Copulatory courtship signals male genetic quality in cucumber beetles

In the spotted cucumber beetle, Diabrotica undecimpunctata howardi (Coleoptera: Chrysomelidae), males court females during copulation by stroking them with their antennae. Stroking occurs exclusively during the first stages of copulation, after a male has penetrated a female's vaginal duct but before he is allowed access to her bursa copulatrix. Females accept the spermatophore of fast-stroking males and reject those of slow-stroking males by relaxing or constricting muscles distorting the vaginal duct. Here, we measure the repeatability of stroking behaviour within males, examine the effect of losing one antenna on male attractiveness and test whether such female control results in direct phenotypic benefits for the discriminating female or indirect genetic benefits that appear in her offspring. We also use a half-sibling design to quantify the variance and heritability of stroking speed and endurance. Female beetles were paired with a male that was known to stroke either quickly or slowly. No difference was found in the resulting fecundity or egg-hatching rate of the females, or in the survivorship, development rate, size, age at first reproduction or fecundity of their offspring indicating that no direct benefits are gained by discriminating among males on the basis of stroking speed. There were, however, good-genes benefits for the mates of fast-stroking males. Offspring of fast-stroking fathers were also fast strokers and were more likely to be accepted as mates than offspring of slow-stroking fathers. There was substantial variance among sires in stroking speed and endurance and the heritability of each trait was high. The antennal stroking rate was highly repeatable in successive mating attempts and males with only one antenna were not accepted as mates. The repeatability within males, variability between males and heritability between generations of copulatory stroking combine to provide females with a reliable and honest signal of the genetic quality of courting males.     

Search behavior of pheromone-stimulated potato tuber moth males (Lepidoptera: Gelechiidae)

The processes of female searching by male potato tuber moths,Phthorimaea operculella, were analyzed. The behavioral components to copulation were antennal cleaning, quiescence, walking, wing fanning, contact with female, hair brush display, copulation attempt, and copulation. Males did not always succeed in mating on their first attempt. Searching behavior of males changes to “area-restricted searching” after contact with a female. Males could, therefore, find females efficiently and copulate.     

Effects of male mating interval on spermatophore formation,transfer, and subsequent female receptivity and fecundity in the sorghum plant bug,Stenotus rubrovittatus

Males of the sorghum plant bug, Stenotus rubrovittatus (Matsumura) (Heteroptera: Miridae), transfer a spermatophore to females during copulation. After a 1‐day interval between the first and second copulation, males transferred both sperm and a spermatophore to females during the second copulation. However, when male mating interval was <1 h, they transferred sperm but no spermatophores to females during the second copulation. Therefore, the male mating interval probably produces two types of mated females, those with and those without a spermatophore. Mated females of S. rubrovittatus do not remate for at least 3 days after mating, even when courted, and lay more eggs than virgin females at the beginning of the oviposition period. The effects of spermatophores on female sexual receptivity and fecundity were examined using mated females with or without a spermatophore. Only one of the 40 (2.5%) mated females with a spermatophore remated, whereas 10 of the 26 (38.5%) without a spermatophore remated. Furthermore, mated females with a spermatophore laid more eggs than those without a spermatophore. These results suggest that spermatophores participate in reducing female sexual receptivity and enhancing female fecundity in S. rubrovittatus.     

The effects of copulation duration in the bruchid beetle Callosobruchus maculatus

