Partial local mate competition in the wasp Trichogramma euproctidis: the role of emergence sex ratio on female mating behaviour

1. Parasitic wasps with structured populations are generally assumed to follow the local mate competition (LMC) model: females lay only the minimal number of sons necessary to inseminate all daughters in the emergence patch, and increase this number when faced with additional broods from unrelated females. After emergence, daughters mate with local males before dispersing for host location and oviposition. The main predictions from the model have been verified for many species. 2. Conflicting evidence exists on the status of the egg parasitoids Trichogramma regarding their on‐patch versus off‐patch mating. Although the life‐history traits of several species indicate that mating must occur on the emergence patch, recent data suggest that mating could occur outside the natal patch. 3. In this study, we measured the level of off‐patch mating in the egg parasitoid Trichogramma euproctidis using two isofemale lines in a greenhouse experiment. The impact of the sex ratio on the level of off‐patch mating was also tested. 4. The overall off‐patch mating proportion was 40.5% with a range between 0 and 85.7%, and was influenced by the sex ratio on the emergence patch: the more males available at emergence, the less off‐patch mating occurring. 5. The mating structure of this species can be described as partial LMC.     

The influence of developmental mortality on optimal sex allocation under local mate competition

In panmictic populations, optimal sex allocation is, under theassumptions of Fisher's model, not influenced by the probabilityof offspring developmental mortality, or by differences in mortalitybetween the sexes. In contrast, when mating opportunities areconfined to siblings, developmental mortality can influenceoptimal sex allocation. Many animal species have both localmating and developmental mortality. We show that when developmentalmortality is random for individual offspring, optimal sex allocationis influenced by mortality among males but not among females.Male mortality increases the allocation to males, but this shouldnever be male biased, even under extreme male mortality. Thisresult applies both when mothers are able to control the sexof individual offspring precisely, and when sex is allocatedwith binomial probability. The influence of mortality becomesprogressively larger when the variance of the distribution ofmortality over clutches diminishes. The reduction in fitnessis greater than the proportion of mortality, especially at smallclutch sizes, and mortality reduces the advantage of producingprecise sex ratios, and of local mate competition in general.     

Insemination potential of male Trichogramma evanescens

Reproduction strategies of male parasitoids have received less attention than those of the females. In hymenopteran parasitoids that reproduce by arrhenotokous parthenogenesis, virgin females are able to reproduce, but they are constrained to produce only males. In such species, the number of sperm transferred to females is of prime importance for female reproductive success. In this study, we measured the insemination potential of male Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). Independent of their age and their sperm‐depletion status, males continued to mate with females until the end of their life. They quickly depleted their sperm supply by fertilizing 18 females during their lifetime, among which 80% were inseminated during the first 24 h. They fathered around 400 daughters over their lifetime. Our results suggest an absence of imaginal spermatogenesis in T. evanescens males that can be designated as prospermatogenic. Sperm is thus a limited resource in this species and females might encounter males with varying amounts of sperm.     

Sources of stochasticity in models of sex allocation in spatially structured populations

There are many ways to include stochastic effects in models of sex allocation evolution. These include variability in the number of mating partners and fecundity in a rich literature that goes back 20 years. The effects of variance in the fecundity and number of mating partners have typically been considered separately from the stochastic effects of mortality. However, I show that these processes produce mathematically equivalent models with subtly different biological details. These scenarios differ in the way that information becomes available to individuals because the parents often have information on mating partners while they are making sex allocation decisions, but must make these decisions before brood mortality takes place. This makes it possible to test which mechanism, stochastic mortality or variation in mating partners, is responsible for observed sex ratios. Alternatively, asymmetric variance between sexual functions can cause skewed sex allocation, even in the absence of local mate competition. This allows the evolution of either female- or male-biased sex ratios depending on which sexual function is more variable.     

Influence of postzygotic reproductive isolation on the interspecific transmission of the paternal sex ratio chromosome in Trichogramma

The paternal sex ratio (PSR) chromosome is a supernumerary chromosome that causes the destruction of the paternal chromosome set in the first mitosis in a fertilized egg. It is known from parasitoid wasps in the genera Nasonia and Trichogramma (Hymenoptera). In these haplodiploids, the egg fertilized by sperm carrying PSR matures as a haploid male that again carries, and is capable of transmitting, the PSR chromosome. Because of its unique transmission behavior, the PSR chromosome may be easily transmitted between species. This study tests whether the interspecific transmission of PSR between Trichogramma kaykai Pinto and Stouthamer and Trichogramma deion Pinto and Oatman (Hymenoptera: Trichogrammatidae) is affected by two types of postzygotic reproductive isolation, i.e., hybrid inviability and hybrid sterility. The results show that PSR can rescue fertilized eggs that would normally be inviable in the interspecific cross and the rescued eggs develop into male offspring that carry PSR. The results suggest that the two types of postzygotic reproductive isolation have no effect on the transmission of PSR between the two Trichogramma species.     

