Sperm-depleted Males Research Articles

Sperm depletion and mate choice of the crab spider, Ebrechtella tricuspidata (Fahricius)

Abstract Mounting evidence suggests that male sperm may be gradually depleted after consecutive matings, resulting in the decline of female reproductive output in insect species. It is predicted that females may employ adaptive strategies to avoid the sperm-depleted males, such as mating multiply with different males and/or discriminating against previously mated males (MMs). Similarly, males may exhibit adaptive behaviors toward females varying in mating status. However, in spiders with males lacking primary copulatory organs and their pedipalps modified to transfer sperm, there are few studies on male mating potential and previous mating experience on their subsequent mate choice. In this study, we used a polyandrous crab spider, Ebrechtella tricuspidata, a sit-and-wait predator with female-biased sex ratio as a model system to ascertain whether 1) male mating experiences influence female reproductive fitness; 2) females respond differently to males varying in mating status; and 3) males respond differently to females varying in mating status. Our results showed that female fecundity was independent of male mating experiences, but female fertility markedly declined with the increase of male previous mating experiences in the first eggsac. Counter to our predictions, females preferred to choose and mate with the larger males, regardless of their mating status. In contrast, male mating status influenced their mating preference toward females. Virgin males did not show any preference between virgin and mated females; however, MMs were more likely to prefer the virgin females over the mated ones. Overall, our results indicated that female choice depended primarily on male relative size rather than male mating status, whereas male choice depended on female mating status. Depending on the investigation of reproductive dynamics and mate choice in E. tricuspidata, the study will provide valuable insights into the adaptive behaviors of both males and females exhibiting toward mates varying in mating status.

Sperm-depleted males of the two-spotted spider mite can replenish sperm in a few hours.

In many animals, males increase their reproductive success by mating with as many females as possible. The number of females a male can fertilize is often limited by male competition for access to females, sperm competition, and the cost of sperm production. Especially, recent studies have shown that sperm production is more costly than previously expected. In the two-spotted spider mite, Tetranychus urticae Koch, the number of females a male can inseminate is limited mainly by male competition for access to females. However, in the absence of rivals, males mate with so many females that they can become sperm-depleted. Mating without sperm transfer does not produce any offspring, although it takes time and energy. Therefore, a question arises as to why males continue to mate even after sperm depletion. In this study, we hypothesized that males continue to mate because sperm is replenished after a short period. To test the hypothesis, we investigated how long it takes for sperm replenishment after sperm depletion. We found that in 3h, sperm can be replenished enough to inseminate a few females. As 3h is sufficiently short not to lose the next mating opportunity, the results support the hypothesis. However, copulation duration in the sperm-replenished males was significantly longer than in the sperm-depleted males but shorter than in males before sperm depletion. To explain the differences, further research would be necessary. In addition, anatomical physiology study in males is also required to confirm that sperm is indeed depleted and replenished.

A Wright-Fisher model with indirect selection.

We study a generalization of the Wright-Fisher model in which some individuals adopt a behavior that is harmful to others without any direct advantage for themselves. This model is motivated by studies of spiteful behavior in nature, including several species of parasitoid hymenoptera in which sperm-depleted males continue to mate despite not being fertile. We first study a single reproductive season, then use it as a building block for a generalized Wright-Fisher model. In the large population limit, for male-skewed sex ratios, we rigorously derive the convergence of the renormalized process to a diffusion with a frequency-dependent selection and genetic drift. This allows a quantitative comparison of the indirect selective advantage with the direct one classically considered in the Wright-Fisher model. From the mathematical point of view, each season is modeled by a mix between samplings with and without replacement, and analyzed by a sort of "reverse numerical analysis", viewing a key recurrence relation as a discretization scheme for a PDE. The diffusion approximation is then obtained by classical methods.

Females remate more frequently when mated with sperm-deficient males.

Polyandry is a source of sexual conflict and males often try to limit female promiscuity. Consequently, male manipulation of receptivity via antiaphrodisiacs and copulatory plugs that prevent female remating can be a source of sexual conflict. This sexual conflict may be intensified when females must remate for fertility insurance. Male red-sided garter snakes produce a large, gelatinous copulatory plug that has been proposed to 1) physically prevent remating and 2) contain an antiaphrodisiac that reduces female receptivity. These males may become sperm depleted because of their dissociated reproductive pattern. If a female mates with a sperm deficient male and is also rendered unreceptive to further mating, then this represents a serious conflict. We tested whether female remating frequency is affected when females are mated with a male that produces a sperm-less copulatory plug. We show that females are significantly more likely to remate after mating with vasectomized males than intact males, even though vasectomized males still produce a copulatory plug. These results suggest that the ejaculate material of the plug does not contain an antiaphrodisiac. Instead, females may use sperm as a cue for post-copulatory mate assessment and seek to remate for the direct benefit of fertility insurance if they have mated with sperm-depleted males.

