Seminal fluid reduces female longevity and stimulates egg production and sperm trigger oviposition in a moth

Previous studies suggest that a number of factors in relation to mating may reduce female longevity and stimulate egg production and oviposition. However, it is still not clear whether these factors act on these parameters independently or in a collective way. Here we carried out a series of experiments including mating trials and seminal fluid injection to determine the factors responsible for reducing female longevity and stimulating egg production and oviposition in relation to mating in the moth Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Results show that seminal fluid and sperm work collectively to allow females to achieve maximum realized fecundity (number of eggs laid) in E. kuehniella but these factors play different roles in the process and their actions are independent. Seminal fluid signals females to allocate resources to ova, resulting in shorter longevity and greater egg production while eupyrene (not apyrene) sperm in the spermatheca trigger females to lay maximum number of eggs. We suggest that the receptors for seminal fluid signal may be located in the female reproductive tract and haemolymph, and those for sperm signal may be in the spermatheca. Hypotheses that females prolong their longevity by oosorption, physical injuries by males reduce female longevity, and mechanical stimulation by males triggers oviposition, are not substantiated in the present study.     

The effects of exposure to seaweed on willingness to mate, oviposition, and longevity in seaweed flies

Abstract  1. Large male seaweed flies (Diptera: Coelopidae) are more likely to mate than smaller males. This is due to sexual conflict over mating, by which females physically resist male attempts to copulate. In some species, large males are simply more efficient at overpowering female resistance.
2. Female reluctance to mate is likely to have evolved due to the costs of mating to females. In many dipterans, males manipulate female behaviour through seminal proteins that have evolved through sperm competition. This behavioural manipulation can be costly to females, for example forcing females to oviposit in sub-optimal conditions and increasing their mortality.
3. Previous work has failed to identify any ubiquitous costs of mating to female coelopids. The work reported here was designed to investigate the effects of exposure to oviposition sites ( Fucus algae) on the reproductive behaviour of four species of coelopid. Algae deposition in nature is stochastic and females mate with multiple males in and around oviposition sites. Spermatogenesis is restricted to the pupal stage and there is last-male sperm precedence. It was predicted that males would avoid wasting sperm and would be more willing to mate, and to remain paired with females for longer, when exposed to oviposition material compared with control males. Females were predicted to incur longevity costs of mating if mating increased their rate of oviposition, especially in the presence of algae.
4. The behaviour of males of all four species concurred with the predictions; however mating did not affect female receptivity, oviposition behaviour, or longevity. Exposure to algae induced oviposition and increased female mortality in all species independently of mating and egg production. The evolutionary ecology of potential costs of mating to female coelopids are discussed in the light of these findings.     

Presence of eupyrene spermatozoa in vestibulum accelerates oviposition in the silkworm moth,Bombyx mori

In the silkmoth, Bombyx mori, mating accelerates egg laying. Sterilized males did not induce females to oviposit, whereas artificial insemination was enough to accelerate oviposition. These findings showed that mechanical stimulation of the outer reproductive organs and the bursa copulatrix (BC) had no effect on oviposition. Factors included in seminal fluids also did not stimulate oviposition because neither implantation of female internal reproductive organs nor injection of the spermatophore extract into virgin females activated oviposition. Preventing sperm precedence by experimental removal of the BC or spermatheca inhibited activation of egg laying. More precise surgeries on the spermatheca showed that the main factor for eliciting oviposition was the presence of matured and fertile eupyrene spermatozoa in the vestibulum. Sperm were not effective unless they reached the vestibulum. Nerve transection and electrophysiological studies revealed that nerve 4 of the terminal abdominal ganglion was the pathway by which the mating signal was transmitted toward the higher central nervous system.     

延迟交配对昆虫生殖行为的影响以及与性信息素防治害虫的关系

对鳞翅目昆虫延迟交配对昆虫生殖力、卵孵化率、交配成功率、成虫寿命等进行了总结。雌虫延迟交配降低雌虫的生殖力、卵的孵化率及与雄虫成功交配率,但可以延长雌虫寿命。雄虫延迟交配降低雌虫的生殖力、卵的孵化率、产卵时间,雄虫的精子质量下降但寿命有所增加。已发现延迟交配在迷向法中控制害虫起着重要的作用,对进一步认识迷向法中不同作用机理以及延迟交配在迷向法防治害虫中的潜力进行了探讨。     

Mating and social contact change egg production and longevity in adult females of the mirid Lygus hesperus

