and other animal species generally report proportion of multiple paternity among litters, mean litter sizes, and mean number of sires per litter. It is shown how these variables can be used to produce an estimate of the probability of reproductive success for a male that has mated with a female. This estimate of male success is more informative about the mating system that alternative measures, like the proportion of litters with multiple paternity or the mean number of sires per litter. The probability of success for a mated male can be measured both theoretically and empirically, and gives an estimate of the intensity of sperm competition and of a male's "confidence of paternity" upon mating. The probability of success for mated males for ten "exemplar" species of mammals is estimated and they are compared for insights into the functioning of their mating systems.

Impact of low sperm competition on male reproductive trait allometries in a bush-cricket

BackgroundStudying reproductive trait allometries can help to understand optimal male investment strategies under sexual selection. In promiscuous mating systems, studies across several taxa suggest that testes allometry is usually positive, presumably due to strong selection on sperm numbers through intense sperm competition. Here, we investigated testes allometry in a bush-cricket species, Metaplastes ornatus, in which females mate promiscuously, but where sperm removal behaviour by males likely drastically reduces realised sperm competition level.ResultsAs hypothesised, we found evidence for negative testes allometry and hence a fundamentally different male investment strategy compared to species under intense sperm competition. In addition, the mean relative testes size of M. ornatus was small compared to other species of bush-crickets. Surprisingly, the spermatophore gland, a potential alternative trait that males could invest in instead of testes, also did not show positive allometry, but was approximately isometric. We further observed the expected pattern of negative allometry for the male morphological structure responsible for sperm removal in this species, the subgenital plate, supporting the one-size-fits-all hypothesis for intromittent genitalia.ConclusionOur findings suggest that the evolution of sperm removal behaviour in M. ornatus was a key adaptation for avoiding sperm competition, with important consequences for reproductive trait allometries. Nevertheless, they also imply that it does not pay for larger males to invest disproportionately in nuptial gift production in this species.

Divergent allocation of sperm and the seminal proteome along a competition gradient in Drosophila melanogaster

Sperm competition favors large, costly ejaculates, and theory predicts the evolution of allocation strategies that enable males to plastically tailor ejaculate expenditure to sperm competition threat. While greater sperm transfer in response to a perceived increase in the risk of sperm competition is well-supported, we have a poor understanding of whether males (i) respond to changes in perceived intensity of sperm competition, (ii) use the same allocation rules for sperm and seminal fluid, and (iii) experience changes in current and future reproductive performance as a result of ejaculate compositional changes. Combining quantitative proteomics with fluorescent sperm labeling, we show that Drosophila melanogaster males exercise independent control over the transfer of sperm and seminal fluid proteins (SFPs) under different levels of male-male competition. While sperm transfer peaks at low competition, consistent with some theoretical predictions based on sperm competition intensity, the abundance of transferred SFPs generally increases at high competition levels. However, we find that clusters of SFPs vary in the directionality and sensitivity of their response to competition, promoting compositional change in seminal fluid. By tracking the degree of decline in male mating probability and offspring production across successive matings, we provide evidence that ejaculate compositional change represents an adaptive response to current sperm competition, but one that comes at a cost to future mating performance. Our work reveals a previously unknown divergence in ejaculate component allocation rules, exposes downstream costs of elevated ejaculate investment, and ultimately suggests a central role for ejaculate compositional plasticity in sexual selection.

Female remating rate and pattern of sperm use suggest intense sperm competition in Drosophila antonietae (Diptera: Drosophilidae)

Sperm competition is conceived as a powerful selective force which acts on genes related to reproduction, promoting the evolution of reproductive adaptations and inter-population divergence that may ultimately lead to speciation. Such selective pressure is believed to be particularly strong in species from the Drosophila repleta group since females of most of these species are highly promiscuous. However, sperm competition is determined by many other factors far less explored than female remating rate; consequently, its actual intensity as a selective pressure continues to remain unknown across most taxa. In this paper, we aim to estimate the intensity of sperm competition in Drosophila antonietae, a South American species from the D. repleta group, by means of behavioural and genetic analyses. In sum, our results, while failing to reveal sperm precedence in twice-mated females, show that sperm competition is likely to occur and may strongly reduce males’ reproductive output. In addition, using highly polymorphic microsatellite loci, we confirmed a high incidence of multiple paternity in wild-inseminated females. We discuss the results within an evolutionary context comparing the mating system between D. antonietae and closely related species.

At the invasion front, male cane toads (Rhinella marina) have smaller testes.