Sperm competition and sex allocation in simultaneous hermaphrodites

Summary Sex allocation theory is developed for hermaphrodites having frequent copulations and long-term sperm storage. Provided the sperm displacement mechanisms are similar to those known in insects, the ESS allocation to sperm versus eggs satisfies a rather simple rule. There are no data to test this rule, as yet.     

Social situation,sperm competition and sex allocation in a simultaneous hermaphrodite parasite,the cestode Schistocephalus solidus

Evolutionary theory predicts an influence of mating group size on sex allocation in simultaneous hermaphrodites. We experimentally manipulated the social situation during reproduction in a simultaneous hermaphrodite parasite, the tapeworm Schistocephalus solidus, by placing worms as singles, pairs or triplets into an in vitro system that replaces the final host. We then determined the reproductive allocation patterns after 24 h (i.e. before the start of egg release) and after 72 h (i.e. around the peak of egg release rate) using stereology. After 24 h, sex allocation strongly depended on worm volume (which is determined in the second intermediate host), but was not significantly affected by the social situation experienced during reproduction. After 72 h, worms in groups had less vesicular sperm (i.e. sperm to be used in future inseminations) than singles. They also stored significantly more received sperm in their seminal receptacles than singles, suggesting that more sperm had been transferred in groups. Moreover, worms in triplets stored significantly more received sperm than worms in pairs, suggesting that they either mated more often and/or transferred more sperm per mating. This suggests a behavioural response to the increased risk of sperm competition in triplets. We further discuss the relative importance of sex allocation decisions at different life‐history stages.     

Sex allocation by a mite parasitic on insects: local mate competition,host quality and operational sex ratio

The aim of this study was to test the predictions of local mate competition (LMC), host quality (HQ) and operational sex ratio (OSR) models, using a non-arrhenotokous parasitic mite, Hemisarcoptes coccophagus (Astigmata: Hemisarcoptidae). The life-history pattern of this mite meets the assumptions of these sex allocation models. Mating group size (LMC model), HQ and OSR affected the sex allocation of H. coccophagus females. Only young mite females adjusted the sex ratio of their progenies according to the predictions of LMC and HQ models; the sex allocation of old females was contrary to these predictions. We explain these patterns by the dynamic nature of the mite's population structure. When parents are young, their population distribution is patchy and progeny matings are local; hence sex allocation is in accordance with LMC theory. When parents become older, their populations shift towards panmixis; factors which had operated previously no longer exist. Consequently, females adjust the sex ratio of late progenies so that it can compensate for the earlier sex allocation, in order to make their total sex ratio unbiased, as expected in panmictic populations. Our data, expressed as the cumulative sex ratio, support this hypothesis.     

The influence of previous host age on current host acceptance in Trichogramma

Trichogramma principium Sug. & Sor. females were sequentially offered two portions of the grain moth (Sitotroga cerealella Oliv.) eggs, either young (1-day old) or old (eggs that had developed 6 days at a temperature of 20 °C). The probability of host acceptance depended not only on current host age, but also on the age of the previously offered host. Particularly, Trichogramma females more often oviposited in old host eggs when previously offered young eggs (35–45% of Trichogramma females laid eggs) compared to females which were sequentially offered two portions of old eggs (15–20% of Trichogramma females laid eggs). In other words, parasitization by Trichogramma was stable even when transferred from young (preferred) to old (usually rejected) eggs. Dissections showed that refusing females had significantly more mature eggs than ovipositing females, independent of host age. Among ovipositing females, wasps provided with young hosts had fewer mature ovarial eggs than wasps provided with old hosts. Supposedly, Trichogramma females offered old hosts require a higher motivation to oviposit and have a correspondingly higher egg load than females offered young (preferred) hosts.     