Sperm-depleted males influence the reproductive behaviour of conspecifics.

In many insect species, sperm-depleted males (SDMs, i.e. males that have exhausted their sperm after a given number of matings) remain sexually active and continue to mate females. Here, we investigated the behavioural modifications that occur in both sexes of the parasitoid Asobara tabida Nees (Hymenoptera: Braconidae), after matings by fertile males and sperm-depleted males. We show that (i) virgin females, mated females and females mated to a SDM exhibited different behaviours and that (ii) males responded differently to females depending on whether the females had previously mated with an SDM or not. Our findings demonstrate that SDM influenced the reproductive behaviour of both males and females, especially with regard to male responsiveness and female attractiveness. These findings are discussed in the context of adaptive behaviour and fitness maximization in both males and females.

Sperm as a limiting factor in mating success in Hymenoptera parasitoids

AbstractThe paradigm that females produce few costly eggs, whereas males produce an unlimited quantity of sperm holds true when matings are dispersed over time and males can replenish their sperm supply. In such a system, the best strategy for males is to mate with as many females as possible, as more is always better. However, in parasitoid species, mating often occurs at the emergence site and males may have to mate successively several females in a short period of time. This can lead to sperm depletion that can be temporary in synspermatogenic species whose males produce sperm throughout their adult life, or definitive in prospermatogenic species whose males emerge with their full sperm complement and do not produce more during their adult life. Both the spermatogeny index and the mating structure of a species will therefore influence the probability and intensity of sperm depletion in males. Sperm‐limited males can court and mate females even in prospermatogenic species. These males still gain some inclusive fitness by preventing competitor males to fully inseminate females, therefore increasing the representation of their daughters in the following generation. Females that mate with partially or completely sperm‐depleted males produce a constrained sex ratio that decreases their lifetime fitness. In species where sperm‐depleted males occur, female choosiness based on sperm supply is predicted, as the cost of mating sperm‐depleted males can be high. In addition, males are also expected to be choosy in prospermatogenic species as mating with sub‐optimal females can be costly when sperm is limited.

Female choice in response to risk of sperm limitation by the stone crab, Hapalogaster dentata

Mating with males that have recently mated would be risky for females because the males may have limited sperm. Females should prefer males that can provide sufficient sperm for successful fertilization. We investigated whether female stone crabs prefer the larger of two males and which type of cue, visual or chemical, is more important for female mate preference. We then investigated whether females show mate choice in response to the risk of sperm limitation by exposing a receptive female in an aquarium to two males simultaneously: an unmated male with sufficient sperm reserves and a male with depleted sperm reserves. We tethered the males and wrapped their chelae to prevent interference in the females' choice. All females approached and mated with the larger males, indicating that females prefer larger to smaller males. Females located larger males by waterborne chemical cues. Using these cues, females showed a preference for unmated males with sufficient sperm reserves over sperm-depleted males, indicating that sperm limitation occurs in nature, and is a selection pressure in the mating strategy of female stone crabs. Thus, the influence of risk of sperm limitation on female choice should be considered in studies of sexual selection by field observations and laboratory experiments, and in sexual selection models.

Why do sperm-depleted parasitoid males continue to mate?

Insect males of several parasitoid species have limited amount of sperm at emergence and experience sperm depletion when mate acquisition rate is high, suggesting that sperm production and storage could be a limiting factor for male's fitness. Sperm-depleted males of the parasitoid wasp Trichogramma evanescens continue to mate, and the impact of this behavior on sperm storage by females has been studied. Virgin females T. evanescens stored 50.6 ± 13.1 (Mean ± SD) sperm when mating first with a virgin male. However, when these females mated first with a sperm-depleted male and then with a virgin male, they stored only 18.9 ± 7.8 sperm, indicating that mating with a sperm-depleted male has a cost and limits sperm acquisition from fertile males. Following a mating with a sperm-depleted male, females had to mate with three virgin males to restore their sperm supply confirming that additional mating enabled the female to store a limited number of sperm. According to our results, by continuing to mate, sperm-depleted males do not prevent mates from copulating again but they decrease their ability to store other male's sperm. Continuing to mate could be a strategy to increase the relative fitness of sperm-depleted males.

