Patterns of sperm precedence and predictors of paternity in the Trinidadian guppy

Despite its widespread occurrence in animals, sperm competition has been studied in a limited range of taxa. Among the most neglected groups in this respect are internally fertilizing fish in which virtually nothing is known about the dynamics of sperm competition. In this study, we examined the outcome of sperm competition when virgin female guppies mated with two males. Behavioural cues were used to ensure that each male mated once (with female cooperation) and that sperm were successfully inseminated at copulation. Two polymorphic microsatellite loci were used to estimate the proportion of offspring sired by the second male (P2) and the results revealed a bimodal distribution with either first or (more often) second male priority The observed P2 distribution differed from that expected under the 'fair raffle' model of sperm competition. Random sperm mixing is therefore unlikely to account for the observed variance in P2 in this study. A further aim of our study was to identify predictors of male reproductive success. Using logistic linear modelling, we found that the best predictors of paternity were time to remating and the difference in courtship display rate between first and second males. Males that mated quickly and performed relatively high numbers of sigmoid displays obtained greater parentage than their slower and less vigorous counterparts. Since females are attracted to high-displaying males, our results suggest that female choice may facilitate sperm competition and/or sperm choice in guppies.     

Population density influences male-male competition in guppies

This study tested the general prediction that population density affects male-male competition, female mate choice and the opportunity for sexual selection. By manipulating the density of guppies, Poecilia reticulata, while keeping the sex ratio constant, I found that male mating tactics were phenotypically plastic with respect to density. As density increased, males decreased their courtship displays. Male-male competition and mate searching were highest at intermediate densities. Population density had no significant effect on the total number of copulations, copulatory tactics or the percentage of postcopulatory guarding. Female preference for males with a higher percentage of orange coloration was similar at all density levels. The 'opportunity for sexual selection', which estimates the upper limit to which a selected trait can shift if directional selection is operating and was calculated as the variance in number of copulations per male divided by the square of the mean number of copulations, was negatively associated with population density. This may be due to the decrease in male-male competition at high density rather than female preference which was similar across density treatments. Copyright 1999 The Association for the Study of Animal Behaviour.     

Sperm transfer through forced matings and its evolutionary implications in natural guppy (Poecilia reticulata ) populations

In species in which individuals alternate between mating strategies, males may respond to elevated predation risk by switching from conspicuous courtship displays to less risky or more profitable sneaky mating attempts. As a consequence, in such species female choice is likely to be undermined more frequently in relatively dangerous localities. We tested this prediction using the guppy, a species of fish in which individual males alternate between courtship (solicited) and forced (unsolicited) copulations according to prevailing levels of predation. We collected females at late stages of gestation from four high- and four low-predation populations in Trinidad and examined them for the presence of sperm in their gonoducts. Due to the patterns of sperm storage in guppies, sperm found in the gonoducts of such late-cycle females can only arise from unsolicited copulations. We anticipated that because female guppies are subject to greater sexual harassment in the form of forced mating attempts in high-risk localities, a higher proportion of females in these populations would contain sperm in their gonoducts arising from recent unsolicited copulations. Contrary to this prediction, only one of the four paired comparisons (from the Quaré River) revealed a significant difference in the proportion of females recently inseminated through forced copulations. The paired comparisons for the remaining three rivers revealed no significant differences in the proportion of females with recoverable sperm in their gonoducts. However, overall, we found that 44.5% (±4.3 SE) of females had sperm in their gonoduct arising from sneaky mating, a figure three times higher than previously reported for this species. We discuss these findings in relation to recent predictions concerning the strength of sexual selection in natural populations.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78 , 605–612.     

Strategic ejaculation in the common dung fly Sepsis cynipsea

Sperm competition has been a major selective force acting on male and female behaviour. Theory predicts that when sperm compete numerically, selection will favour males that vary the number of sperm they transfer with sperm competition risk. This often leads to increased copula duration when sperm competition risk is high, the selective advantage of which is increased paternity. We investigated the copulatory behaviour of the common dung fly Sepsis cynipsea in relation to male and female size, female mating status, age, and presence or absence of dung. This fly is unusual in that males mate-guard before copula while females use the sperm of previous males for their current clutch. Body size had no effect on copula duration, but duration of first copulations depended on female age, with older females having longer copulations. For females that copulated twice, there was an interaction between female age and mating status influencing copula duration: old females had longer copulations than young females, but second copulas were longer for young females. Residual testis size of nonvirgin males was smaller than for virgins, and testis shrinkage was significantly associated with copula duration, which indicates that males transfer more ejaculate with longer copulations. We therefore conclude that copulation duration and ejaculate transfer vary in accordance with sperm competition theory.     

