Impact of mating status on egg-laying and superparasitism behaviour in a parasitoid wasp

Most parasitoid female wasps can distinguish between unparasitized and parasitized hosts and use this information to optimize their progeny and sex allocation. In this study, we explored the impact of mating on oviposition behaviour (parasitism and self‐ and conspecific superparasitism) on both unparasitized and already parasitized hosts in the solitary parasitoid wasp Eupelmus vuilleti (Crw.) (Hymenoptera: Eupelmidae). Virgin and mated females had the same oviposition behaviour and laid eggs preferentially on unparasitized hosts. The sex ratio (as the proportion of females) of eggs laid by mated females in parasitism and conspecific superparasitism was 0.67 ± 0.04 and 0.57 ± 0.09, respectively. Likewise, females laid more eggs in conspecific superparasitism than self‐superparasitism under our experimental conditions. These experiments demonstrate that E. vuilleti females can (i) discriminate between unparasitized and parasitized hosts and adapt the number of eggs they lay accordingly, and (ii) probably discriminate self from conspecific superparasitized hosts. Finally, mating does not appear to influence the host discrimination capacity, the ovarian function, or the oviposition behaviour.     

Reproductive strategies under multiparasitism in natural populations of the parasitoid wasp Nasonia (Hymenoptera)

Parasitoid Nasonia wasps adjust their progeny sex ratio to the presence of conspecifics to optimize their fitness. Another trait under female control is the induction of offspring diapause. We analysed progeny sex ratios and the proportion of diapausing offspring of individual Nasonia females in host patches parasitized by two species, Nasonia vitripennis and Nasonia giraulti, in North American field populations using microsatellite fingerprinting. Both Nasonia species produced similar sex ratios on hosts that were co‐parasitized by their own species as by the other species, indicating that females do not distinguish between con‐ and heterospecific clutches. The sex ratios of the diapause and adult fractions of mixed broods from single females were not correlated. We found further indications that N. vitripennis females take the emergence time of the offspring into account in their sex allocation. The reproductive strategies of Nasonia under multiparasitism are largely adaptive, but also partially constrained by information.     

Impact of superparasitism time intervals on progeny survival and fitness of an egg parasitoid

1.Superparasitism influences the fitness of female parasitoids and their progeny, and increasing time interval between oviposition bouts generally reduces survival probabilities of the second clutch. However, the timing of superparasitism may, under certain conditions, favour the second clutch. 2. This study investigated the effects of superparasitism time intervals on survival and fitness of both clutches, allowing the egg parasitoid Trichogramma euproctidis to parasitise previously parasitised Ephestia kuehniella host eggs at different time intervals. 3. In short intervals (0–1 h), a significant advantage was found for the second clutch over the first clutch (93.1% survival). In contrast, the second clutch was outcompeted by the first clutch in 17–19 h and 27–29 h intervals. Females deposited their eggs into larvae (intraspecific hyperparasitism) in a 39–41 h interval with a probability of survival of 57.1%. Females mostly refused to hyperparasitise pupae (～80% rejection at 124–126 h), and when they did, their progeny never survived. 4. Hyperparasitism significantly increased parasitoid mortality in both clutches from less than 20% (superparasitism only) to over 35%. 5. Except on newly laid eggs (0–1 h), superparasiting females were frequently observed attempting to stab immatures of all stages (from 36.4% to 89.4% of all ovipositions depending on treatment), but infanticide only appeared to succeed on larvae (39–41 h). 6. When the second clutch survived, emerging parasitoids were smaller than control individuals, probably due to resource depletion. 7. These results suggest that T. euproctidis females can detect that a host has been previously parasitised but they cannot perceive superparasitism time intervals.     