There is frequently a tradeoff between fecundity and longevity, but the relationship is inconsistent across species and influenced by various exogenous and endogenous factors. Previous studies of Lygus hesperus Knight (Hemiptera: Miridae) established that egg production is promoted by insemination, at least temporarily, but little is known about the long‐term effects of mating and nonsexual interactions with conspecifics on egg production and female lifespan. To elucidate these relationships, survivorship and oviposition rate were tracked daily in females that were isolated or paired with a fertile male or another female throughout their adult lives. Mating rates were determined by postmortem examination. Results indicate that male‐specific stimuli accelerate female reproductive maturation, and that mating elevates oviposition rate. However, females paired with either a female or male companion had shortened lifespans, suggesting that social contacts exact a significant cost in this solitary species. Despite the negative impact of conspecific interactions and the finding that a singly mated female has sufficient sperm to fertilize a lifetime supply of eggs, many females were found to have mated more than once. Multiply mated females had higher sustained oviposition rates, lived longer, and had greater lifetime fecundities. Collectively, no strong evidence was found of a direct physiological link between fecundity and longevity, but environmental factors and mating were found to significantly influence both traits.     

Mating frequency and reproductive success in an income breeding moth,Mnesampela privata

The frequency of mating in insects is often an important determinant of female reproductive output and male sperm competition. In Lepidoptera that provide male nutrients to the female when mating, it is hypothesized that polyandry may be more prevalent. This is thought to be especially so among species described as income breeders; that is, in species who do not derive all their nutrients for reproductive output entirely from the resources obtained during the larval stage. We selected the geometrid moth, Mnesampela privata (Guenée) (Lepidoptera: Geometridae), to examine this hypothesis further. We found this species was best characterized as an income breeder with female weight on emergence positively correlated with total egg load but not with the number of eggs laid. Further, in accord with income breeders, females emerged with a partially developed egg load and lifetime fecundity was positively correlated with the number of oviposition days. However, in the laboratory we found that incidence of repeated matings or polyandry was rare. When moths were paired singly over their lifetime, only 4% of mated females multiple mated. When females were paired with three males concurrently, female mating success increased from 60 to 81% with multiple mating among mated females increasing to just 15%. Dissection of wild caught M. privata found that polyandry levels were also low with a maximum of 16.4% of females collected at any one time being multiple mated. In accord with theory, mating significantly increased the longevity of females, but not of males, suggesting that females acquire essential resources from male ejaculates. Despite this, multiple mated females showed a trend toward decreasing rather than increasing female reproductive output. Spermatophore size, measured on death of the female, was not correlated with male or female forewing length but was negatively correlated with the number of fertile eggs laid and female longevity. Smaller spermatophore width may be related to uptake of more nutrients by the female from a spermatophore. We discuss our findings in relation to income breeding and its relationship to polyandry in Lepidoptera.     

水稻二化螟的交配行为

在室内条件下,对水稻二化螟Chilo suppressalis的交配行为及能力进行了研究.结果表明：大多数二化螟雌蛾一生只交配一次,平均0.92次;而雄蛾具有多次交配能力,最多达4次,平均2.72次.二化螟雌蛾的日龄影响其交配率、交配起始时间和持续时间,随二化螟雌蛾日龄的增加,其交配率逐渐下降,交配起始时间逐渐提前,而交配持续时间逐渐上升.相反,二化螟雄蛾日龄对其交配率、交配起始时间和持续时间没有明显影响.交配日龄对二化螟雌蛾的生殖力也存在显著影响,随着二化螟雌蛾交配日龄的增加,雌蛾产卵量下降,卵孵化率降低,产卵期缩短,它们都与雌蛾交配日龄存在显著的负相关;而雌蛾产卵前期和雌蛾寿命随雌蛾交配日龄的增加而延长,与雌蛾交配日龄存在显著的正相关.但二化螟雄蛾交配日龄对雌蛾的生殖力没有明显影响,二化螟雄蛾一生都具有较强的交配繁殖能力.同时,不同交配史的雄蛾与雌蛾交配,对雌蛾的生殖力也没有显著影响.表明二化螟的交配活动是由雌蛾主导控制的.最后,对这些结果在二化螟性信息素防治中应用的可行性进行了探讨.在应用性信息素控制二化螟的实践中,可以在两方面取得实效,一是性信息素可以阻碍雌雄之间正常交配,降低交配率;二是可以推迟二化螟雌虫的交配,使其产卵量和卵孵化率降低.     