Male scorpionflies assess the amount of rival sperm transferred by females' previous mates

Theory predicts that when sperm compete numerically, selection will favor males who vary the number of sperm they transfer with the immediate level of sperm competition. In this study, I measured male mating investment in response to both female mating status (virgin vs. mated) and the number of foreign sperm stored by females in a previous mating in the scorpionfly Panorpa cognata. Female sperm storage was manipulated by interrupting copulations at different time points. Female mating status did not significantly influence male mating investment, but resource-limited males invested strategically in relation to the amount of sperm stored by females in a previous mating. I found continuously decreasing male investment in response to increasing amounts of competing sperm. These results demonstrate an unprecedented male ability to assess the number of sperm stored by females. As a result, males are capable of an extraordinarily fine-tuned reaction to the intensity of sperm competition.     

The copulatory plug delays ejaculation by rival males and affects sperm competition outcome in house mice

Females of many species mate with multiple males (polyandry), resulting in male–male competition extending to post‐copulation (sperm competition). Males adapt to such post‐copulatory sexual selection by altering features of their ejaculate that increase its competitiveness and/or by decreasing the risk of sperm competition through female manipulation or interference with rival male behaviour. At ejaculation, males of many species deposit copulatory plugs, which are commonly interpreted as a male adaptation to post‐copulatory competition and are thought to reduce or delay female remating. Here, we used a vertebrate model species, the house mouse, to study the consequences of copulatory plugs for post‐copulatory competition. We experimentally manipulated plugs after a female's first mating and investigated the consequences for rival male behaviour and paternity outcome. We found that even intact copulatory plugs were ineffective at preventing female remating, but that plugs influenced the rival male copulatory behaviour. Rivals facing intact copulatory plugs performed more but shorter copulations and ejaculated later than when the plug had been fully or partially removed. This suggests that the copulatory plug represents a considerable physical barrier to rival males. The paternity share of first males increased with a longer delay between the first and second males' ejaculations, indicative of fitness consequences of copulatory plugs. However, when males provided little copulatory stimulation, the incidence of pregnancy failure increased, representing a potential benefit of intense and repeated copulation besides plug removal. We discuss the potential mechanisms of how plugs influence sperm competition outcome and consequences for male copulatory behaviour.     

Male display rate reveals ejaculate characteristics in the Trinidadian guppy,Poecilia reticulata.

Previous work (Reynolds and Gross 1992) has demonstrated that mate choice enables female guppies, Poecilia reticulata, to obtain heritable benefits (''good genes'') for their offspring. It is not yet known whether males also signal their functional fertility, that is, their viability as fathers, to female guppies. Our study tested the hypothesis that a male''s behaviour reveals characteristics of his ejaculate. We uncovered a strong correlation between display rate and sperm number in male guppies derived from two wild Trinidadian populations. This result indicates that information on the functional fertility of potential mates is available to females. However, our investigation also found a significant relationship between the frequency of sneaky mating and sperm number. Female guppies in wild populations, particularly those experiencing a high predation regime, are constantly subjected to sneaky mating attempts. As the males responsible for these sneaky matings have highest reserves of sperm they may have the capacity to undermine female choice. The implications of these findings for sperm competition are discussed.     

Polygynandry,face-to-face copulation and sperm competition in the Hihi Notiomystis cincta (Aves: Meliphagidae)

The Hihi or Stitchbird Notiomystis cincta breeding system is highly variable and includes monogamy, polyandry, polygyny and polygynandry. Males have large testes (4.2% of body mass), very large numbers (1460 × 10⁶) of sperm in their seminal glomera and an unusually enlarged cloacal protuberance. These features are also found in other species with highly variable mating systems where males are under intense sperm competition. Hihi copulate in two different positions: face to face and, more conventionally, with the male on the female's back. Face-to-face copulation is unique among birds and appears to be a form of forced copulation. The presence of enlarged cloacas in both sexes could aid the transfer of sperm. Both male and female Hihi appear to benefit from a mixed reproductive strategy where a female Hihi can solicit copulations from males other than her partner and male Hihi can perform extra-pair copulations both with willing females or by forced copulation.     

