Measuring the discrepancy between fecundity and lifetime reproductive success in a pollinating fig wasp

Lifetime reproductive success in female insects is often egg‐ or time‐limited. For instance in pro‐ovigenic species, when oviposition sites are abundant, females may quickly become devoid of eggs. Conversely, in the absence of suitable oviposition sites, females may die before laying all of their eggs. In pollinating fig wasps (Hymenoptera: Agaonidae), each species has an obligate mutualism with its host fig tree species [Ficus spp. (Moraceae)]. These pro‐ovigenic wasps oviposit in individual ovaries within the inflorescences of monoecious Ficus (syconia, or ‘figs’), which contain many flowers. Each female flower can thus become a seed or be converted into a wasp gall. The mystery is that the wasps never oviposit in all fig ovaries, even when a fig contains enough wasp females with enough eggs to do so. The failure of all wasps to translate all of their eggs into offspring clearly contributes to mutualism persistence, but the underlying causal mechanisms are unclear. We found in an undescribed Brazilian Pegoscapus wasp population that the lifetime reproductive success of lone foundresses was relatively unaffected by constraints on oviposition. The number of offspring produced by lone foundresses experimentally introduced into receptive figs was generally lower than the numbers of eggs carried, despite the fact that the wasps were able to lay all or most of their eggs. Because we excluded any effects of intraspecific competitors and parasitic non‐pollinating wasps, our data suggest that some pollinators produce few offspring because some of their eggs or larvae are unviable or are victims of plant defences.     

Evolution of behavioural and cellular defences against parasitoid wasps in the Drosophila melanogaster subgroup

It may be intuitive to predict that host immune systems will evolve to counter a broad range of potential challenges through simultaneous investment in multiple defences. However, this would require diversion of resources from other traits, such as growth, survival and fecundity. Therefore, ecological immunology theory predicts that hosts will specialize in only a subset of possible defences. We tested this hypothesis through a comparative study of a cellular immune response and a putative behavioural defence used by eight fruit fly species against two parasitoid wasp species (one generalist and one specialist). Fly larvae can survive infection by melanotically encapsulating wasp eggs, and female flies can potentially reduce infection rates in their offspring by laying fewer eggs when wasps are present. The strengths of both defences varied significantly but were not negatively correlated across our chosen host species; thus, we found no evidence for a trade‐off between behavioural and cellular immunity. Instead, cellular defences were significantly weaker against the generalist wasp, whereas behavioural defences were similar in strength against both wasps and positively correlated between wasps. We investigated the adaptive significance of wasp‐induced oviposition reduction behaviour by testing whether wasp‐exposed parents produce offspring with stronger cellular defences, but we found no support for this hypothesis. We further investigated the sensory basis of this behaviour by testing mutants deficient in either vision or olfaction, both of which failed to reduce their oviposition rates in the presence of wasps, suggesting that both senses are necessary for detecting and responding to wasps.     

Why resource history matters: age and oviposition history affect oviposition behaviour in exploiters of a mutualism

1. Acceptance of hosts for oviposition is often hardwired in short‐lived insects, but can be dynamic at the individual level due to variation in physiological state determinants such as ageing and prior oviposition. However, the effect of the oviposition history of resources together with time taken to accept less preferred hosts in ageing insects has rarely been investigated. 2. The time taken by parasitic fig wasps to accept resources with different oviposition histories was recorded in order to investigate the effect of wasp physiological state and resource oviposition history on oviposition behaviour. These wasps, which differ in life‐history traits, oviposit at specific developmental stages of enclosed fig inflorescences called syconia. 3. Behavioural assays were performed with naive wasps and wasps aged with and without prior oviposition experience. Syconia at the same developmental stage but differing in oviposition history were offered in no‐choice assays and the time taken to first oviposition attempt was recorded. 4. One short‐lived pro‐ovigenic galler species exhibited a decline with age in time taken to accept a syconium for oviposition. The exact timing of the transition from non‐acceptance to acceptance of less preferred syconia was determined in terms of the proportion of elapsed life span at the transition; this occurred at 25% of elapsed life span. 5. Longer‐lived parasitoids did not show any decline in specificity despite being aged for 50% of their life span. Therefore, host quality, trophic position, egg load and age may individually affect oviposition decisions or have interaction effects.     

