Male copulation behaviour and the risk of sperm competition

When females mate with more than one male during their reproductive cycle, males may increase their share of paternity by copulating repeatedly with the same female. Accordingly, males should mate repeatedly with the same female more frequently when the risk of sperm competition is greater. We examined this idea experimentally in the orb-web spiderNephila edulis , which is characterized by both extreme sexual size dimorphism and extreme male size variation. Comparison of the mating behaviour of solitary and pairs of males on the webs of virgin and mated females revealed that males adjust the frequency and duration of copulation according to the mating history of the female and the presence of rival males. Males copulated more frequently and for longer with virgin than mated females. The copulation behaviour of males in the presence of rivals depended upon their relative size. Typically, larger males prevented smaller rivals from gaining access to the female and therefore were able to copulate more frequently. Smaller males copulated less frequently, but for longer periods, which may have increased their share of paternity. The size of male N. edulis can vary by an order of magnitude, and our results suggest that this variation may be maintained by the alternative size-dependent strategies of preventing or winning sperm competition. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Pairing and insemination patterns in a giant weta (Deinacrida rugosa: Orthoptera; Anostostomatidae)

Positive size assortative mating can arise if either one or both sexes prefer bigger mates or if the success of larger males in contests for larger females leaves smaller males to mate with smaller females. Moreover, body size could not only influence pairing patterns before copulation but also the covariance between female size and size of ejaculate (number of spermatophores) transferred to a mate. In this field study, we examine the pre-copulatory mate choice, as well as insemination, patterns in the Cook Strait giant weta (Deinacrida rugosa). D. rugosa is a large orthopteran insect that exhibits strong female-biased sexual dimorphism, with females being nearly twice as heavy as males. Contrary to the general expectation of male preference for large females in insects with female-biased size dimorphism, we found only weak support for positive size assortative mating based on size (tibia length). Interestingly, although there was no correlation between male body size and the number of spermatophores transferred, we did find that males pass more spermatophores to lighter females. This pattern of sperm transfer does not appear to be a consequence of those males that mate heavier females being sperm depleted. Instead, males may provide lighter females with more spermatophores perhaps because these females pose less of a sperm competition risk to mates.     

Female mate choice and mating costs in the polyandrous butterflyPieris napi (Lepidoptera: Pieridae)

Males of the green-veined white butterfly (Pieris napi L.) transfer large ejaculates that represent on average 15% of their body mass when mating for a first time. Shortly after mating a male is able to transfer only a small ejaculate when mating a second time. Male ejaculate production plays a crucial role in the mating system ofP. napi because females use male-derived nutrients for egg production and somatic maintenance. Here we study how timing of female rematings and copulation duration are influenced by the mating history of their mates and, also, study if females exert mate choice to minimize their mating costs. Mating with a recently mated male increased female mating costs by increasing time in copula and mating frequency. Virgin females that mated with virgin males remated after an average of 6 days, whereas virgin females that mated with recently mated males remated after an average of 2 days. Moreover, copulations involving recently mated males lasted on average almost 7 h, whereas copulations involving virgin males lasted on average 2 h. Recently mated males were eager to remate, in spite of the fact that the size of the ejaculate they transfer is small and that they remain in copula for a long time. Hence it seems that males are more successful in the sexual conflict over mating decisions and that females do not minimize mating costs by choosing to mate preferentially with virgin males.     

Size Dependent Sexual Selection in Drosophila ananassae

Mate choice based on body size is widespread and can have numerous consequences. We present data, which show the effect of male and female body size on sexual selection in Drosophila ananassae. The relationships between wing size, locomotor activity, mating latency, courtship pattern, fertility and mating success were studied. Mating latency was negatively correlated with wing length and with locomotor activity, while wing length and locomotor activity was positively correlated in males as well as in females. In female- and male-choice, we found that mate choice influenced size-assortative mating by: (1) large and small males preferring to mate with large females, (2) large males successfully competing for large females, leaving small males to mate with small females. Males increased their reproductive success by mating with large and more fecund females. In addition, in pairs of long/short winged flies, long winged flies courted and mated more successfully than short winged flies and they also have longer duration of copulation and more progeny than short winged flies. We found sterile mating in pairs of small winged males and females.     