Male sexual harassment alters female social behaviour towards other females

Male harassment of females to gain mating opportunities is a consequence of an evolutionary conflict of interest between the sexes over reproduction and is common among sexually reproducing species. Male Trinidadian guppies Poecilia reticulata spend a large proportion of their time harassing females for copulations and their presence in female social groups has been shown to disrupt female-female social networks and the propensity for females to develop social recognition based on familiarity. In this study, we investigate the behavioural mechanisms that may lead to this disruption of female sociality. Using two experiments, we test the hypothesis that male presence will directly affect social behaviours expressed by females towards other females in the population. In experiment one, we tested for an effect of male presence on female shoaling behaviour and found that, in the presence of a free-swimming male guppy, females spent shorter amounts of time with other females than when in the presence of a free-swimming female guppy. In experiment two, we tested for an effect of male presence on the incidence of aggressive behaviour among female guppies. When males were present in a shoal, females exhibited increased levels of overall aggression towards other females compared with female only shoals. Our work provides direct evidence that the presence of sexually harassing males alters female-female social behaviour, an effect that we expect will be recurrent across taxonomic groups.     

Copulation behaviour in mammals: evidence that sperm competition is widespread

We review information on copulation behaviour and sperm competition in mammals using data primarily from the literature. Female mammals of many species regularly copulate with more than one male during each oestrous period. Such multi-male copulations are reported more often in social, compared with solitary species. In addition, the mates of males of polygynous species experience multi-male copulations as often as the mates of males or monogamous species. Male mammals attempt to increase their certainty of paternity through a number of reproductive tactics. Copulation frequency is higher in specks with multi-male copulations compared with other species. Consortships, which can br regarded as a form of mate guarding, are often absent from species in which more than one male copulates with each female during her oestrous period. Most solitary burrow-living small mammal species copulate in the open, whereas social species often copulate inside their burrows. Insurance copulations may occur in many species since high copulation rates occur in four circumstances: (i) when mates are reunited, (ii) when a new male takes over a female, (iii) when a strange male steals a copulation, and (iv) when an audience of males is present.     

Males Respond to the Risk of Sperm Competition in the Sexually Cannibalistic Praying Mantis, Mantis religiosa

Although studies on sperm competition examined a wide range of taxa, little is known about the selection pressures on male traits in systems with simultaneous risk of sperm competition and sexual cannibalism. Here, we experimentally studied how the risk of sperm competition affects male copulatory behavior in the sexually cannibalistic praying mantis Mantis religiosa. We recorded the onset and duration of copulations following the introduction of virgin, adult praying mantises into mating arenas with three different sex ratio treatments: polyandrous, monogamous, and polygynous. We did not detect any female phenotypic trait predicting cannibalism. The chance of male survival was related to his condition, with males in better condition being cannibalized significantly less often. In contrast, we did not identify any male trait that would favor some males to obtain copulations. Our results on copulation duration support sperm competition theory in that the copulations in the male‐biased treatment, where the perceived risk of sperm competition was greatest, were significantly longer than those in single‐male treatments. Importantly, males in better condition copulated significantly longer regardless of sex ratio. Overall, our study suggests that males can adjust their copulation behavior in response to the risk of sperm competition even in a system with frequent sexual cannibalism.     

The effect of size and sex ratio experiences on reproductive competition in Nicrophorus vespilloides burying beetles in the wild

Male parents face a choice: should they invest more in caring for offspring or in attempting to mate with other females? The most profitable course depends on the intensity of competition for mates, which is likely to vary with the population sex ratio. However, the balance of pay‐offs may vary among individual males depending on their competitive prowess or attractiveness. We tested the prediction that sex ratio and size of the resource holding male provide cues regarding the level of mating competition prior to breeding and therefore influence the duration of a male's biparental caring in association with a female. Male burying beetles, Nicrophorus vespilloides were reared, post‐eclosion, in groups that differed in sex ratio. Experimental males were subsequently translocated to the wild, provided with a breeding resource (carcass) and filmed. We found no evidence that sex ratio cues prior to breeding affected future parental care behaviour but males that experienced male‐biased sex ratios took longer to attract wild mating partners. Smaller males attracted a higher proportion of females than did larger males, securing significantly more monogamous breeding associations as a result. Smaller males thus avoided competitive male–male encounters more often than larger males. This has potential benefits for their female partners who avoid both intrasexual competition and direct costs of higher mating frequency associated with competing males.     