As a colonizing species expands its range, individuals at the invasion front experience different evolutionary pressures than do those at the range-core. For example, low densities at the edge of the range mean that males should rarely experience intense sperm competition from rivals; and investment into reproduction may trade-off with adaptations for more rapid dispersal. Both of these processes are predicted to favour a reduction in testis size at the invasion front. To explore effects of invasion stage in Australian cane toads (Rhinella marina), we collected and dissected 214 adult males from three regions: one in the species' range-core (northeastern Australia), and two from invasion fronts (one in northwestern Australia and one in southeastern Australia). Despite the brief duration of separation between toads in these areas (approx. 85 years), testis masses averaged greater than 30% higher (as a proportion of body mass) in range-core males than in conspecifics sampled from either vanguard of the invasion. Previous work has documented low reproductive frequencies in female cane toads at the invasion front also, consistent with the hypothesis that evolutionary and ecological pressures unleashed by an invasion can favour relatively low resource allocation to reproduction in both sexes.

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.

Silk‐ and volatile‐based male mate choice in the genital plug‐producing spider

AbstractFemale mating history can have a strong effect on male fertilization success. Although males often prefer to mate with virgin females, they often also engage with mated females. As the intensity of sperm competition can differ among mated females, males are expected to evolve means to identify their status. In spiders, males often use female silk to gather information about female quality. Males of many spider species deposit mating plugs into female genitalia to hinder further copulations. We tested whether males of the foliage‐dwelling, plug‐producing spider Philodromus cespitum, which is an important natural enemy of pests, discriminate between females of different mating status and whether they can determine the extent of genital plugging in mated females solely on the basis of cues gained from deposited female silk. We presented males with draglines of females that varied in either mating status (virgin vs. mated), the extent of plugging (small vs. big plug), or the age of the plug (fresh vs. old plug) and examined their mate preferences. Additionally, we tested whether males were attracted to volatile cues produced by female bodies. Our experiments revealed that males preferred draglines of virgin females to those of mated females, and mated females with small plugs to those with large plugs. They were also attracted to female volatile cues. This study suggests that males are able to extract fine‐scale information on mating status from female draglines.

Male semelparity and multiple paternity confirmed in an arid‐zone dasyurid

AbstractA fifth of all species in the carnivorous‐insectivorous marsupial family Dasyuridae show obligate male semelparity (die‐off), where males die after their first mating season, but females may breed in more than one season. Life history strategies of many species in the genera Antechinus and Phascogale are well known, but the other dasyurid genus with apparently obligately semelparous males, Dasykaluta, is poorly known, and there have been no demographic studies of this monotypic genus in the wild. Both sexes in Antechinus and Phascogale species are highly polygamous. Comparative and experimental tests of insectivorous marsupials indicate that this polygamy is linked to the evolution of semelparity in more strongly seasonal breeders, through intense sperm competition. We assessed whether the kaluta (Dasykaluta rosamondae), a small dasyurid endemic to the broader Pilbara region of Western Australia, has obligate male semelparity, multiple paternity within litters, and positive testis allometry in the wild. We documented complete die‐off of males over two breeding seasons. Multiple paternity was confirmed in seven of eight litters, where either two or three fathers sired young. The seven young in the remaining litter appeared to be sired by one male. Intraspecific positive testis allometry was found in adult males. We conclude that the life history strategies of wild male and female kalutas are consistent with those of the two other genera of dasyurids with obligate male semelparity (Antechinus and Phascogale), and sperm competition is likely to be important in the mating system of kalutas. Our results show that male obligate semelparity has evolved twice in dasyurids.

Small, Variable Sperm in a Barn Swallow Population with Low Extra-Pair Paternity

Sperm competition can theoretically affect sperm morphology; however, it remains unclear whether and how sperm morphology tracks the intensity of sperm competition in each population. The barn swallow Hirundo rustica is a model species used in the study of sexual selection, and exhibits considerable variation in extra-pair paternity (percentage extra-pair young, ca. 3-30%) among populations. In the Joetsu population of the barn swallow, extra-pair paternity is virtually absent (< 3%), providing a rare opportunity to study sperm morphology under limited sperm competition, and to compare it with those reported in populations with frequent extra-pair paternity (>15%). We found that head, midpiece, and total sperm length were significantly shorter in the Joetsu population than in populations with frequent extra-pair paternity. Moreover, the variability in total sperm length, measured as the coefficient of variation in the Joetsu population, was twice as high as that of populations with frequent extra-pair paternity. These results are consistent with a positive, directional, and stabilizing effect of sperm competition on sperm morphology. Together with previous studies in populations with frequent extra-pair paternity, the current study provides one of few sets of evidence to show a link between the intensity of sperm competition and the mean and variance of sperm morphology within a wild bird species.

Sexual selection and ageing: interplay between pre- and post-copulatory traits senescence in the guppy.