The role of mating history and male size in determining mating behaviours and sexual conflict in a water strider

We conducted three experiments to test the effects of mating history of both sexes and of male body size on mating behaviours in the water strider, Gerris buenoi. Our manipulations influenced the interests of both sexes and, thus, the degree of conflict over mating behaviours. Mating history was a dichotomous variable (deprived/mated), depending on holding conditions in the laboratory. Experiment 1 considered and found independent effects of male and female mating history on latency to copulation and copulation duration. In experiment 2, we manipulated only female mating history, using unsuccessful struggle rates as evidence for female reluctance and conflict over mating. Finally, we investigated the relation between male body size and mating history on copulation duration. We predicted that intersexual conflict over mating would be lowest when females were deprived, because female interests under these conditions should more closely match those of males. Deprived females began mating in half the time of mated females and were twice as likely to mate because of reduced reluctance. Furthermore, copulation duration for deprived males was about one and a half times longer than that for mated males. Although previous studies examining nonrandom mating patterns by size predicted longer copulations for small males, we found that small males prolonged copulation when deprived more than large males. We conclude that females primarily influence copulation frequency, but males primarily influence copulation duration. Our results favour the hypothesis that reduced mating opportunity for small males accounts for their extended copulation duration. Finally, our findings provide evidence for strong effects of male body size on selection mechanisms in water striders, and support the hypothesis of conflicting pre- and postcopulatory selection mechanisms in this group. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.     

Male age and sexual experience affect male mating behavior in the hawthorn spider mite,Amphitetranychus viennensis

As is reported, in species with first-male sperm precedence, male age and previous sexual experience play crucial roles in male mating behavior. In the hawthorn spider mite, Amphitetranychus viennensis Zacher, previous studies showed that only females that copulated for the first time could achieve fertilization. Based on this, the effects of male age and mating history on male mate choice and male mate competition were investigated. It was confirmed that males could distinguish virgins from fertilized females but they were unable to discriminate between virgins and unfertilized females. Interestingly, the copulation duration of males mated with fertilized females was much shorter than that of males mated with virgins or unfertilized females. Additionally, for male mating choice, males of all ages and more experienced males preferred 5-day-old virgin females, whereas only less experienced males preferred 1-day-old virgin females. In male-male competition, 3-day-old males were more competitive and obtained more copulations compared with others. Copula duration was closely related to male age. Though no significant differences were observed in mating competition between virgin and mated males, copula duration of males in first copulation was the longest and gradually shortened in subsequent copulations. In all, this investigation demonstrated that male age and sexual experience affected male mate choice and male-male competition, leading to further insight into the influences of male age and sexual experience on the reproductive fitness of both sexes.

     

Mating Status Effects on Sexual Response of Males and Females in the Parasitoid Wasp <Emphasis Type="Italic">Urolepis rufipes</Emphasis>

Although mate preferences are most commonly examined in females, they are often found in both sexes. In the parasitoid wasp Urolepis rufipes, both female and male mating status affected certain aspects of sexual interactions. Female mating status mattered only in the later stages of mating. Males did not discriminate between virgin and mated females in terms of which they contacted or mounted first. However, once mounted, most virgin females were receptive to copulation, whereas very few mated females were. Whether a male’s mating status affected his own sexual response depended on the female’s ability to respond and the stage of mating. Examining male behavior toward dead females allowed elimination of the role of female behavior in how males responded. Virgin and mated males are both attracted to dead females as evidenced by their fanning their wings at such females. However, mated males were quicker than virgin males to contact and to mount in an experiment with dead females, whereas there was no such differential response in an experiment with live females. This difference is consistent with greater female sexual responsiveness to virgin males. Male mating status also affected female receptivity to copulate. Once mounted, live virgin females were less likely to become receptive to copulation by mated males than to virgin males, but only in a choice experiment, not in a no-choice experiment.     