Soay rams target reproductive activity towards promiscuous females' optimal insemination period

Female promiscuity is thought to have resulted in the evolution of male behaviours that confer advantages in the sperm competition that ensues. In mammalian species, males can gain a post-copulatory advantage in this sperm 'raffle' by inseminating females at the optimal time relative to ovulation, leading to the prediction that males should preferentially associate and copulate with females at these times. To the best of our knowledge, we provide the first high-resolution test of this prediction using feral Soay sheep, which have a mating system characterized by male competition for access to highly promiscuous females. We find that competitive males time their mate guarding (and hence copulations) to occur close to the optimal insemination period (OIP), when females are also increasingly likely to 'cooperate' with copulation attempts. Subordinate males practice an alternative mating tactic, where they break the integrity of the consort pair and force copulations on females. The timing of these forced copulations is also targeted towards the OIP. We thus provide quantitative evidence that female promiscuity has resulted in the evolution of reproductive strategies in which males 'load' the sperm raffle by targeting their mating activity towards female OIPs, when the probability of sperm-competition success is at its greatest.     

Social status and availability of females determine patterns of sperm allocation in the fowl

Where sperm competition occurs, the number and quality of sperm males inseminate relative to rival males influences fertilization success. The number of sperm males produce, however, is limited, and theoretically males should allocate sperm according to the probability of gaining future reproductive opportunities and the reproductive benefits associated with copulations. However, the reproductive opportunities and value of copulations males obtain can change over their lifetime, but whether individuals respond to such changes by adjusting the way they allocate sperm is unclear. Here we show that, in the fowl, Gallus gallus, dominant males, which have preferential access to females, modulate the number of sperm they ejaculate according to the availability of females. When presented with two females, dominant males allocated more sperm to higher quality females, whereas when females were on their own, only copulation order had an affect on their sperm numbers. In contrast, subordinate males, whose mating activity is restricted by dominant males, allocated high numbers of sperm to initial copulations, irrespective of female availability. We further show, by manipulating male social status, that sperm allocation is both phenotypically plastic, with males adjusting their patterns of sperm allocation according to their dominance rank, and intrinsic, with males being consistently different in the way they allocate sperm, once the effects of social status are taken into account. This study suggests that males have evolved sophisticated patterns of sperm allocation to respond to frequent fluctuations in the value and frequency of reproductive opportunities.     

Reproductive costs of mating with a sibling male: sperm depletion and multiple mating in Cephalonomia hyalinipennis

Polygynous parasitoid males may be limited by the amount of sperm they can transmit to females, which in turn may become sperm limited. In this study, I tested the effect of male mating history on copula duration, female fecundity, and offspring sex ratio, and the likelihood that females will have multiple mates, in the gregarious parasitoid Cephalonomia hyalinipennis Ashmead (Hymenoptera: Bethylidae: Epyrinae), a likely candidate for sperm depletion due to its local mate competition system. Males were eager to mate with the seven females presented in rapid succession. Copula duration did not differ with male mating history, but latency before a first mating was significantly longer than before consecutive matings. Male mating history had no bearing on female fecundity (number of offspring), but significantly influenced offspring sex ratio. The last female to mate with a given male produced significantly more male offspring than the first one, and eventually became sperm depleted. In contrast, the offspring sex ratio of first‐mated females was female biased, denoting a high degree of sex allocation control. Once‐mated females, whether sperm‐depleted or not, accepted a second mating after a period of oviposition. Sperm‐depleted females resumed production of fertilized eggs after a second mating. Young, recently mated females also accepted a second mating, but extended in‐copula courtship was observed. Carrying out multiple matings in this species thus seems to reduce the cost of being constrained to produce only haploid males after accepting copulation with a sperm‐depleted male. I discuss the reproductive fitness costs that females experience when mating solely with their sibling males and the reproductive fitness gain of males that persist in mating, even when almost sperm‐depleted. Behavioural observations support the hypothesis that females monitor their sperm stock. It is concluded that C. hyalinipennis is a species with a partial local mating system.     

Intrasexual mounting in the beetle Diaprepes abbreviatus (L.).