The function of host discrimination and superparasitization in parasitoids

Summary Host discrimination, i.e. the ability to distinguish unparasitized hosts from parasitized ones, and to reject the latter for egg laying is present in many parasitic wasp species. This property is classically considered as an example of contest competition, and is supposed to have a number of functions. However, different species do not react to each other's marks and lay eggs in hosts parasitized by the other species. Apparently the marks used for recognition are specific.Multiparasitization is the best strategy when hosts are scarce and the egg supplies of the parasitoids are not limited. Interspecific host discrimination is not an ESS.Superparasitization within one species would have selective advantage if the number of unparasitized hosts is small and the wasp has a reasonable chance to lay her egg in a host that is not parasitized by herself, and if the chance for her offspring to survive the competitive battle with the first parasitoid larva is not too small. This is shown to be the case.However, marks are not individual and wasps cannot distinguish hosts parasitized by themselves from those parasitized by others. The hypothesis is tested that the egg laying strategy (i.e. the decision to superparasitize) of wasps is dependent on the number of conspecifics that is searching simultaneously for hosts, since this determines the chance that a parasitized host encountered by a wasp is parasitized by herself.It is shown that host discrimination cannot be regarded as a case of contest competition. Other aspects of superparasitization, related to interference and population regulation, sex allocation and encapsulation are briefly discussed.     

To mark the host or the patch: Decisions of a parasitoid searching for concealed host larvae

We found evidence for patch marking in the parasitic wasp Halticoptera laevigata (Hymenoptera: Pteromalidae) foraging for concealed hosts. Wasps attack larvae of the fruit fly Myoleja lucida (Diptera: Tephritidae) in fruits of honeysuckle. A special feature of this host-parasitoid system is the limited food supply of a patch (i.e. a fruit of honeysuckle), which allows the successful development of only a single host fly larva. Females of the parasitoid H. laevigata were found to mark the host patch with a pheromone and to abandon the patch following oviposition into a single host larva. Field data revealed that eggs of the parasitoid were spread out evenly among infested patches, with several larvae of the host fly left unparasitized in those patches that contained more than one host. Since many parasitic insects mark the parasitized host after oviposition, we assumed host marking to be the ancestral character state and studied the patch-marking behaviour of H. laevigata as a derived character state as an alternative foraging strategy. We used stochastic dynamic modelling to investigate under what conditions mutant (patch) markers would be able to invade a population of normal (larval) markers. The models suggested that, under a variety of conditions, wasps marking the patch obtained higher fitness than wasps only marking the larva. Consequently, the results from our model predict the evolution of the patch-marking behaviour found in the empirical investigation. Finally, we discuss alternative pathways to the evolution of patch marking and point out under what circumstances the evolution of a patch-marking behaviour can generally be expected.     

Divvying up an incubator: How parasitic and mutualistic fig wasps use space within their nursery microcosm

Differential occupancy of space can lead to species coexistence. The fig–fig wasp pollination system hosts species-specific pollinating and parasitic wasps that develop within galls in a nursery comprising a closed inflorescence, the syconium. This microcosm affords excellent opportunities for investigating spatial partitioning since it harbours a closed community in which all wasp species are dependent on securing safe sites inside the syconium for their developing offspring while differing in life history, egg deposition strategies and oviposition times relative to nursery development. We determined ontogenetic changes in oviposition sites available to the seven-member fig wasp community of Ficus racemosa comprising pollinators, gallers and parasitoids. We used species distribution models (SDMs) for the first time at a microcosm scale to predict patterns of spatial occurrence of nursery occupants. SDMs gave high true-positive and low false-positive site occupancy rates for most occupants indicating species specificity in oviposition sites. The nursery microcosm itself changed with syconium development and sequential egg-laying by different wasp species. The number of sites occupied by offspring of the different wasp species was negatively related to the risk of syconium abortion by the plant host following oviposition. Since unpollinated syconia are usually aborted, parasitic wasps ovipositing into nurseries at the same time as the pollinator targeted many sites, suggesting response to lower risk of syconium abortion owing to reduced risk of pollination failure compared to those species ovipositing before pollination. Wasp life history and oviposition time relative to nursery development contributed to the co-existence of nursery occupants.     