Sexual selection and mating advantages in the giant sperm species, Drosophila bifurca

Mate choice may be exercised by either sex; however, females are generally choosier than males because they invest more in their gametes. Female choice is often based on direct benefits, such as better reproductive output, whereas male choice appears to be based on differences in female fecundity. However, when gamete production is limited, sexual selection theories predict that mate choice will be decisive for reproductive success in both sexes. Here, we investigate how mating advantage is achieved in Drosophila bifurca, a giant sperm species in which both sexes produce only a few gametes. Our initial expectations were as follows: (1) females would discriminate against sperm-depleted males to avoid fertility cost; and (2) males would discriminate against inseminated females to reduce sperm competition and increase the assurance of paternity of individual gametes. Differences in courtship behaviors were analyzed with regard to the sexual maturity, which is reached after 22 days in males at 21°C, and the reproductive history of both sexes (inseminated versus virgin for females, and sperm-depleted versus sperm-loaded for males). Our results show that: (1) sexual immaturity precludes mating in both sexes; (2) virgin females do not discriminate between sperm-loaded and sperm-depleted males, and (3) males mate preferentially with virgin females, because inseminated females fend off the male, which tended to bring male courtship to an end. Female remating was limited, but increased significantly when the first male was sperm-depleted. Contrary to our initial expectations, these findings suggest that male sperm depletion does not affect female mating preference, whereas the success of male courtship is driven by female behavior. The possibility that female remating was only promoted in response to low sperm transfer is discussed in relation to the gametic system of this species.

Unnatural selection: Effects of a male-focused size-selective fishery on reproductive potential of a blue crab population

A male-focused size-selective fishery, like the one targeting the blue crab ( Callinectes sapidus Rathbun) along the Atlantic and Gulf coasts of the U.S., has the potential to reduce the average size of the males in the population, reduce the density of males in the population, and/or raise the ratio of females to males. All of these may affect the mating dynamics of the population by reducing the amount of sperm that males provide to females and decreasing the number of males available for copulation. We investigated the effect of the fishery on a blue crab population in upper Chesapeake Bay by collecting crabs in areas of markedly different fishing pressure. Crabs were taken as individuals and as mating pairs, which permitted assessing the size of males currently mating in nature, and the seminal resources they possess and transfer to females. Average size of males in subpopulations that have been subjected to heavier fishing pressure is indeed smaller, and the smaller males pass less sperm and accessory fluid to females than would larger males if they were still present. Some males in pre-copulatory pairs are as sperm depleted as males that had just completed copulation, indicating that they are mating more frequently than they can replace their seminal resources. The most sperm-depleted males in the population are not even pairing or attempting to mate.

Sexual selection and mating advantages in the giant sperm species, Drosophila bifurca

Mate choice may be exercised by either sex; however, females are generally choosier than males because they invest more in their gametes. Female choice is often based on direct benefits, such as better reproductive output, whereas male choice appears to be based on differences in female fecundity. However, when gamete production is limited, sexual selection theories predict that mate choice will be decisive for reproductive success in both sexes. Here, we investigate how mating advantage is achieved in Drosophila bifurca, a giant sperm species in which both sexes produce only a few gametes. Our initial expectations were as follows: (1) females would discriminate against sperm-depleted males to avoid fertility cost; and (2) males would discriminate against inseminated females to reduce sperm competition and increase the assurance of paternity of individual gametes. Differences in courtship behaviors were analyzed with regard to the sexual maturity, which is reached after 22 days in males at 21 degrees C, and the reproductive history of both sexes (inseminated versus virgin for females, and sperm-depleted versus sperm-loaded for males). Our results show that: (1) sexual immaturity precludes mating in both sexes; (2) virgin females do not discriminate between sperm-loaded and sperm-depleted males, and (3) males mate preferentially with virgin females, because inseminated females fend off the male, which tended to bring male courtship to an end. Female remating was limited, but increased significantly when the first male was sperm-depleted. Contrary to our initial expectations, these findings suggest that male sperm depletion does not affect female mating preference, whereas the success of male courtship is driven by female behavior. The possibility that female remating was only promoted in response to low sperm transfer is discussed in relation to the gametic system of this species.