Control over copulation duration is a potentially importantgenerator of sexual conflict that has received little empiricalattention. The copulatory behavior of the bruchid beetle Callosobruchusmaculatus may reflect a sexual conflict over copulation duration.Males have spines on their intromittent organs that puncturethe female reproductive tract, and females kick their matesduring copulation. If females are prevented from kicking, copulationslast longer and the injuries females sustain are more severe.Males supposedly use the spines as anchors to prolong copulationduration, and females kick to terminate copulations. We manipulatedcopulation duration experimentally and quantified its effectson male and female fitness components to test whether or notthere is a conflict over copulation duration in C. maculatus.Females did not suffer from long copulations but instead experiencedincreased lifetime fecundity. Ejaculate size increased withcopulation duration, and females apparently derive materialbenefits from the ejaculates. Males that mated first and hadlong copulations were relatively unsuccessful when competingwith sperm from other males. However, there was a trend forfemale remating propensity to decrease with long copulationdurations, and first males may therefore also benefit from longcopulations. The copulation duration of the second male to matedid not have a significant effect on sperm precedence. We concludethat even though it seems likely that the male spines have evolvedto act as an anchor during copulation, there seems to be littleconflict over copulation duration per se in C. maculatus.     

Male Condition, Female Choice, and Extreme Variation in Repeated Mating in a Scaly Cricket, Ornebius aperta (Orthoptera: Gryllidae: Mogoplistinae)

Mating in the scaly cricket Ornebius aperta often includes the transfer of many spermatophores to individual females during extended copulatory interactions. We manipulated male condition in staged matings to determine whether this could explain variation in the number of repeated copulations seen across pairs. Males on a high nutrient diet were in good condition, were more likely to mate repeatedly, and transferred more spermatophores on average than low-diet males (in poor condition). High-diet males were more likely to produce a vibratory signal that increased female receptivity to repeated mating attempts. Courtship and copulatory interactions were always terminated by females, and in every case males had already formed a spermatophore when deserted by females. We conclude that variation in male repeated mating success may be due to female choice rather than an inability or unwillingness of low-diet males to produce spermatophores.     

Functional and nonfunctional female receptivity signals in the parasitoid wasp Spalangia endius (Hymenoptera: Pteromalidae)

In many taxa, females signal during courtship when they are receptive. However, just because a female signals does not mean that the male responds to the signal. This study examines female signaling of receptivity (readiness to copulate) and male response in the parasitoid wasp Spalangia endius Walker. Females folded their antennae against their heads when they were receptive, and antennal folding has been shown to be effective in eliciting male copulation attempts in a confamilial. However, male S. endius did not respond to antennal folding: males did not contact the female's antennae during courtship, and how quickly a male attempted copulation was independent of whether or not the female had antennae. Males courted from on top of the female's abdomen and appeared to detect receptivity directly from the female's abdomen rising as her genital orifice opened. On females whose abdomens did not rise, initiation of male copulation attempts were delayed but not eliminated. Based on its current lack of function as a receptivity signal and on comparisons to published reports of mating behavior in confamilials, we hypothesize that female antennal folding at receptivity is a vestigial trait in S. endius.     

Spermatophore expulsion in the carrion beetle Silpha perforata (Coleoptera: Silphidae)

Silphinae (Coleoptera: Silphidae) is an abundant decomposer that plays important roles in the ecosystem. However, there is little information about the life history of this taxon. We found sperm displacement behavior in carrion beetle Silpha perforata. Copulating males bit the female's antenna strongly and inserted the penis into the partner's genital organ more than once. We found a white substance on the tip of penis during copulation. We examined whether this white substance is a previous male's spermatophore, which was removed from the mating partner. When females were dissected just after mating, the same substance that often presents on the penis of mating males was found in the bursa copulatrix of females, although the bursa copulatrix of virgin females was empty. Male behavior during copulation with females of different mating history was also observed to confirm that the removal of spermatophores was observed only in copulation with females that have the spermatophores of previous males. Consequently, we estimated that S. perforata males removed spermatophores of previous males from mating partners. In addition, we dissected the males frozen during copulation, and inspected the penis morphology. This observation revealed that the apical part of the penis was usually hidden in the basal part of penis, but expanded and appeared during insertion. This apical part had many spines, which play an important role in sperm displacement and sexual conflict in some species. These results indicate that there is the sperm competition in S. perforata. This is the first report on sperm competition in Silphinae.     