Egg load is a cue for offspring sex ratio adjustment in a fig‐pollinating wasp with male‐eggs‐first sex allocation

Fig‐pollinating wasps (Agaonidae) only reproduce within fig tree inflorescences (figs). Agaonid offspring sex ratios are usually female‐biased and often concur with local mate competition theory (LMC). LMC predicts less female‐bias when several foundresses reproduce in a fig due to reduced relatedness among intra‐sexually competing male offspring. Clutch size, the offspring produced by each foundress, is a strong predictor of agaonid sex ratios and correlates negatively with foundress number. However, clutch size variation can result from several processes including egg load (eggs within a foundress), competition among foundresses and oviposition site limitation, each of which can be used as a sex allocation cue. We introduced into individual Ficus racemosa figs single Ceratosolen fusciceps foundresses and allowed each to oviposit from zero to five hours thus variably reducing their eggs‐loads and then introduced each wasp individually into a second fig. Offspring sex ratio (proportion males) in second figs correlated negatively with clutch size, with males produced even in very small clutches. Ceratosolen fusciceps lay mainly male eggs first and then female eggs. Our results demonstrate that foundresses do not generally lay or attempt to lay a ‘fixed’ number of males, but do ‘reset to zero’ their sex allocation strategy on entering a second fig. With decreasing clutch size, gall failure increased, probably due to reduced pollen. We conclude that C. fusciceps foundresses can use their own egg loads as a cue to facultatively adjust their offspring sex ratios and that foundresses may also produce more ‘insurance’ males when they can predict increasing rates of offspring mortality.     

Oviposition decisions in an endoparasitoid under self-superparasitism conditions

Superparasitism is a widespread phenomenon. Having accepted superparasitism, mated female parasitoids must decide on the sex of each egg they subsequently lay into the same host. Theory predicts that this decision is either based on host quality, when more male eggs are laid in hosts that are already parasitized because they are perceived to be of poorer quality; or more eggs are laid of the sex that is most likely to be a strong larval competitor, i.e. generally females.Anastatus disparis is a facultative endoparasitic egg parasitoid. We used ‘artificial’ hosts to explore outcomes of decision making by A. disparis during superparasitism under a manipulated absence of larval competition. When only one egg was laid it was always female. As the number of eggs laid increased, so more of them were male. This supports the theory that oviposition decisions are based on host quality; more male eggs were laid in hosts that were already parasitized and thus of poorer quality.In a second experiment, eggs were exposed to parasitoids for different periods of time. Half the eggs were dissected to determine the number of parasitoid eggs that had been laid. The remaining eggs were incubated and the number and sex of offspring that ultimately emerged, following larval competition, were recorded. Under superparasitism conditions fierce larval competition ensued; only one offspring survived and they were predominantly female.In conclusion, oviposition decisions by female A. disparis accepting self-superparasitism were made based on host quality.     

Sex Allocation Decision Under Superparasitism by the Parasitoid Wasp Eupelmus vuilleti

Superparasitism is a widespread phenomenon in parasitoids and may be advantageous in some circumstances. In this study, offspring sex ratio was analysed in three superparasitism situations: when the second egg was laid by a random Eupelmus vuilleti (Hymenoptera: Eupelmidae) female from a group, when an isolated female was allowed to lay two eggs on the same host (self-superparasitism) or laid one egg on a host already parasitized by a conspecific (conspecific superparasitism). Females produced a different offspring sex ratio according to the different superparasitism situations tested. These sex ratios are in line with the local mate competition theory. The results further suggest that females can discriminate between hosts parasitized by a conspecific or by themselves and adapt the sex of the eggs they lay accordingly.     

Presence of a conspecific increases superparasitism but not infanticide under self‐ and conspecific superparasitism in a semisolitary parasitoid,Echthrodelphax fairchildii (Hymenoptera: Dryinidae)

Female parasitoids are expected to avoid superparasitism (ovipositing in and/or on parasitized hosts) when unparasitized hosts are available. However, when the supply of unparasitized hosts is restricted, they are expected to self‐ as well as conspecifically superparasitize. One of the cues of a reduced availability of unparasitized hosts is the presence of a conspecific. Moreover, if the focal species can perform infanticide, after encountering a conspecific female, the females are expected to kill eggs existing in and/or on hosts when superparasitizing, because the eggs are more likely to be laid by others. In this study we investigated whether females of an infanticidal semisolitary parasitoid, Echthrodelphax fairchildii, increase their frequencies of superparasitism and infanticide after encountering a conspecific female. Echthrodelphax fairchildii females are capable of discriminating between self‐ and conspecific superparasitism until up to 0.75 h after the first egg was laid (self‐superparasitism frequency < conspecific superparasitism frequency). As expected, the female parasitoids were more likely to perform self‐ and conspecific superparasitism after they had encountered a conspecific. In particular, the self‐superparasitism frequency increased highly within a short period after the first oviposition, so that no difference between the self‐ and conspecific superparasitism frequencies was found. In contrast, the infanticidal‐probing frequency remained extremely low, irrespective of whether or not the female parasitoids had encountered a conspecific. Moreover, when superparasitizing, females usually laid female eggs. Possible causes for the low frequency of infanticidal probing and the female‐biased sex ratio are discussed.     