Costs and benefits of polyandry in the egg parasitoid Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae)

Abstract Polyandry implies costs (i.e., time, energy, predation risk, etc.) especially in short-lived parasitoid species but females of several hymenopteran parasitoid species, mostly gregarious, do mate with multiple males. Several hypotheses have been proposed to explain the benefits of polyandry but controversy remains, especially in facultative gregarious species that bridge the gap between solitary and gregarious development. In this study, we investigated the possibility that polyandry may bring material benefits to Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) females, a short-lived and facultative gregarious egg parasitoid. Females mated several times with different males both at emergence and throughout their life. No significant difference was found in the offspring sex ratio and the fecundity of multiple mated and single mated females and pre-mating duration increased with the female’s age. The longevity of females did vary significantly with the number of matings but only in the presence of hosts. Female T. evanescens received enough sperm from one mating to allocate an optimal offspring sex ratio and we found no evidence of either nutritional resources or convenience polyandry in this species. Polyandry in facultative gregarious parasitoids might be an adaptive strategy to minimize the risk of mating with males that have already emptied their sperm bank or to accumulate sperm from several partially sperm-depleted males. Polyandry may also increase the probability of non-sib mating in patches exploited by several females.

Sexual conflict and cooperation under naturally occurring male enforced monogamy

An evolutionary conflict often exists between the sexes in regard to female mating patterns. Females can benefit from polyandry, whereas males mating with polyandrous females lose reproductive opportunities because of sperm competition. Where this conflict occurs, the evolution of mechanisms whereby males can control female remating, often at a fitness cost to the female, are expected to evolve. The fitness cost to the female will be increased in systems where a few high status males monopolise mating opportunities and thus have limited sperm supplies. Here we show that in the cockroach Nauphoeta cinerea, a species where males enforce female monogamy in the first reproductive cycle, males that have become sperm depleted continue to be able to manipulate female remating behaviour. Although the manipulation severely decreases fecundity in females mated to sperm-depleted males, males benefit, increasing their relative fitness by preventing other males from reproducing. Our results suggest that there is selection on maintaining the mechanism of manipulation rather than maintaining sperm numbers. Taken with previous research on sexual conflict in N. cinerea, this study suggests that the causes and consequences of sexual conflict are complex and can change across the life history of an individual.

A Potential Cost of Monandry in the Lekking Sandfly Lutzomyia Longipalpis

Multiple mating by females is a subject of considerable controversy. In some species, however, females appear to mate only once, and the potential costs and benefits of this behavior are equally intriguing. When male mating success is highly skewed, monandrous females potentially risk mating with a sperm depleted male. In lek-breeding species, a male may gain up to 80% of available matings, yet few studies have explored whether these highly successful males suffer sperm depletion. These points are investigated in a series of laboratory experiments on the lekking sandfly, Lutzomyia longipalpis. It is shown that females may actively reject males prior to and after genital contact and that mated females do not remate within a single egg-laying cycle regardless of the refractory period between the first and subsequent matings. Males mate multiply and suffer from the effects of sperm depletion after their fifth copulation. Despite this, they continue to court and copulate females with equal vigor and females do not appear to detect sperm-depleted males: they lay similar numbers of eggs irrespective of the number of females their mate has previously copulated with. The implications of a single mating for L. longipalpis females in natural and laboratory leks are discussed.

Eolian sorting and roundness of beach and sand dunes : Eisma D., 1965. Netherlands J. Sea Res., 2 (4): 541–555

A male-focused size-selective fishery, like the one targeting the blue crab (Callinectes sapidus Rathbun) along the Atlantic and Gulf coasts of the U.S., has the potential to reduce the average size of the males in the population, reduce the density of males in the population, and/or raise the ratio of females to males. All of these may affect the mating dynamics of the population by reducing the amount of sperm that males provide to females and decreasing the number of males available for copulation. We investigated the effect of the fishery on a blue crab population in upper Chesapeake Bay by collecting crabs in areas of markedly different fishing pressure. Crabs were taken as individuals and as mating pairs, which permitted assessing the size of males currently mating in nature, and the seminal resources they possess and transfer to females. Average size of males in subpopulations that have been subjected to heavier fishing pressure is indeed smaller, and the smaller males pass less sperm and accessory fluid to females than would larger males if they were still present. Some males in pre-copulatory pairs are as sperm depleted as males that had just completed copulation, indicating that they are mating more frequently than they can replace their seminal resources. The most sperm-depleted males in the population are not even pairing or attempting to mate.