Copulation reduces male but not female longevity in Saltella sphondylli (Diptera: Sepsidae)

Mating more than once is extremely costly for females in many species, making the near ubiquity of polyandry difficult to understand. However, evidence of mating costs for males is much rarer. We investigated the effects of copulation on longevity of male and female flies (Saltella sphondylli). We also scrutinized potential fecundity and fertility benefits to females with differing mating history. Copulation per se was found to decrease the longevity of males but not that of females. However, when females were allowed to lay eggs, females that mated died earlier than virgin females, indicating costs of egg production and/or oviposition. Thus, although longevity costs of copulation are higher for males, reproduction is nevertheless costly for females. We also found no differences in fecundity or fertility relative to female mating history. Results suggest that polyandry may be driven by minor costs rather than by major benefits in this species.     

Male accessory gland proteins induce female monogamy in anopheline mosquitoes

The role of male accessory gland (MAG) secretions in inducing refractoriness to further mating in mosquitoes (Diptera: Culicidae) was established in the late 1960s. In a set of simple experiments, MAG extract was injected intra-thoraxically into the hemocoel of virgin Aedes aegypti (L.), Culex pipiens pipiens (L.) and Anopheles quadrimaculatus Say females. This subsequently caused most females to remain unmated when exposed to males. For anophelines these findings were later challenged by a study involving intra-abdominal injections of MAG extracts into Anopheles gambiae Giles s.l. and Anopheles albimanus Wiedmann females, which failed to induce refractoriness to further mating. These findings led to controversy about the respective role of sperm and accessory gland peptides in inducing female monogamy in Anopheles and are at odds with our current understanding of the mating process in Drosophila spp. (Diptera: Drosophillidae) and other dipterans. Here we confirm the function of MAG secretions in anophelines experimentally by showing that intra-thoracic injections in Anopheles stephensi Liston and in the M and S molecular forms of An. gambiae s.s. result in the expected female monogamy. Cross-injections of MAG extracts between the M and S molecular forms of An. gambiae , two cryptic taxa within An. gambiae s.s. which are thought to be undergoing incipient speciation, also elicited effective refractoriness, suggesting that the two sub-taxa have not diverged with regard to sex peptides responsible for female monogamy. Importantly, this also suggests that the rare cases of re-mating following cross-mating observed in this species may not be a form of reproductive barrier between molecular forms.     

Effects of delayed mating and male mating history on longevity and reproductive performance of the rice stem borer, Chilo suppressalis (Walker) (Lep., Pyralidae)

Abstract:  The mating potential, effects of delayed mating and male mating history on longevity and reproductive performance of female rice stem borer (RSB), Chilo suppressalis , were investigated under laboratory conditions. Given the opportunity, RSB males copulated an average of 2.7 times, while females generally mated only once. Females were more severely affected by mating delay than males in terms of female longevity and reproductive performance. With increasing age at mating, females' longevity increased, while oviposition period, fecundity and egg fertility decreased. Mean fecundity and egg fertility of females mated 1 and 7 days after emergence were 251.3% and 99.2%, and 96.2% and 75.5% respectively. Both were reduced significantly when female mating was delayed beyond 4 days after emergence. However, irrespective of the first mating age and different mating history of the males, the results indicated that both did not result in a significant difference in the quality of their contributions to female longevity and reproductive performance. The results obtained in this study are discussed in relation to the potential effect on pheromone control of RSB.     

Factors involved in the post-copulatory neural inhibition of pheromone production in Choristoneura fumiferana and C. rosaceana females

Normal mating lasts approximately 3 h in Choristoneura fumiferana and C. rosaceana. Data generated from interrupted matings showed that the act of mating did not suppress pheromone production (pheromonostasis) in either species although, in C. rosaceana, pheromone titre declined slightly the night following mating. In both species the migration of sperm to the spermatheca (SP) occurred several hours after mating, and coincided with a significant and permanent depression in pheromone titre, as well as egg fertilisation and oviposition. However, disrupting matings within 2 h of the onset resulted in oviposition patterns similar to virgins in both species, with mostly infertile eggs being laid by C. fumiferana females while oviposition was totally inhibited in C. rosaceana. The transection of the ventral nerve cord (VNC) 1 h post-mating did not result in the depression of pheromone titres the following night in either species but if the VNC was transected 3 h post-mating, pheromonostasis was observed. While 25% of C. fumiferana females had sperm in their SP 2 h after mating, it took at least 4 h in C. rosaceana. This suggests that while the physical presence of sperm in the SP may play some role in the termination of pheromone production in C. fumiferana, other factors must trigger the neural signal that elicits pheromonostasis in both species. A better understanding of the temporal dynamics of both apyrene and eupyrene sperm within the different parts of the female reproductive system might clarify these interspecific differences.     