Sex ratio regulation in the waspEupelmus vuilleti (crwf.), an ectoparasitoid on bean weevil larvae (Hymenoptera: Pteromalidae)

In Africa, the seeds and/or pods ofVigna unguiculata andVigna radiata (Papilionacea) are attacked in fields and storage structures by bruchid beetlesCallosobruchus maculatus andBruchidius atrolineatus, on which parasitoid communities can develop. One of these parasitoids is the solitary ectoparasitoidEupelmus vuilleti (Eupelmidae). The storage conditions ofV. unguiculata andV. radiata favor the overlapping of all host stages during several months. These conditions suggest that female parasitoids would vary the sex ratio of their offspring according to the different sizes or developmental stages of hosts. The sex ratio ofE. vuilleti was strongly related to the developmental stage of the hostC. maculatus. Under our experimental conditions, where superparasitism is rare, the proportion of daughters varied between 5 and 25% on the third larval stage but reached 70 to 90% on the pupae. The increase in the proportion of daughters was also observed in the absence of superparasitism. In this case, there was an absolute coincidence between the sex ratio of eggs laid and that of emerged adults. Manipulation of the sex of the egg by the females seems to take place at the time of the egg's fertilization. The relation between host weight and egg sex showed that the male eggs are preferentially laid on lighter host larvae and the female eggs on heavier ones.     

寄主大小及寄生顺序对蝇蛹佣小蜂寄生策略的影响

寄主大小模型认为寄生蜂后代性比与寄主大小相关,寄生蜂倾向于在大寄主上产出更多雌性后代,在小寄主上产出更多雄性后代.探讨了以家蝇蛹为寄主时,蝇蛹佣小蜂后代产量和性比变化;单次寄生情况下,寄主大小及寄生顺序对寄生蜂后代性比等影响.结果表明,蝇蛹佣小蜂的产卵期为(8.93±3.34)d,单头雌蜂能产雌性后代(34.11±16.34)头和雄性后代(11.04±8.87)头,且雄性百分比为0.24±0.11.随成蜂日龄的增大,寄生蜂产生雄性后代的比率显著增加.蝇蛹佣小蜂在寄生家蝇蛹时,会优先选择寄生个体较大的蛹;在单次寄生的情况下,蝇蛹佣小蜂倾向于在较大的家蝇蛹内产出更多的雌性后代.     

Brood sex ratios of the solitary parasitoid wasp, Coccophagus atratus

Abstract.

• 1 Female eggs of Coccophagus atratus are deposited within the haemolymph of coccoid scale insects. Male eggs are deposited on to late larval and prepupal stages of parasitoids of scale insects, including conspecifics.
• 2 When presented with either one host type or a combination of both host types, female C.atratus deposit all their available eggs, assigning the appropriate sex egg to each host encountered. Brood sizes are not adjusted for different combinations of hosts.
• 3 Behavioural observations show that females do not move away from patches of hosts until all their eggs are laid, regardless of the host type.
• 4 Brood sex ratios varied with changes in the relative availability of hosts for males and hosts for females. When both host-types were present in equal numbers, male biased sex ratios resulted (mean ±SEM =0.71 ± 0.009) and when 70% of hosts provided were suitable for female eggs, mostly female-biased sex ratios resulted (mean ± SEM = 0.37±0.01).
• 5 Our results do not fit predictions based on the assumption that a sex ratio of 0.5 should be expected in C.atratus. Observed sex ratios indicate that the unusual life histories of these parasitoids need to be taken into account in explanations of their sex ratios.