Competitive PCR reveals the complexity of postcopulatory sexual selection in Teleogryllus commodus

The outcome of mate choice depends on complex interactions between males and females both before and after copulation. Although the competition between males for access to mates and premating choice by females are relatively well understood, the nature of interactions between cryptic female choice and male sperm competition within the female reproductive tract is less clear. Understanding the complexity of postcopulatory sexual selection requires an understanding of how anatomy, physiology and behaviour mediate sperm transfer and storage within multiply mated females. Here we use a newly developed molecular technique to directly quantify mixed sperm stores in multiple mating females of the black field cricket, Teleogryllus commodus. In this species, female postcopulatory choice is easily observed and manipulated as females delay the removal of the spermatophore in favour of preferred males. Using twice‐mated females, we find that the proportion of sperm in the spermatheca attributed to the second male to mate with a female (S₂) increases linearly with the time of spermatophore attachment. Moreover, we show that the insemination success of a male increases with its attractiveness and decreases with the size of the female. The effect of male attractiveness in this context suggests a previously unknown episode of mate choice in this species that reinforces the sexual selection imposed by premating choice and conflicts with the outcome of postmating male harassment. Our results provide some of the clearest evidence yet for how sperm transfer and displacement in multiply mated females can lead directly to cryptic female choice, and that three distinct periods of sexual selection operate in black field crickets.     

Male Reproductive Success in a Promiscuous Armoured Catfish Corydoras Aeneus (Callichthyidae)

Among a variety of fish mating systems, promiscuity with random-mating seems to be most prevalent. However, detailed studies of promiscuity have been rare due partly to the peculiar difficulty in examination of male mating and reproductive success in the random mating. Females of the armoured catfish Corydoras aeneus (no sexual dimorphism other than size of males > females) spawn 10–20 egg-clutches with multiple males at a time, but an entire egg clutch is inseminated by sperm of a single male. We studied mating system of this fish in aquarium. Males had neither mating territories nor monopolized females, never being aggressive against rival males. Evidence of female preference for certain male traits including size was not detected. Females mated a male in proportion to his relative courtship frequency among males. Courtship frequency was not related to male size, and male mating success was not different between small and large males. Clutch size and insemination rate were different neither between small and large males nor between frequently and less frequently courting males. Thus, the male reproductive success will not be related to the male size, but directly to courtship frequency, indicating the random mating in this fish. There seemed to be fecundity advantage with size in female, and the consequent sexual difference in energy allocation will be responsible to the sexual dimorphism. We also discuss the low male-GSI in this promiscuous fish in which sperm competition hardly occurred.     

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.     

Female receptivity and male mate-guarding in the jewel spiderGasteracantha minax thorell (Araneidae)

In field populations, several male jewel spidersGasteracantha minax Thorell (Araneidae) may be found at the periphery of the orb web of a female, indicating that males may compete for fertilisation success. Laboratory experiments revealed that virgin femaleG. minax readily remate shortly after their first mating. However, they appear to enter a refractory period between 1 and 24 h postmating and respond aggressively to courting males. Males that have mated with a female initially defend her from rival males but cease to do so after the onset of the refractory period. These data can be interpreted within the context of mate-guarding and sperm competition. There is marked size dimorphism in this species, which may be the result of selection for protandry. In contrast with other orb-weaving spiders, this selection pressure does not seem to be counterbalanced by selection for larger male size through either sexual cannibalism or male-male competition.     

Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles

Sexual selection is thought to favor the evolution of secondary sexual traits in males that contribute to mating success. In species where females mate with more than one male, sexual selection also continues after copulation in the form of sperm competition and cryptic female choice. Theory suggests that sperm competition should favor traits such as testes size and sperm production that increase a male's competitive fertilization success. Studies of experimental evolution offer a powerful approach for assessing evolutionary responses to variation in sexual selection pressures. Here we removed sexual selection by enforcing monogamy on replicate lines of a naturally polygamous horned beetle, Onthophagus taurus, and monitoring male investment in their testes for 21 generations. Testes size decreased in monogamous lines relative to lines in which sexual selection was allowed to continue. Differences in testes size were dependent on selection history and not breeding regime. Males from polygamous lines also had a competitive fertilization advantage when in sperm competition with males from monogamous lines. Females from polygamous lines produced sons in better condition, and those from monogamous lines increased their sons condition by mating polygamously. Rather than being costly for females, multiple mating appears to provide females with direct and/or indirect benefits. Neither body size nor horn size diverged between our monogamous and polygamous lines. Our data show that sperm competition does drive the evolution of testes size in onthophagine beetles, and provide general support for sperm competition theory.     

Effect of male and female multiple mating on the fecundity, fertility, and longevity of diamondback moth, Plutella xylostella (L.)

Abstract:  The effect of diamondback moth (DBM), Plutella xylostella (Lep., Plutellidae) male and female multiple mating on fecundity, fertility, and longevity was studied. Males could mate for five times with virgin females during scotophase. The successful copulation rates, fecundity of female, and longevity of both females and males decreased when male mating times increased, whereas copulation duration increased. Correlation coefficient between copulation duration and male mating times was significant ( r  = 0.7358, P = 0.0001, spearman rank-order correlation). There were linear relationships between mating history of males and longevities of males and females, and regression relationships between them were significant. Mated females had similar daily reproductive pattern, which laid the most eggs on the first day after mating in spite of their mates' mating history. Virgin females laid some infertile eggs before they died. Most of the females mated once during their lifespan but 19.9% of females mated twice when one female kept with one male during scotophase. There were no significant differences in the fecundity, fertility and longevity between the single- and twice-mated females. Correlation coefficient between copulation duration and female mating times was not significant ( r  = 0.0860, P = 0.8575). Results suggested that DBM females may be monandrous. Multiple mating did not increase male or female mating fitness.     

Postmating sexual selection: the effects of male body size and recovery period on paternity and egg production rate in a water strider

The role of male body size in postmating sexual selection wasexplored in a semiaquatic insect, the water strider Gerris lateralis.To separate effects of male size per se from those due to numericsperm competition, male recovery period (shown here to be proportionalto ejaculate size) was manipulated independently of body sizein a factorial experiment where virgin females were mated firstwith sterile males and then with focal males. Both relativemale fertilization success and female reproductive rate were measured.The number of sperm transferred increased with male recoveryperiod, an effect that was mediated by longer copulation duration,but there were no effects of body size on ejaculate size. Neithermale size nor recovery period had any significant direct effectson male fertilization success. However, copulation durationinfluenced relative fertilization success, suggesting that malesable to transfer more sperm also achieved higher fertilizationsuccess. Females exercised cryptic female choice by modulatingtheir reproductive rate in a manner favoring large males andmales that were successful in terms of achieving high relativefertilization success. Thus, successful males gained a twofoldadvantage in postmating sexual selection. This study has important implicationsfor previous estimates of sexual selection in this group of insectsbecause pre- and postmating sexual selection will be antagonisticdue to limitations in male sperm production: males mating frequently(high mating success) will on average transfer fewer sperm ineach mating and will hence tend to fertilize fewer eggs permating (low fertilization success).     