How to evade a coevolving brood parasite: egg discrimination versus egg variability as host defences

Arms races between avian brood parasites and their hosts often result in parasitic mimicry of host eggs, to evade rejection. Once egg mimicry has evolved, host defences could escalate in two ways: (i) hosts could improve their level of egg discrimination; and (ii) negative frequency-dependent selection could generate increased variation in egg appearance (polymorphism) among individuals. Proficiency in one defence might reduce selection on the other, while a combination of the two should enable successful rejection of parasitic eggs. We compared three highly variable host species of the Afrotropical cuckoo finch Anomalospiza imberbis, using egg rejection experiments and modelling of avian colour and pattern vision. We show that each differed in their level of polymorphism, in the visual cues they used to reject foreign eggs, and in their degree of discrimination. The most polymorphic host had the crudest discrimination, whereas the least polymorphic was most discriminating. The third species, not currently parasitized, was intermediate for both defences. A model simulating parasitic laying and host rejection behaviour based on the field experiments showed that the two host strategies result in approximately the same fitness advantage to hosts. Thus, neither strategy is superior, but rather they reflect alternative potential evolutionary trajectories.     

Could the egg itself be the source of the oviposition deterrent marker in the ectoparasitoid Dinarmus basalis?

Females of Dinarmus basalis, a solitary ectoparasitoid, strongly avoid superparasitising hosts bearing eggs which are 20 or more hours old. Our objective was to determine the mechanism by which the factors inducing host discrimination and such an oviposition deterring effect act, and the origin of the deterrent. This study showed that the information is carried by the parasitised host. It is acquired by a transfer of molecules from the wasp egg onto the host and it requires contact between egg and host for at least 4 h. The factors transferred do not, as commonly reported in other species, come from the female's genital apparatus but from the live egg itself. Consequently, the D. basalis egg directly participates in the success of parasitism by releasing factors which elicit the oviposition host deterring effect. The originality and the ecological importance of these results are discussed.     

寄生蜂寄主选择行为研究进展

寄生蜂是膜翅目昆虫中的重要类群,在自然界种类多,数量大。据文献报道全世界膜翅目昆虫大约有10万种”’,其中许多种类与农林害虫长期保持一定的制约关系,在害虫防治中占有重要地位。由于大量使用化学农药导致害虫的抗药性增加,利用天敌昆虫来防治害虫越来越显示出其重要性和优越性。但是,直到近20年来,寄生蜂的寄生行为才受到重视,并给予了广泛的、深入的研究”－‘’严格地讲,寄生蜂应该称为拟寄生蜂,它与通常所说的寄生昆虫像虱子、臭虫等有明显不同,主要区别在于：1．寄生仅仅发生在未成熟阶段,而成虫阶段营自由生活;2．寄…     

Delayed inhibition of host development by the nonparalyzing venoms of parasitic wasps

The nonparalyzing venoms of two unrelated parasitic wasps, Eulophus larvarum and Clinocentrus gracilipes, in separate ways cause delayed yet well-defined arrests in their hosts' development, apparently by disrupting events normally under endocrine control. The venom of E. larvarum (for which species host acceptance and oviposition behavior is described) prevents apolysis in its host after a depressed feeding period. The venom employed by C. gracilipes switches the host to a pharate pupal stage irrespective of its larval instar.     