     

Discrimination of the age of conspecific eggs by an ovipositing ectoparasitic wasp

The recognition and avoidance of already parasitized hosts is a major issue in parasitoid behavioural ecology. A key factor affecting the fitness reward expected from superparasitism is the probability that the second or subsequent egg laid on a host will win the contest with the first-laid egg. The present study investigated the ability of females of the solitary ecto parasitoid Anisopteromalus calandrae Howard (Hymenoptera: Pteromalidae) to (i) discriminate between unparasitized Callosobruchus maculatus (Fabricius) (Coleoptera: Bruchidae) hosts and those parasitized by a conspecific, and (ii) discriminate between a host parasitized by an egg just laid (2 h) and one parasitized by an egg about to hatch (28 h). However, they did not adjust their offspring sex ratio on already parasitized hosts compared to unparasitized ones. Our results show that A. calandrae females can discriminate between parasitized and unparasitized hosts, as they lay more eggs on the latter. The probability of the second or subsequent egg laid on a host (superparasitism) winning the contest with a conspecific increases as the time between the two ovipositions decreases. Consequently, parasitoid females should lay more eggs on recently parasitized hosts than on those that have been parasitized for a long time (i.e., when the first eggs are about to hatch), and that is indeed what they were found to do. To increase their fitness in spite of the presence of already parasitized hosts, A. calandrae females have developed highly discriminative capacities regarding the parasitism status of hosts.     

Host discrimination modulates brood guarding behaviour and the adaptive superparasitism in the parasitoid wasp Trissolcus semistriatus (Hymenoptera: Scelionidae)

Because hosts utilized by parasitoids are vulnerable to further oviposition by conspecifics, host guarding benefits female wasps. The present study aims to test whether female adults regulate brood guarding behaviour by host discrimination in a solitary parasitoid Trissolcus semistriatus by presenting an intact or parasitized host egg mass to a female adult. Virgin females without oviposition experience have host discrimination ability, which enables them to adjust the number of eggs laid in the hosts. Mating experience increases superparasitism by female adults, whereas mated females achieve a higher discrimination ability as a result of oviposition experience and show a lower superparasitism rate. As expected, females exhibit brood guard after parasitizing an intact host egg mass, whereas those females visiting a previously parasitized host egg mass, do not. Because the survival of eggs in superparasitized hosts is relatively low, regulating brood guarding behaviour by host discrimination is adaptive for female wasps.     

When should a female avoid adding eggs to the clutch of another female? A simultaneous oviposition and sex allocation game

Summary Avoidance of double oviposition (ADO) is the strategy not to oviposit on food patches where another female has oviposited before. If two females oviposit on the same patch, competitive and mating interactions within and between broods may lead to both a clutch size game and a sex allocation game between the two visitors. Though the two games interact, they are usually considered separately. Here, the ESS conditions for ADO are investigated in an analysis that combines the two games into one. The analysis strengthens the notion that it is really ADO that needs to be explained, because role-dependent net pay-off from an additional egg is most likely to favour double oviposition (DO). To a first female, the net payoff includes the effect on the eggs already present, whereas to a second female only the egg's gross pay-off matters. ADO is the evolutionary stable strategy (ESS) if there are enough patches still without eggs and either (1) the fitness of an additional egg is so low that the first female would not lay it even in the absence of detrimental effects on earlier offspring, so neither would a second female, or (2) differences in either the survival probability of the offspring or their reproductive success are sufficient to counterbalance the differential interest in the eggs already present. The first condition requires that eggs are relatively large, because then the decrease in pay-off between two successive eggs can be large. The second condition may be met when there is a time interval between ovipositions of subsequent females. The resulting developmental lag of the second clutch will (1) diminish its ability to compete for food and (2) lower its reproductive success when there is local mate competition and sons are too late to mate with daughters of the first female. If sons of first and second females compete on equal terms, however, ADO is unlikely. Male migration between patches reduces the influence of sex allocation strategies on clutch size decisions; the same holds for small clutch sizes. To illustrate the importance of considering sex allocation and clutch size decisions in an integrated way, oviposition strategies of plant-inhabiting predatory mites (Acari: Phytoseiidae) are discussed.     