Assortative Mating by Size in the American Rubyspot Damselfly (<Emphasis Type="Italic">Hetaerina americana</Emphasis>)

Assortative mating refers to the non-random nature of mating patterns between certain males and females. Thus, males and females may associate negative- or positively, based on different traits. Amongst these associations, assortative mating by size is one of the most common patterns found in natural populations of animals. Two main hypotheses have been proposed to account for the occurrence of assortative mating by size. First, it may be the result of mechanical, temporal, or physiological constraints. Second, it may occur in response to direct or indirect selection on mating preferences. Here we investigate whether the American rubyspot damselfly exhibits true assortative mating by size. Males of this species exhibit high levels of male-male competition, as they compete over territories, to which females are attracted for copulation. There is a documented large male body size advantage: the largest males are better able to hold their territories and thus secure more copulations. Our major results show that i) mated males are more likely to be larger than unmated males, whereas mated and unmated females tend to have similar body sizes; ii) H. americana exhibits true assortative mating by size; as such, this pattern is not driven by seasonal changes in the body sizes of males and females. We suggest that this mating pattern occurs in this species given the advantages of large male size, and the advantages of large female body size (i.e. higher fecundity). We believe that males may be able to evaluate a female’s reproductive value and exert mate choice.     

The adaptive significance of mate guarding in the soapberry bug,Jadera Haematoloma (Hemiptera: Rhopalidae)

Male soapberry bugs (Jadera haematoloma)face severe mating competition at the northern edge of their range due to male-biased adult sex ratios. Copulations lasting up to 11 days may serve a mate guarding function (encompassing four or more ovipositions), but copulation duration is highly variable, with some pairings lasting as little as 10 min. Data were gathered to describe factors that influence the reproductive costs and benefits of prolonged copulation. Estimated copulation durations (mean ± SD) were 20 ± 23 h in the lab and 50 ± 8 h in the field and were only weakly affected by sex ratio. Females mated for 5 min produced as many fertile eggs as those mated for 600 min laid; they became depleted of fertile sperm after about 25 days. In twicemated females, the first male's paternity was reduced by about 60%, and all females (N = 13) whose mates were removed experimentally mated again within an average of 6 min. The outcome of sperm competition on a perclutch basis was not highly predictable. The possibility of increased sperm displacement in longer copulations was not tested. Males often guarded females during oviposition and successfully defended them from intruding single males by recopulating. Such intrusions occurred in the majority of oviposition attempts observed in nature. Even though most females mated promiscuously, in a focal aggregation with a mean sex ratio of 2.2 ± 0.4 males/female, the interval between matings by males was commonly several days. Males appeared to respond facultatively to several aspects of the distribution and availability of females. The intensities of mating competition and sperm competition indicate that monogamous mate guarding should be favored over nonguarding in nature. Unpredicted brief. pairings may result from assessment by males of female reproductive value or of their own physical condition, or from female resistance.     

Sexual selection in hermit crabs: a review and outlines of future research

The information currently available on sexual selection in hermit crabs is reviewed to identify the role of males and females before, during and after mating. According to this information, possible mechanisms of male–male competition, female choice and/or sexual conflict are suggested. Important male components that may affect mating success include dragging the female shell, rotations of the female's shell and male cheliped palpations, and male size and/or shell characteristics (species and size). Possible female determinants of male mating/fertilization success include size (as an indicator of egg production capacity), signalling of sexual receptivity to males, delay from mate guarding to copulation and mating duration. Avenues for deeper exploration in males include the role of the number and morphometry of male sexual tubes during sperm transfer, and whether ejaculate size and sperm number can be adjusted with variable situations of sperm competition intensity and risk. In females it would be interesting to investigate the chemical and behavioural mechanisms affecting spermatophore breakage for sperm release and the variable duration from sperm transfer to spawning. Given these possibilities, and that sperm is externally deposited on the female's body but inside her shell (except for those species that do not use shells, e.g. Birgus , or species where shells are rather small and do not cover the body totally, e.g. Parapagurus ), we conclude that hermit crabs are unique subjects for separating male and female effects, particularly with respect to the applicability of current ideas in sexual selection such as female choice and sexual conflict. Some practical ideas are provided to disentangle both hypotheses using these animals.     