The avoidance of superparasitism in four species of parasitic wasp—Mathematical models and experimental results

Experimental results, and interpretation, are presented which relate to oviposition behaviour in four species of parasitic wasp (Hymenoptera: Chalcidoidea). All lay their eggs in pupae of the common house fly (Musca domestica) and of other flies associated with man. Probability models suggested byD. J. Daley for describing the avoidance of superparasitism are used to analyse the data. Certain of the models considered by previous authors appear as specieal cases. A satisfactory fit was obtained either by assuming a fixed probability of oviposition in an already parasitised pupa, or by using a model motivated by supposing that a female will tolerate without oviposition some fixed number of visits to already parasitised pupae. A third model was considered which makes the probability depend on the number of previous ovipositions in the pupae now visited. In all four species the presence of other females (with parasite: host ratio unchanged) increased the probability of oviposition upon encountering an already parasitised pupa. In the presence of other females Spalangia endius laid an increased number of eggs, whereas the other three species laid fewer eggs.     

Host discrimination of a larval parasitoid: the quick movement of Microplitis demolitor

Many parasitoids discriminate previously parasitised hosts from unparasitised ones to avoid mortality of offspring. Parasitoids that parasitise aggressive hosts such as lepidopteran larvae are known to attack hosts very quickly to avoid being attacked. However, little is known about host discrimination of such quick attacking parasitoids. We investigated host discrimination of Microplitis demolitor (Wilkinson) (Hymenoptera: Braconidae) a quick attacking parasitoid of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Results showed that ratios of female wasps that rejected the hosts after antennal examination did not differ between parasitised and unparasitised hosts, indicating that M. demolitor did not discriminate hosts by antennal examination. However, 95% of females that inserted ovipositor into unparasitised hosts actually laid eggs, whereas it was only 31% for parasitised hosts, indicating that females discriminated hosts by oviposition insertion. Analyzing video recordings revealed that the ovipositor exploration of the host took 0.3 s. Female wasps that had experienced high-host density of unparasitised hosts readily rejected parasitised hosts, while wasps with experience of low host availability of parasitised hosts tended to accept parasitised hosts. This suggests that host discrimination behaviour of M. demolitor is affected by previous experience of different host availability and host quality.

     

拟寄生蜂搜索产卵过程中对寄主的竞争

综述拟寄生蜂搜索产卵过程中对寄主竞争的最新研究进展.这类竞争具有四种方式,即标记寄主、杀卵和杀幼、守护寄主和捕食寄主.（1）标记寄主常涉及寄主标记信息素,这是由雌蜂在产卵前、产卵时或产卵后分泌的化学物质.寄主标记信息素常介导拟寄生蜂对已寄生和健康寄主的辨别、减少过寄生和多寄生、减轻种内和种间竞争压力.（2）雌蜂遇到已寄生寄主时,很多种类杀死前一雌蜂遗留的卵和幼虫,再产下自己的卵.雌蜂使用三种方法杀卵和杀幼,即产卵器穿刺、取食和使用有毒物质.通过杀卵和杀幼,产卵雌蜂清除了前一雌蜂遗留的后代,主动改善了寄主品质,从而有利于自身后代的生存.（3）守护寄主在肿腿蜂科、缘腹细蜂科、金小蜂科、缨小蜂科和茧蜂科中均有报道,守护者驱逐入侵者以保护后代及健康寄主.（4）捕食寄主不仅减少了健康寄主数量,且直接导致已寄生寄主中拟寄生蜂卵和幼虫的死亡.雌蜂一般在体内成熟卵量较少时捕食寄主.讨论了研究拟寄生蜂搜索产卵过程中竞争寄主的理论意义和实际应用价值.     

Parasitic mites as part-time bodyguards of a host wasp

Some bees and wasps that host mites have peculiar pocket-like structures called acarinaria. These have long been considered as morphological adaptations to securely transfer beneficial mites into nests, and thus are thought to be the product of a mutualistic relationship. However, there has been little compelling evidence to support this hypothesis. We demonstrated that the parasitic mite Ensliniella parasitica, which uses acarinaria, increases the reproductive success of its host wasp Allodynerus delphinalis by protecting it from parasitoid wasps. Every time the parasitoid Melittobia acasta accessed a prepupal or pupal wasp host cell, adult mites attacked it, continuously clinging to it and possibly piercing the intersegmental membrane of the parasitoid with their chelicerae. Subsequent mortality of the parasitoid depended on the number of attacking mites: an average of six mites led to a 70% chance of mortality, and 10 mites led to a 100% chance of mortality. In this way, parent mites protect the food source (juvenile wasps) for themselves and ultimately for their offspring. We propose that wasps evolved acarinaria to maintain this protective guarding behaviour.     