Patch exploitation by non‐aggressive parasitoids under intra‐ and interspecific competition

The behavioral strategies evolved by insect parasitoids to optimize their foraging efforts have been the subject of many theoretical and empirical studies. However, the effects competition may have on these strategies, especially for species that do not engage in antagonistic behaviors, have received little attention. The objective of this study was to evaluate the effects of intraspecific and interspecific competition on patch exploitation strategies by two non‐aggressive species, Trichogramma pintoi Voegelé and Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae), both generalist egg parasitoids. We analyzed the patch residence times of females, their patch‐leaving mechanisms, and the sex allocation of their progeny while foraging either alone, with an intraspecific competitor, or with an interspecific competitor. To some extent, each species responded differently to the presence of a competitor in the patch. Trichogramma pintoi females did not change their patch‐leaving mechanisms in response to competition and behaved as if under an exploitative competition regime, whereas T. minutum females did change their patch‐leaving mechanisms in response to competition and remained longer in the host patch than expected. Antennal rejection, and not oviposition, was the proximate behavioral mechanism underlying patch‐leaving decisions by both species. Neither species adjusted the sex allocation of their progeny in response to competition. These results indicate that the effects of competition differ even among closely related parasitoid species.     

Density-dependent dispersal promotes female-biased sex allocation in viscous populations

A surprising result emerging from the theory of sex allocation is that the optimal sex ratio is predicted to be completely independent of the rate of dispersal. This striking invariance result has stimulated a huge amount of theoretical and empirical attention in the social evolution literature. However, this sex-allocation invariant has been derived under the assumption that an individual''s dispersal behaviour is not modulated by population density. Here, we investigate how density-dependent dispersal shapes patterns of sex allocation in a viscous-population setting. Specifically, we find that if individuals are able to adjust their dispersal behaviour according to local population density, then they are favoured to do so, and this drives the evolution of female-biased sex allocation. This result obtains because, whereas under density-independent dispersal, population viscosity is associated not only with higher relatedness—which promotes female bias—but also with higher kin competition—which inhibits female bias—under density-dependent dispersal, the kin-competition consequences of a female-biased sex ratio are entirely abolished. We derive analytical results for the full range of group sizes and costs of dispersal, under haploid, diploid and haplodiploid modes of inheritance. These results show that population viscosity promotes female-biased sex ratios in the context of density-dependent dispersal.     

Size‐dependent sex allocation in a simultaneous hermaphrodite parasite

Most models of sex allocation distinguish between sequential and simultaneous hermaphrodites, although an intermediate sexual pattern, size‐dependent sex allocation, is widespread in plants. Here we investigated sex allocation in a simultaneous hermaphrodite animal, the tapeworm Schistocephalus solidus, in which adult size is highly variable. Sex allocation was determined using stereological techniques, which allow measuring somatic and reproductive tissues in a common currency, namely volume. We investigated the relationships between individual volume and allocation to different reproductive tissues using an allometric model. One measure of female allocation, yolk gland volume, increased more than proportionally with individual volume. This is in contrast to the measure of male allocation, testis volume, which showed a strong tendency to increase less than proportionally with individual volume. Together these patterns led to sex allocation being strongly related to individual volume, with large individuals being more biased towards female allocation. We discuss these findings in the light of current ideas about size‐dependent sex allocation in, primarily, plants and try to extend them to simultaneous hermaphrodite animals.     

Selectivity evaluation of insecticides used to control tomato pests to Trichogramma pretiosum

The effects of the insecticides abamectin, acetamiprid, cartap and chlorpyrifos on larvae, pupae (within the host egg) and adults of the egg parasitoid Trichogramma pretiosum Riley (Hym.: Trichogrammatidae) were evaluated under laboratory conditions, using three standard tests described by IOBC. When sprayed on the immature stages of this parasitoid, cartap and chlorpyrifos proved to be the most harmful insecticides, affecting both the emergence success and parasitism capacity of this parasitoid, whereas abamectin and acetamiprid were selective. Abamectin was harmful to adults (residue test on glass plates), slightly harmful to larvae, and moderately harmful to pupae (sprayed on the immature stages within host eggs Anagasta kuehniella (Zeller)); acetamiprid was moderately harmful to adults, harmless to larvae, and slightly harmful to pupae; cartap was harmful to adults, moderately harmful to larvae and harmful to pupae; chlorpyrifos to adults, harmless to larvae and harmful to pupae.     

Reduced competitive ability due to Wolbachia infection in the parasitoid wasp Trichogramma kaykai

Several hymenopteran parasitoids are infected with parthenogenesis‐inducing (PI) Wolbachia. Infected wasps produce daughters instead of sons from unfertilized eggs. Thus far, little is known about the direct effects of PI Wolbachia on their host's fitness. Here, we report reduced competitive ability due to Wolbachia infection in a minute parasitoid wasp, Trichogramma kaykai Pinto and Stouthamer (Hymenoptera: Trichogrammatidae). Immature survival of infected individuals in a host parasitized by a single infected female, laying a normal clutch of eggs, was lower than those parasitized by a single uninfected individual. When the offspring of infected and uninfected females shared the same host, the infected immatures had significantly lower survival rates than their uninfected counterparts. The survival rate of infected immatures was higher when they competed with other infected immatures from a different infected parent than in competition with uninfected immatures of conspecific wasps. Thus, the host Trichogramma can suffer a substantial reduction in fitness when it is infected with the PI Wolbachia. We discuss why such a reduction is to be expected when populations of infected and uninfected individuals co‐occur, and how the reduced competitive ability of PI Wolbachia influences the spread of the bacteria in the field.     