Copulation in the neritic chaetognath Sagitta crassa

The number of spermatophores found attached to Sagitta crassa,the dominant chateognath in Tokyo Bay, ranged from one to four.Individuals with one spermatophore were most abundant, accountingfor 70% of chaetognaths with spermatophores (A). Using the meanminimum body length of chaetognaths with spermatophores (A),those without spermatophores were subdivided into two categories:those >7 mm (B) were considered to be mature animals, andthose <7 mm (C) to be immature. The ratio of chaetognathswith spermatopbores (A) to all chaetognaths (A+B+C) varied withtime, with high values from 0040 through 0120 h as in a previousstudy. Variations in the ratio of chaetognaths with spermatophores(A) to all adults (A+B) showed a pronounced peak at 0100 h.Thus, it was confirmed that copulation of S. crassa is a periodicactivity with a peak soon after midnight. Most of the chaetognathpairs exchange one spermatophore. The frequency of copulationis considered to be two times per night at most because thechaetognaths have a single pair of seminal vesicles. However,the presence of chaetognaths with 3–4 spermatophores suggeststhat occasionally a reciprocal exchange of spermatophores doesnot occur. This could be called false copulation. It is suggestedthat copulation in S. crassa including false copulation occursat most four times per night.     

Nuptial gifts and sexual selection in photinus fireflies

The phenomenon of nuptial gift transfer during mating occursacross a remarkably wide range of taxa, and such male donationsare likely to influence both pre-copulatory and post-copulatorysexual selection. This paper reviews what is known about nuptialgifts in Photinus fireflies (Coleoptera: Lampyridae), and discussesthe adaptive significance of spermatophores in firefly matingsystems. During copulation Photinus males transfer a spiral,gelatinous spermatophore to the female: sperm are released intothe female's spermatheca for storage, while the remainder ofthe spermatophore disintegrates within a specialized gland.Radiolabelling studies indicate that male-derived protein isused to help provision the female's developing oocytes, andmultiply-mated females show increased fecundity. As most Photinusadults do not feed, these studies suggest that females shouldcontinue to forage for matings to supplement their diminishinglarval reserves, even after they have gained sufficient spermto fertilize their eggs. Male spermatophore mass declines acrosssequential matings, and smaller spermatophores are associatedwith lower paternity success in situations where males competefor fertilizations. Declining spermatophore size across sequentialmatings may thus lead to diminishing reproductive returns forfirefly males. Taken together, these results suggest that seasonalchanges in nuptial gift availability may contribute to reversalsof traditional courtship roles, with male choice and female-femalecompetition occurring as spermatophore availability declines.     

A Review of Size at Maturity in Male Tanner (Chionoecetes bairdi) and King (Paralithodes camtschaticus) Crabs and the Methods Used to Determine Maturity

This paper reviews existing studies on the size of sexual maturityfor male Tanner or snow crab (Chionoecetes bairdi), a brachyuran,and the anomuran red king crab (Paralithodes camtschaticus).In this report the term sexual maturity is denned as the abilityto reproduce. A variety of indirect and direct methods thathave been used to determine maturity are reviewed. Examiningthe vas deferens for the presence of spermatophores was usefulin determining the size at which males first become mature.Breeding experiments in the laboratory demonstrated that mostmales, from both species, that produced spermatophores couldbreed with soft-shelled mates. Males of both species can breedat smaller sizes than do females. Morphometric techniques basedon reproductive tract weights and chela morphometry overestimatedthe sizes at which males mature in both species. Previous experimentsfor Tanner crab, which have internal fertilization, suggestsmall mature males can fertilize two to five females. Breedingexperiments showed recently matured red king crab do not appearto be able to fertilize more than one female per breeding season,while males nearing harvestable size can fertilize more thanone female. Breeding experiments and in situ observations of grasping pairsappear to be the most feasible methods for identifying malesize at maturity for these species. The value of morphometricestimations for determining when males mature is questionable.     