Effects of size at metamorphosis on stonefly fecundity, longevity, and reproductive success

Many organisms with complex life cycles show considerable variation in size and timing at metamorphosis. Adult males of Megarcyssignata (Plecoptera: Perlodidae) are significantly smaller than females and emerge before females (protandry) from two western Colorado streams. During summer 1992 stoneflies from a trout stream emerged earlier in the season and at larger sizes than those from a colder fishless stream, and size at metamorphosis did not change over the emergence period in either stream. We performed two experiments to determine whether variation in size at metamorphosis affected the fecundity, reproductive success and longevity of individuals of this stonefly species and if total lifetime fecundity was affected by the number of matings. In the first experiment, total lifetime fecundity (eggs oviposited) was determined for adult females held in small plastic cages in the field. Males were removed after one copulation, or pairs were left together for life and allowed to multiply mate. Most copulations occurred in the first few days of the experiment. Females in treatments allowing multiple matings had significantly lower total lifetime fecundity and shorter adult longevity than females that only mated once. Multiple matings also reduced longevity of males. Fecundity increased significantly with female body mass at emergence, but only for females that mated once. While multiple matings eliminated the fecundity advantage of large female body size, number of matings did not affect the significant positive relationship between body mass at metamorphosis and longevity of males or females. In a second experiment designed to determine if body mass at emergence affected male mating success, we placed one large and one small male Megarcys in an observation arena containing one female and recorded which male obtained the first mating. The large and the small male had equal probabilities of copulating with the female. Copulations usually lasted all night, and the unmated male made frequent, but unsuccessful attempts to take over the copulating female. Our data suggest that selection pressures determining body size at metamorphosis may operate independently on males and females, resulting in evolution of sexual size dimorphism, protandry, and mating early in the adult stage. We emphasize the importance of interpreting the fitness consequences of larval growth and development on the timing of and size at metamorphosis in the context of the complete life cycle. Received: 1 July 1997 / Accepted: 12 November 1997     

Mating tactics and male wing dimorphism in the damselfly,Mnais pruinosa costalis selys (Odonata: Calopterygidae)

Males of the damselfly,Mnais pruinosa costalis, exhibit wing color dimorphism: one form has orange wings, and the other hyaline wings which resemble female wings. The former is usually territorial and the latter uses sneaky mate securing tactics. When orange-winged males failed to establish territory, they became floaters that day. Hyaline-winged males perched around their territories and often, formed in tandem without any apparent courtship behavior when they found females. Their copulation frequency was higher and copulation duration longer than those of territorial males. A few females oviposited without remating. Total oviposition duration of females with which a hyaline-winged male mated was more than 32 min per male on average in a day Females that copulated with hyaline-winged males often remated with orange-winged residents before oviposition. Total duration of oviposition bouts of females after mating with floaters was short (15 min), while that with territorial residents was long (66 min). As a result, total oviposition duration of females with which an orange-winged male mated was about 40 min in a day. The reproductive success of the hyaline-winged males may be similar to that of the orange-winged males.     

Sexual behaviour and evolution of sexual dimorphism in body size in Jaera (Isopoda Asellota)

Individuals of the genus Jaera do not mate at random. In the species from the Mediterranean group, J. italica and. J. nordmanni, large males and medium sized females are at an advantage and their sizes are positively assorted. These effects are attributable to sexual competition between males. In the Ponlo-caspian species J. istri, no advantage of large males exists, but sexual selection could be the cause for a long passive phase prior to copulation and for normalizing selection upon female size at pairing. In the Atlantic species, J. albifrons, no selection can be ascertained.
Differential mating success in males appears as one of the causes of the evolution of sexual dimorphism in body size, which makes males larger, of equal size, or smaller than females according to the species. The reason for this reversal in dimorphism seems to differ in the two sexes. Sexual selection provides an explanation for the evolution of male size, while the interspecific changes in female length are more likely due to ecological factors.