Effect of mating status on the fecundity of a cricket,Teleogryllus emma

Abstract Fecundity in some insects is affected by mating status. The effect of mating status on the fecundity and total egg production of Teleogryllus emma (Ohmachi et Matsumura) (Orthoptera: Gryllidae) was examined in this study. The results showed that the pre‐oviposition period was shorter for amphigonic females than that for virgin females. However, no significant difference in pre‐oviposition was found between amphigonic females and those that had mated with a male with either the phallodeum or testes extirpated. There is no difference in adult longevity between the above four groups. The fecundity and total egg production were much higher in amphigonic females than in those controlled under the three non‐amphigonic treatments. The females of T. emma that mated with the testes‐extirpated males produced more eggs (up to two‐fold more) than both the virgin females and those that mated with the phallodeum‐extirpated males, but there was no difference between them. The fecundity‐enhancing substances transferred from male to female can stimulate the female to produce more eggs, but this stimulation has to occur in collaboration with sperm.     

Reproductive biology and function of multiple mating in the mating system of a tree cricket,Truljalia hibinonis (Orthoptera: Podoscritinae)

A tree cricket,Truljalia hibinonis, is known to show a novel sperm removal during copulation. The pattern of copulations and ovipositions showed that the sperm removal functioned to increase reproductive success for sperm removing males. The sperm removal by males evolves under the system in which female accept multiple mating. The possible benefits of multiple mating for females are examined. Multiple mating did not seem to be necessary for avoiding sperm depletion, because females stored huge number of sperm in their sperm storage organ after finishing oviposition. The ingestion of metanotal secretion during copulation also had no effect on increasing fecundity and egg size. However, mating experience may have a positive effect on increasing fecundity slightly, though there were no differences between once- and twice-mated females. The other possible benefits for each male and female are discussed.     

Nuptial gifts and female fecundity in the neotropical katydid Conocephalus ictus (Orthoptera: Tettigonidae)

In general, female fitness is greatly increased in gift‐giving insects. In katydids, this nuptial gift consists of a gelatinous mass produced by accessory glands: the spermatophylax, which is attached to the ampulla. During mating, males of the neotropical katydid Conocephalus ictus transfer a spermatophylax that is ingested by the females. Fecundity, egg‐laying rate and longevity were higher in females that consumed the spermatophylax than in those that did not. Also, female receptivity turned off after mating. Females actively rejected other males by hitting them with their forelegs and moving away. Their refractory period lasted as long as 17 d. Only a few females accepted a 2nd mating and died a few days later. In C. ictus, spermatophylax consumption can be beneficial for both males and females. On one hand, the compounds in the spermatophylax or the ejaculate could prevent or delay females from copulating with rivals, thus avoiding sperm competition. On the other hand, such compounds can improve the females’ opportunity to increase their lifespan and fecundity. Moreover, a rise in egg‐laying rate may lower the risk of female prereproductive death caused by rapid oviposition. In any case, the boost in female egg laying might also be beneficial for males because their number of offspring increases.     

Male accessory gland derived factors can stimulate oogenesis and enhance oviposition in Helicoverpa armigera (Lepidoptera: Noctuidae)

In Helicoverpa armigera, female moths began to lay eggs on the third day after emergence. Mating stimulated earlier egg maturation/oogenesis (P = 0.002) and oviposition (P < 0.01). We established a suitable bioassay model for the influence of male accessory glands (MAG) on the physiology of virgin females: Crude extracts of MAG (2- to 3-day-old) were injected into 2-day-old virgin females, and the injected females were dissected 20 h after mating. It was shown that crude extracts of MAG stimulated earlier egg maturation (P < 0.001) and oviposition (the oviposition ratio was more than 2 times the ratio of the control). Proteinaceous components in crude extracts purified by fractionation and sub-fractionation in reverse phase high performance liquid chromatography also stimulated earlier egg maturation (P < 0.01) and ovipositon (more than 2 times the ratio of the control), and we called them the oogenesis and ovipostion factors (OOSF). With SDS-PAGE, the molecular mass of the bands from OOSF was estimated to be between 55-66 KD. Arch.     

Material Benefits from Multiple Mating in Female Mealworm Beetles (Tenebrio molitor L.)