Nuptial gift in the spider Pisaura mirabilis maintained by sexual selection

The nuptial prey gift in the spider Pisaura mirabilis has been suggested to function as a male protection against sexual cannibalismduring courtship and mating. This hypothesis together withtwo alternatives—male mating effort and paternal investment hypotheses—were tested in a laboratory experiment withsexually inexperienced males and females. One group of malesoffered no gift to the female while three groups of males offeredsmall, medium, or large sized gifts, respectively. No malewas cannibalized among 82 trials. Aggression was observed onlyin encounters where a gift was presented. Males without a gift courted females, and 40% of these males managed to copulate,compared to 90% of males offering a gift. The copulation durationwas positively correlated with gift size. In general, the femaleterminated the copulation and ran away with the gift. The proportionof eggs fertilized increased with copulation time. Presenceor size of the nuptial gift did not affect female fecundityor spiderling size significantly. The results refute the hypothesesof sexual cannibalism and paternal investment. The nuptialgift represents a male mating effort; it entices the femaleto copulate, facilitates coupling during copulation, and byprolonging copulation it may increase the amount of sperm transferred.I conclude that the nuptial prey gift in Pisaura mirabilisis maintained by sexual selection.     

Mating tactics and courtship behavior inCleogonus rubetra (Fabricius) (Coleoptera: Curculionidae)

Females of the tropical weevilCleogonus rubetra oviposit into fruits of the leguminous treeAndira inermis, and larvae develop in the pulp and seed of these fruits. We hypothesized three alternative tactics by which males might secure matings. By using focal observations of males and by evaluating predictions specific to each hypothesis, we demonstrate that males search within aggregations of conspecifics for receptive females, and upon finding a suitable partner, males mount and perform courtship behavior consisting of stroking the eyes and sides of the female's abdomen. Males also stridulate and emit a sequence of short buzzing sounds. While mounted, males actively prevent rival males from mating with their partner. Males defend their mates for a mean duration of 3.7 h (including copulation). As predicted, paired males were larger than solitary individuals, although the difference was marginally nonsignificant. The overabundance of fruits relative to males, the prolonged period during which females are active, and the probability of last male sperm precedence are factors that may have contributed to the evolution of this female-defense tactic by males. Paired females were significantly larger than solitary females. We observed no competition among females for mates, and the correlation between elytron length of paired males and females was not significant.     

Factors Affecting Sperm Quality Before and After Mating of Calopterygid Damselflies

Damselflies (Odonata: Zygoptera) have a more complex sperm transfer system than other internally ejaculating insects. Males translocate sperm from the internal reproductive organs to the specific sperm vesicles, a small cavity on the body surface, and then transfer them into the female. To examine how the additional steps of sperm transfer contribute to decreases in sperm quality, we assessed sperm viability (the proportion of live sperm) at each stage of mating and after different storage times in male and female reproductive organs in two damselfly species, Mnais pruinosa and Calopteryx cornelia. Viability of stored sperm in females was lower than that of male stores even just after copulation. Male sperm vesicles were not equipped to maintain sperm quality for longer periods than the internal reproductive organs. However, the sperm vesicles were only used for short-term storage; therefore, this process appeared unlikely to reduce sperm viability when transferred to the female. Males remove rival sperm prior to transfer of their own ejaculate using a peculiar-shaped aedeagus, but sperm removal by males is not always complete. Thus, dilution occurs between newly received sperm and aged sperm already stored in the female, causing lower viability of sperm inside the female than that of sperm transferred by males. If females do not remate, sperm viability gradually decreases with the duration of storage. Frequent mating of females may therefore contribute to the maintenance of high sperm quality.     