The weevil Diaprepes abbreviatus shows three kinds of same-sex mountings: males mount other unpaired males, males mount males already engaged in copulation and females mount other females. Four hypotheses were evaluated in order to explain same-sex matings by males: (i) female mimicry by inferior males, (ii) dominance of larger males which affects the behaviour of small males, (iii) sperm transfer in which smaller males gain some reproductive success by 'hitchhiking' their sperm with the sperm of larger males, and (iv) poor sex recognition. Data from mate choice and sperm competition experiments rejected the female mimicry, dominance and sperm transfer hypotheses and supported the poor sex recognition hypothesis. We tested three hypotheses in order to explain female mounting behaviour: (i) females mimic male behaviour in order to reduce sexual harassment by males, (ii) females mount other females in order to appear larger and thereby attract more and larger males for mating, and (iii) female mimicry of males. The results of our mate choice experiments suggested that the female mimicry of males hypothesis best explains the observed female mounting behaviour. This result is also consistent with the poor sex recognition hypothesis which is the most likely explanation for male and female intrasexual mating behaviour in many insect species.     

Colourful male guppies produce faster and more viable sperm

In guppies (Poecilia reticulata) precopulatory sexual selection (via female choice) and post-copulatory selection (via sperm competition) both favour males with relatively high levels of carotenoid (orange) pigmentation, suggesting that colourful males produce more competitive ejaculates. Here we test whether there is a positive association between male orange pigmentation and sperm quality. Our analysis of sperm quality focused on sperm swimming speeds (using CASA: computer-assisted sperm analysis to estimate three parameters of sperm velocity in vitro), sperm viability (proportion of live sperm per stripped ejaculate) and sperm lengths. We found that males with relatively large areas of orange pigmentation had significantly faster and more viable sperm than their less ornamented counterparts, suggesting a possible link between dietary carotenoid intake and sperm quality. By contrast, we found no relationship between sperm length (head length and total sperm length) and male phenotype. These findings, in conjunction with previous work showing that highly ornamented male guppies sire higher quality offspring, suggest that female preference for colourful males and sperm competition work in concert to favour intrinsically higher quality males.     

Phenotypic correlates of spermatozoon quality in the guppy, Poecilia reticulata

The phenotype-linked fertility hypothesis suggests that a femalecan benefit directly from mate choice when the cues she usesindicate the quantity and/or quality of his spermatozoa. Wetested the link between sperm quality and male body size andcoloration in the resource-free mating system of the guppy,a tropical fish characterized by strong female choice. Largermales possessed larger testes and are therefore predicted toproduce larger numbers of spermatozoa than smaller males. Largermale guppies also produced longer spermatozoa than smaller males.Degree of carotenoid coloration did not predict either the quantityor the quality of a male's spermatozoa. These results are consistentwith a previous study that showed that female guppies in thestudy population prefer larger males to brightly colored males.The male-size directed increase in spermatozoon size may bethe result of interplay between sperm competition and the coevolutionof spermatozoon traits with the female reproductive tract.     

Cryptic male choice: sperm allocation strategies when female quality varies

We examined evolutionary stable sperm allocation and included stochastic variation in male mating frequency, not included in previous models examining sperm allocation strategies. We assumed sperm mixing and variation in female quality and used a genetic algorithm to analyse the evolution of male sperm allocation. Our results show that males should invest more sperm in initial copulations than in subsequent copulations as a male might fail to mate again. The inclusion of variation in female fecundity had no influence on the evolutionary stable sperm allocation strategy if males were unable to recognize female quality. If males were assumed to allocate sperm in response to female quality, the proportion of sperm allocated was positively correlated with female quality. Moreover, with increasing variance in female quality, males conserved more sperm for later copulations. Literature data on sperm allocation from diverse taxa show a good fit with the predictions given by our model.     

Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata)

In the guppy (Poecilia reticulata), males have two alternative mating tactics. Individual males may either display to a receptive female prior to attempting to copulate with her or attempt to quickly sneakcopulate with a female without first displaying to her or without a prior receptive response from her. In this study, I experimentally investigated the effects of simulated local increases in the risk of predation (in the form of a cichlid fish predator model in situ) on the mating tactics used by free-ranging male guppies in two typical macrohabitats (riffle and pool) of a Trinidadian river. Focal male guppies displayed to females significantly less often on average, and conversely attempted sneak copulations more often, in the presence of the predator model than in its absence; this pattern was similar for both habitats. These fish therefore performed a lower proportion of sigmoid displays and increased their sneaky mating attempts when the apparent risk of predation had increased locally. This predator-mediated response is consistent with a trade-off between mating success and risk of mortality due to predation. The results are the first to confirm risk-sensitive mating behaviour in free-ranging male guppies within a population, and demonstrate the potential importance of predators in influencing the relative use of alternative mating tactics in this species on a microgeographical scale in the wild.