Traits associated with mating and fertilization success are expected to senesce with age, but limited information is available on their relative rates of senescence. In polyandrous species, male reproductive fitness depends on both mating and fertilization success. Because successful mating is a prerequisite for post-copulatory sexual selection, ejaculate traits are expected to senesce faster than pre-copulatory traits, as pre-copulatory sexual selection is often deemed to be stronger than post-copulatory sexual selection. This pattern has generally been found in the few empirical studies conducted so far. We tested this prediction in the guppy ( Poecilia reticulata), a livebearing fish characterized by intense sperm competition, by comparing the expression of male sexual traits at two ages (four and nine months). Contrary to prediction, we found that post-copulatory traits senesced at a significantly slower rate than pre-copulatory traits. We also looked at whether early investment in those sexual traits affects longevity, and the interaction between sperm age (duration of sperm storage inside the male) and male age. Our results suggest that the relative senescence rate of pre- and post-copulatory sexual traits may vary among species with different mating systems and ecology.

Intraspecific morphological variation of the sperm storing organ in two hermaphroditic land snail species

BackgroundPostcopulatory sexual selection is very important in species with reproductive strategies that involve multiple mating and prolonged sperm storage. The sperm storage organ has been hypothesized to evolve in response to different levels of sperm competition in several species while population density has been considered as a factor that approximates sperm competition risk and intensity in the field. Apart from population density, local microclimatic conditions may also play a role in determining sperm competition levels in natural populations of land snails by affecting their chances of encountering mates. The goal of this study was to investigate the variation of the structure of the sperm storage organ in the simultaneously hermaphroditic land snails Helix lucorum and Cepaea vindobonensis occurring sympatrically in two sites which differed in habitat humidity. The populations of both species from the two sites, also differed in density and in duration of reproductive period. Multiple samples were taken from each population in order to test for temporal variation.ResultsIn both species, the spermatheca consisted of a simple fertilization chamber and a variable number of lateral tubules. The length of the spermatheca showed no temporal or spatial differentiation nor did it show any correlation with snail size. The number of tubules in Helix lucorum ranged from five to sixteen and in Cepaea vindobonensis from one to eight and in both species a significant difference of this trait between the two study sites was detected. In Cepaea vindobonensis, the difference in tubule number led to difference of the total tubule length which reflects sperm storage capacity of the spermatheca but this was not the case with H. lucorum in which no increase in total tubule length was detected.ConclusionsIntraspecific variation in the spermatheca was observed in both snail species studied. The variation observed was independent of snail size, and reproduction status, while the two species responded differently to higher sperm competition levels.

Testes size increases with sperm competition risk and intensity in bony fish and sharks

Female multiple mating provides the opportunity for sexual selection to continue after gamete release, generating strong selection on male reproductive traits. In particular, in species where femal ...

Interspecific diversity of testes mass and sperm morphology in the Philippine chrotomyine rodents: implications for differences in breeding systems across the species.

The high diversity of native Philippine murid rodents includes an old endemic group, the chrotomyines, which are the sister group of the Australasian hydromyines. Herein we detail their interspecific diversity of relative testes mass (RTM) and sperm morphology. We find that in chrotomyines, as in the Australasian hydromyines, testes mass relative to body mass differs by an order of magnitude across the species and ranges from a large RTM in Soricomys and Chrotomys species to a small RTM in Apomys. Sperm morphology is associated with these findings, with individuals in species of Soricomys and Chrotomys producing relatively larger spermatozoa with a prominent apical hook and long tail, whereas, by contrast, the Apomys species have a sperm head that either has a very short or no apical hook and a shorter tail. These findings indicate coevolution of RTM with sperm morphological traits across the species, with the marked interspecific differences in RTM suggesting differences in the intensity of intermale sperm competition and hence breeding system. Thus, we hypothesise that species of Soricomys and Chrotomys that produce more streamlined spermatozoa with longer tails have a polyandrous or promiscuous mating system, whereas the Apomys species, which produce smaller and less streamlined spermatozoa, may exhibit monogamy.

No support for cryptic choice by ovarian fluid in an external fertilizer.

Whether the ovarian fluid (OF) represents a selective environment influencing cryptic female choice was tested using an external fertilizer experiencing intense sperm competition and large effects of OF on sperm swimming behavior—the Arctic charr (Salvelinus alpinus). We physically separated the OF from the eggs of reproductively active females and reintroduced either their own OF or fluid from another female to the eggs. The eggs were then fertilized in vitro in a replicated split‐brood design with sperm from two males under synchronized sperm competition trials, while also measuring sperm velocity of the individual males in the individual OFs. We found large effects of males, but no effect of females (i.e., eggs) on paternity, determined from microsatellites. More important, we found no effect of OF treatments on the relative paternity of the two competing males in each pair. This experimental setup does not provide support for the hypothesis that OF plays an important role as medium for cryptic female choice in charr. Power analyses revealed that our sample size is large enough to detect medium‐sized changes in relative paternity (medium‐sized effect sizes), but not large enough to detect small changes in relative paternity. More studies are needed before a conclusion can be drawn about OF's potential influence on paternity under sperm competition—even in charr.