Sexual conflict and cryptic female choice in the black field cricket, Teleogryllus commodus

The prevalence and evolutionary consequences of cryptic female choice (CFC) remain highly controversial, not least because the processes underlying its expression are often concealed within the female reproductive tract. However, even when female discrimination is relatively easy to observe, as in numerous insect species with externally attached spermatophores, it is often difficult to demonstrate directional CFC for certain male phenotypes over others. Using a biological assay to separate male crickets into attractive or unattractive categories, we demonstrate that females strongly discriminate against unattractive males by removing their spermatophores before insemination can be completed. This results in significantly more sperm being transferred by attractive males than unattractive males. Males respond to CFC by mate guarding females after copulation, which increases the spermatophore retention of both attractive and unattractive males. Interestingly, unattractive males who suffered earlier interruption of sperm transfer benefited more from mate guarding, and they guarded females more vigilantly than attractive males. Our results suggest that postcopulatory mate guarding has evolved via sexual conflict over insemination times rather than through genetic benefits of biasing paternity toward vigorous males, as has been previously suggested.     

Mating Behavior of Cephalonomia tarsalis (Ashmead) (Hymenoptera: Bethylidae) and the Effect of Female Mating Frequency on Offspring Production

The courtship behavior of Cephalonomia tarsalis, a solitary semiectoparasitoid of Oryzaephilus surinamensis, was investigated in the laboratory. Courtship behavior includes a series of stereotypic movements. Males play the most active role, executing the majority of courtship action, and females respond with relatively limited observable behaviors. Males typically keep antennae still during encounters with females prior to mounting, which may be correlated with recognition of the female's sexual status. After mounting, males display a series of movements on females, such as antennae touching female's antennae, antennae or mouth touching female's head or thorax, and walking around on female, which may serve to stimulate females towards increased receptivity. Females signal receptivity by assuming a stereotypical posture of remaining stationary, with head down, and antennae still in front of the body. The male then inserts his aedeagus and the pair copulates. After an average of 40.4 s of copulation, females signal the end of copulation by waving the antennae and moving away from the copulation site. Males continue copulating for a short time after females start moving but dismount soon thereafter. After dismounting, the two wasps move away from each other immediately, and they typically begin grooming. Neither males nor females exhibit mating preference based on mate's mating status in both choice and no-choice tests. The male is polygynous and the mated female can mate multiple times within the first 3 days after starting oviposition. However, female mating frequency does not affect the production of female progeny.     

Daily production of spermatophores, sperm number and spermatophore size in two eriophyoid mite species

Under dissociated sperm transfer, (non-pairing) males deposit spermatophores on a substrate, while females seek spermatophores and pick up sperm on their own. Spermatophore expenditures of non-pairing males should be high, due to the increased uncertainty of sperm uptake by a female. In this study I examined spermatophore expenditures in two eriophyoid species that differed in the degree of dissociation between sexes: (1) Aculus fockeui (Nalepa and Trouessart) males rarely visit quiescent female nymphs (QFNs), and mostly deposit spermatophores all over the leaves, whereas (2) Aculops allotrichus (Nalepa) males guard QFNs for many hours and deposit several spermatophores beside them. Males of both species were collected from the field and tested in solitude. Aculus fockeui males deposited on average 19.1 spermatophores per day, whereas A. allotrichus deposited only 3.6 spermatophores per day, and had a very large coefficient of variation. Males and spermatophores of A. allotrichus were significantly smaller and contained less sperm than those of A. fockeui. In both eriophyoids, spermatophore size was fitted to the size of female genitalia and the height of females. The ratio between the diameter of spermatophore head and the width of a female genital coverflap was 0.6, whereas the ratio between the female leg and the length of spermatophore stalk was 0.5. Several factors could be responsible for the discrepancy in spermatophore expenditures between species. Among other factors, the effects of male size, male reproductive strategy and female genitalia size on spermatophore output and size of spermatophores are discussed.     