In yellow mealworm beetles (Tenebrio molitor), females are sexually receptive throughout their adult lives. We examined how access to mates affected female fecundity by varying the number of matings per female and quantifying cumulative egg production. Also, we dissected females at successive intervals after a single mating to assess the relationship among time since mating, sperm supplies, egg load, and oviposition rate. Females that mated at intervals greater than 2 days did not produce as many eggs as females that mated every 2 days or were allowed to mate ad libitum. Dissections showed that the amount of sperm remaining in a female spermatheca was correlated with the number of eggs she had laid recently, which suggests sperm replenishment as the material benefit gained through multiple mating. However, females mate more frequently than necessary for sperm replenishment, and therefore material benefits alone may not fully explain the continuous receptivity of T. molitor females.     

柳毒蛾繁殖生物学的初步观察

【目的】为了明确柳毒蛾Leucoma salicis(Linnaeus)交配的日节律高峰,温度和不同交配持续时间处理对成虫寿命、产卵量和孵化率等繁殖生物学的影响。【方法】将新羽化的柳毒蛾成虫置于养虫笼中,观察交配的日节律高峰,并统计不同温度和不同交配持续时间处理下的成虫寿命、产卵量和孵化率。【结果】成虫在羽化当晚的后半夜凌晨开始交尾,次日晚上开始产卵。成虫交配集中在羽化翌日凌晨3:00—5:00之间,高峰为4:00。产卵高峰都出现在2日龄成虫,但是,25℃下成虫交配持续时间(9.2 h)显著短于28℃(11.8 h)。交配持续时间为30、60和300 min的处理,雌成虫平均寿命显著长于对照(对照9.2 h),雄虫仅60 min的处理显著长于对照。同时,极短的交配持续时间(30 min)显著降低雌虫的产卵量和孵化率。【结论】试验明确了成虫交配的日节律高峰,在适宜的温度范围内(25~28℃),雌雄成虫的寿命、单雌总产卵量无显著差异,交配持续时间明显影响成虫寿命、产卵量和卵孵化率。     

Increased fecundity, as a function of multiple mating, in an arctiid moth, Utetheisa ornatrix

1. Female Utetheisa ornatrix mate multiply and may receive up to thirteen spermatophores. Spermatophores provide the female not only with sperm but also with a nuptial gift of pyrrolizidine alkaloid that she transmits to the eggs, protecting them against predation. Thus, through multiple mating the female accrues nuptial gifts that add to the defence of her offspring.
2. Multiple mating in female U. ornatrix brings about increases in fecundity, but not in longevity or egg mass. These increases occur through the third mating; the fourth and fifth matings, however, have no additional effect on fecundity.
3. These results, taken with the fact that spermatophores are sizeable and are digested within the female, suggest that they bear nutritive gifts that the female uses in egg construction. Multiple mating thus allows females to accrue the resources to build additional eggs.
4. These results are discussed in relation to the potential benefits accruing to donating such gifts and to male and female mating strategies.     

Asymmetric effects of adult nutrition on reproductive success of male and female Diaeretiella rapae (Hymenoptera: Aphidiidae)

The role of diet supplements (honey, water or no supplements) on egg maturation, oviposition strategy and longevity of the parasitic wasp Diaeretiella rapae McIntosh (Hymenoptera: Aphidiidae) is investigated. Parasitoids feed as larvae on hosts to acquire nutrition for growth and development, and further gain additional resources during their adult stage by feeding on either host or nonhost resources. The additional resources acquired by adults can help them to increase their reproductive activity or life expectancy, or both. Diaeretiella rapae females emerge with some developed eggs and no additional resources are required for egg maturation or successful oviposition. Females are able to oviposit and produce viable offspring immediately after emergence, and the number of eggs left in the ovaries of females decreases with subsequent oviposition, suggesting that ovigeny index of D. rapae is inclined towards pro‐ovigenic status. When unmated males and females are offered honey solution, females are attracted to it, whereas males display courtship and make mating attempts but then feed on honey after mating. The oviposition efficiency of female D. rapae increases by 30% when they feed on honey compared with when starved. Honey‐fed D. rapae adults live significantly longer (almost twice as long) than starved adults. Honey‐fed females deprived of hosts live longer than those offered hosts regularly. The positive effects of honey‐feeding on longevity are greater in females than in males. Taken together, the results of the present study suggest that the provision of additional resources to adult D. rapae parasitoids could enhance their life expectancy and parasitism efficiency in biological control programmes.     

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

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.