A sex allocation cost to polyandry in a parasitoid wasp

The costs and benefits of polyandry are central to understanding the near-ubiquity of female multiple mating. Here, we present evidence of a novel cost of polyandry: disrupted sex allocation. In Nasonia vitripennis, a species that is monandrous in the wild but engages in polyandry under laboratory culture conditions, sexual harassment during oviposition results in increased production of sons under conditions that favour female-biased sex ratios. In addition, females more likely to re-mate under harassment produce the least female-biased sex ratios, and these females are unable to mitigate this cost by increasing offspring production. Our results therefore argue that polyandry does not serve to mitigate the costs of harassment (convenience polyandry) in Nasonia. Furthermore, because males benefit from female-biased offspring sex ratios, harassment of ovipositing females also creates a novel cost of that harassment for males.     

Superparasitism in gregarious hymenopteran parasitoids: ecological, behavioural and physiological perspectives

Abstract.  Superparasitism in gregarious wasps occurs with the deposition of a clutch of eggs by a female into a host already parasitized by itself or a conspecific female. This review synthesizes and interprets the available results in the literature reported from field studies, and from behavioural and physiological investigations. To study superparasitism at the ecosystem level, methodological issues have to be solved to determine threshold values beyond which multiple offspring can be indisputably classified as originating from superparasitism. This life strategy is then discussed from the parasitoid's perspective, considering time and egg limitation, host discrimination, clutch size, offspring body size and sex ratio, as well as development time and survival rate of offspring, with special emphasis on physiological facilitation and constraints. Then, superparasitism in gregarious species is evaluated from the host's angle, addressing host survivorship and development, host food consumption and growth. Although superparasitism may be beneficial for either the first or the superparasitizing female, depending on the system, it is detrimental for both of them under conditions of extreme superparasitism. Recent methodological and experimental advances encourage further studies on the adaptive host choice under field and laboratory conditions, as well as on mechanisms underlying success of the first or the superparasitizing female and their progeny.     

Phytophagous insect oviposition shifts in response to probability of flower abortion owing to the presence of basal fruits

Phytophagous insects use a wide range of indicators or associated cues to avoid laying eggs in sites where offspring survival is low. For insects that lay eggs in flowers, these unsuitable sites may be created by the host plant's resource allocation to flowers. In the sequentially flowering host plant, Yucca glauca, late‐opening distal flowers are more likely to be aborted in the presence of already‐initiated basal fruits because they are strong resource sinks. If flowers are aborted, all eggs of the phytophagous insect, Tegeticula yuccasella, within the flower die. We used the phytophagous insect T. yuccasella that lays eggs in and pollinates host plant Y. glauca flowers to test the hypothesis that phytophagous insect females are less likely to invest eggs in host plant flowers if basal fruits are present because they are more likely to be aborted. We also investigated potential predictors of arrival of T. yuccasella at inflorescences at the onset of flowering. These factors may influence a phytophagous insect's decisions to select oviposition sites. We carried out a behavioral experiment using wild‐caught T. yuccasella females on manipulated inflorescences with distal flowers with basal fruits and without fruits. As potential predictors of T. yuccasella arriving at inflorescences, we used floral display size and day of onset of flowering. In support of our hypothesis, our experimental results showed that T. yuccasella was significantly less likely to oviposit in distal flowers on inflorescences with basal fruits. We also found that T. yuccasella arrival was higher at inflorescences with larger floral display size and earlier in the flowering season. These findings uncover a novel indicator of unsuitable oviposition sites—the presence of basal fruits, that phytophagous insects use to make oviposition decisions. Further, our study contributes to the growing body of evidence that shows that females prefer sites that increase the probability of survival of their offspring.     