Sex differences in copulation attempts in wild bonobos at Wamba

We examined sex differences in copulation attempts in a group of wild bonobos at Wamba, Congo, by analyzing the behavioral sequence. Most copulation attempts were initiated by approach or courtship behaviors by males. Males showed these behaviors when they were more than 5 m from females, whereas females did so only when males solicited them from within 5 m. Most copulations involved females showing perineal swelling, because males solicited those females more frequently and those females accepted copulation more frequently than did females in the non-swelling phase. Nevertheless, males solicited females in the non-swelling phase in one-third of copulation attempts, and those females accepted copulation in half of those attempts. This is markedly different from chimpanzees, in which sexual behaviors almost exclusively involve females in the swelling phase. The perineum of female bonobos during the non-swelling phase is soft and wrinkled but fairly large, which may attract males to some extent. The low, but existing, attractiveness and receptivity of female bonobos during the non-swelling phase might have evolved to control sexual competition among males and provide higher social status for females.     

No direct or indirect benefits to cryptic female choice in house crickets (Acheta domesticus)

Cryptic female choice in crickets occurs through the prematureremoval of a male's spermatophore after copulation, which terminatessperm transfer. Although it is known that this behavior candirectly influence the paternity of offspring, its effects onfemale fitness have not been directly assessed. We tested thehypothesis that spermatophore removal by female house crickets(Acheta domesticus) confers fitness benefits on females, byrandomly assigning mates to females but permitting some femalesto freely remove spermatophores after mating (cryptic-choicetreatment) while forcing others to accept complete ejaculates(no-choice treatment). Although there was about a two-fold differencein the volume of ejaculate received by females of the two treatments,there were no significant differences in female longevity, reproductiveoutput, or offspring quality, as measured by offspring massand developmental time. Although differential spermatophoreremoval by females imposes strong sexual selection on males,the absence of a clear treatment effect suggests that femalesobtain no direct or indirect genetic benefits through theirpostcopulatory mating preferences.     

Mating strategies based on foraging ability: an experiment with grasshoppers

Female mate choice and the benefits of this behavior are criticalaspects of Darwinian sexual selection, but they are seldom documentedbecause it is difficult to identify the male trait(s) that femalesmay be seeking. We conducted experiments with grasshoppers (Melanoplussangutnipes: Orthoptera, Acrididae) to examine this behavior.Males that feed more intensively and select a diet mix thatpermits greater food intake (food intake per body mass per time)in laboratory trials were preferentially selected by females.These better foraging males on average provide greater paternalinvestment (greater spermatophore mass) to the female, whichincreases her reproductive rate (eggs produced per body massper time). However, paternal investment may not entirely explainfemale choice of better foraging males, because these maleswere still selected even if they had their food intake restrictedor had been allowed to recently mate, which reduces spermatophoreproduction. Furthermore, males change their mating strategyin response to female choice and the foraging abilities of surroundingmales. Poorer foraging males attempt forcible copulation ratherthan displaying and allowing female choice. A male will facultativelyswitch between these strategies depending on the foraging abilitiesof the surrounding males. While females attempt to reject forciblecopulation, forcible copulation reduces the frequency with whichfemales successfully copulate with better foraging males. Therefore,males that are less "attractive" to females adopt alternativemating strategies to counter female choice which would excludethem from mating.[Behav Ecol 7: 438–444 (1996)]     

Complex Courtship Behavior in the Striped Ground Cricket, Allonemobius socius (Orthoptera: Gryllidae): Does Social Environment Affect Male and Female Behavior?

Complex courtship in the striped ground cricket, Allonemobius socius, involves a series of behaviors alternating between the sexes. We examined if complex courtship allows either or both genders to evaluate their mate and how mating behavior changes in different social environments. While complex courtship may allow discrimination by both sexes, here only females exhibited a preference. Males did not alter their courtship behavior or change spermatophore size for different size females. In contrast, females initiated copulation more quickly with bigger males possessing bigger spermatophores. In a different social environment (additional male, female, or both), males were less likely to omit courtship songs and female discrimination of mates changed. The distinct differences in male and female behavior suggest that subtle changes in social environment can have important consequences in structuring courtship and mating behavior.