Combined effects of host quality and local mate competition on sex allocation inLariophagus distinguendus

Summary Many parasitoid wasps are known to adjust sex ratio in response to either local mate competition (LMC) or host quality. Nevertheless, few studies have investigated the combined effects of these two factors on sex allocation. The sex allocation pattern inLariophagus distinguendus, a parasitoid of granary weevil larvae, is contrasted to the expectations of Werren's (1984) model combining LMC and host quality. Several predictions of the model are confirmed, but others are not. Sex ratio on both large and small hosts declines with proportion of small hosts attacked in a manner consistent with the model. However, when only one host size is parasitized, sex ratio is not independent of that host size, as predicted by the model. Various possibilities for the deviation between expected and observed are discussed. A partial LMC/host quality model is developed which allows for some matings outside the natal patch, and predictions of this model conform more closely to the pattern observed inL. distinguendus. Finally, the application of parasitoid studies to basic questions in evolutionary ecology is briefly discussed.     

Female-biased sex ratios under local mate competition: An experimental confirmation

Summary Experimental work of Nadel and Luck (1992) on a chalcidoid wasp provides a confirmation of sex ratio theory under local mate competition.     

Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

Local mate competition with lethal male combat: effects of competitive asymmetry and information availability on a sex ratio game

We constructed a sex allocation model for local mate competition considering the asymmetry of competitive abilities among sons. This model assumes two females of a parasitoid wasp oviposit on the same host in sequential order. The evolutionarily stable strategy will be in either Stackelberg or Nash equilibrium, depending on whether the females can recognize their opponent's sex ratio or not, respectively. The Nash equilibrium predicts the second female produce more males than the first. If the second female is able to know and respond to the strategy of the first (a Stackelberg equilibrium), the first will decide an optimal sex ratio assuming that the second reply to it. Under such an assumption, our model predicts that not producing sons is adaptive for the second female when the sons she produces have low competitive ability. Males of parasitoid wasps Melittobia spp. are engaged in lethal male-male combat, indicating large asymmetry in mating success among sons. If females have the ability to recognize their opponent's sex ratio, our model suggests that the severe lethal male-male combat may be one factor explaining their extremely female-biased sex ratio that is unexplainable by pre-existent models.     

稻螟赤眼蜂与二种赤眼蜂对水稻二化螟卵寄生竞争作用

稻螟赤眼蜂是我国水稻二化螟的优势卵寄生蜂,本文在室内条件下,初步研究了稻螟赤眼蜂分别与松毛虫赤眼蜂和螟黄赤眼蜂在水稻二化螟卵上的种间竞争作用。结果表明,同时接入稻螟赤眼蜂和松毛虫赤眼蜂时,寄生水稻二化螟卵(40.2粒)及子代雌蜂总数(32.0头)最多,且松毛虫赤眼蜂平均寄生二化螟卵的数量(26.5粒)明显高于单独接蜂的平均寄生的数量,后代雌蜂比率(76.3%)明显低于单独接蜂时的雌蜂比率,发育历期(10.7 d)明显长于接入同种时的发育历期。而稻螟赤眼蜂和螟黄赤眼蜂共存时,螟黄赤眼蜂平均寄生二化螟卵的数量(10.3粒)、后代雌蜂比率(75.3%)以及发育历期(8.0 d)与单独接蜂时相似;同样,当稻螟赤眼蜂与松毛虫赤眼蜂混合接蜂时,稻螟赤眼蜂平均寄生二化螟卵的数量(14.4粒)、后代雌蜂比率(79.0%)以及发育历期(8.6 d)与单独接蜂时相似,但是,当稻螟赤眼蜂与螟黄赤眼蜂混合接蜂时,其后代雌蜂比率(76.7%)明显低于单独接蜂处理,而发育历期(8.8 d)明显长于单独接蜂处理。总的来看,在二化螟卵上,同时接入二种赤眼蜂时,蜂种间存在一定的竞争作用,其中混合接入稻螟赤眼蜂和松毛虫赤眼蜂时,对水稻二化螟的控制效果最佳。