Sequences of sex allocation and mortality in clutches of Metaphycus parasitoids of soft scale insects and the prevalence of all‐female broods

1. In many gregarious or quasi‐gregarious parasitoids that experience local mate competition, precise sex ratios with low variance are observed. Precise sex ratios can be achieved by laying male and female eggs in non‐random sequences. 2. Developmental mortality can also alter sex ratios of emerging offspring, and subsequently influence sex ratio optima. 3. The present study investigates sex allocation by Metaphycus flavus Howard, M. luteolus Timberlake, and M. angustifrons Compere (Hymenoptera: Encyrtidae), endoparasitoids of soft scale insects, in the laboratory. 4. All three Metaphycus species had precise secondary sex ratios when parasitising brown soft scale, Coccus hesperidum, L. in the laboratory. Moreover, we documented that all three species lay fertilised (= female) eggs first followed by unfertilised (= male) eggs at the end of the oviposition bout. However, there were significant differences in sex allocation sequences among species. 5. Mortality rates of eggs allocated within an oviposition bout also varied considerably, indicating that there is a significant interspecific variation in sequence position‐specific mortality. 6. Using a stochastic Monte Carlo simulation approach, we provide evidence that the incidence of all‐female broods in these parasitoid wasps appears mainly due to developmental mortality and not due to decisions by the ovipositing female. In two species the prevalence of all‐female broods was independent of clutch size, contrary to what is expected from theory. The influence of mortality on optimal sex allocation in these parasitoids is discussed.     

The effect of sperm storage and timing of mating on offspring sex ratios in the yellow dung fly Scatophaga stercoraria

1. Offspring sex ratios in the yellow dung fly Scatophaga stercoraria were examined in the laboratory. 2. Previous work indicated that females using previously stored sperm to fertilise their eggs produced male‐biased sex ratios. This result may have been due to female influences or the effects of sperm storage per se. 3. This pattern was not reproduced in the study presented here. Females that were allowed to mate just prior to oviposition produced similarly male‐biased sex ratios to those females that used previously stored sperm to fertilise their clutch. 4. Captive‐reared females may have perceived a lack of males in the population and thus produced a male‐biased offspring sex ratio. Alternatively, gamete ageing or extra‐chromosomal sex ratio distorters may have produced the male bias.     

Host-discrimination by <Emphasis Type="Italic">Phymastichus coffea</Emphasis>, a parasitoid of the coffee berry borer

Phymastichus coffea (LaSalle) (Hymenoptera: Eulophidae) is an African endoparasitoid of the coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae) that has been introduced to several countries to control this important pest. In the present study we performed a series of laboratory experiments in order to determine if there was evidence of host discrimination and superparasitism in P. coffea. Our choice experiments demonstrate that P. coffea females showed significant preference to attack unparasitized hosts, rather than those parasitized conspecifically. No significant preferences were detected in self-specific attacks between parasitized hosts and the healthy ones. A further dissection of hosts sequentially attacked either self or conspecifically, revealed that there were no more than two eggs per host. As P. coffea is a species that normally allocates two eggs per host in a single attack, we assumed that females were able to attack already parasitized hosts, but they did not lay eggs in them. Based on this fact, we conclude that there is a host discrimination ability in P. coffea females. With respect to the superparasitism by P. coffea using non-choice experiments, there was no significant difference between self-specific or conspecific attacks with respect to the control after one or two successive attacks. Conspecific attacks yielded the largest numbers of eggs after 3rd, 4th and 5th attacks and significant differences were found between this treatment and the control. The maximum number of eggs found in a single host was six individuals (conspecific treatment). These results confirmed that P. coffea usually laid two eggs per host; however, when there are no hosts available, conspecific attacks can result in the superparasitism in this species.     

Host size,superparasitism and sex ratio in mass-reared <Emphasis Type="Italic">Diachasmimorpha longicaudata</Emphasis>, a fruit fly parasitoid

We analyzed the relationship among host size, superparasitism and sex-ratio in mass reared Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Individual host pupae of Anastrepha ludens (Diptera: Tephritidae) were measured (length and width), and the number of oviposition scars per pupa was used as a reliable indicator of superparasitism. The probability of an emerging parasitoid being a female was positively associated with the number of oviposition scars on the host cuticle, but not with the host size. The number of scars per host pupae from which females emerged was slightly but significantly higher than in those pupae giving raise to males. In D. longicaudata, the influence of host size on sex allocation decisions of individual females seems to be overridden by the level of superparasitism, which itself was positively correlated with pupa length. This suggests that larger pupae could experience a higher number of ovipositions than their smaller counterparts, and that a high level of superparasitism may conduct to a female biased sex ratio. We discuss the relevance of these findings which could provide new elements (e.g., the manipulation of superparasitism) for optimizing the mass rearing of this parasitoid.