Host concealment: a determinant for host acceptance and feeding in an ectoparasitoid wasp

In general, ectoparasitoids attack concealed hosts in protected situations whereas endoparasitoids use both concealed and exposed hosts. The difference is assumed to be the consequence of ecological constraints; ectoparasitic larvae are vulnerable both to predation and to climatic factors such as rainfall, and, hence, require some structures to protect themselves. I hypothesized that such ecological constraints should act as a within-species selection pressure to female ectoparasitoids, and hence that females should recognize the degree of concealment of the host and prefer concealed over exposed hosts for oviposition. To test this hypothesis, I examined 1) whether host concealment could influence host acceptance by the ectoparasitoid wasp Agrothereutes lanceolatus and 2) whether host concealment could influence the fitness of the offspring. Female wasps recognized and attacked (probed) both cocooned and exposed host prepupae in equal proportions, but discriminated between them after ovipositor insertion, and preferred the former for oviposition and the latter for host-feeding. They also selected to oviposit on hosts concealed in paper tubes. Thus host concealment was important for host selection in A. lanceolatus . Offspring fitness (measured as survival and size) was much lower on exposed hosts than on cocooned and paper-concealed hosts, even under laboratory conditions. Thus, host concealment influenced the fitness of wasp offspring, and, hence, is a good indicator of host quality for female wasps. Adaptiveness of host selection and host-feeding in A. lanceolatus in relation to host concealment is discussed.     

Host selection by virgin and inseminated females of the parasitic wasp, Dinarmus basalis (Pteromalidae, Hymenoptera)

1. Fitness is related to reproduction and survival. There apparently exists a negative correlation between the numbers of male and female offspring. There also exists a trade-off between survival and reproduction. This paper investigates optimal decisions with the reproduction and survival trade-off in host selection by wasps.
2. Whereas inseminated female wasps could manipulate the sex of their offspring, virgin females produced only male offspring. I surveyed behavioural differences and the consequences of oviposition by inseminated and virgin females of a solitary parasitic wasp in host choice situations.
3. Two host types were available at the same time to both inseminated and virgin female wasps: one (a 17-day-old host in one bean) presenting difficulties for the laying of eggs, but more benefits for the offspring and the other (five 12- or 13-day-old hosts in one bean) easier for the female wasp for laying of eggs but less beneficial for the offspring.
4. Inseminated female wasps chose more 17-day-old hosts than 12-day-old hosts, but more 13-day-old hosts than 17-day-old hosts in each pair-wise choice. Virgin females chose the smaller hosts in both situations.
5. Virgin females, having greater longevity than inseminated females, laid larger numbers of eggs than the inseminated females during their lifetime by adopting an energy-saving host choice that had little effect on male offspring fitness.     

Plasticity in life features,parasitism and super-parasitism behavior of Bracon hebetor,an important natural enemy of Galleria mellonella and other lepidopteran host species

The wasp, Bracon hebetor Say, is an important potential biocontrol agent of a wide range of lepidopteran insect species. The current study was subjected to compare these ectoparasitoid fitness traits on different host species belonging to the order Lepidoptera. Moreover, we determine the population dynamic with different host densities, sex ratio patterns, super-parasitism, longevity, paralysis success, and reproductive potential under laboratory conditions. Our results revealed that oviposition increased with an increase in host density, while the adult emergence and egg hatching were decreased due to the super-parasitism on host larvae. A higher male and female-biased population were observed when virgin and mated females offered fresh hosts. Adults' longevity was recorded more in females than males when kept only with bee honey + royal jelly + host larvae. The mean duration of egg-adult development was recorded higher on Galleria mellonella and lowest on Busseola fusca. The parasitization rate, super-parasitism, and cumulative fecundity of mated and virgin female wasps with different host species were observed higher on specific host Galleria mellonella while it was lower on Phthorimaea operculella. Furthermore, the parasitoids having mating experience preferred fresh, while the parasitoids' lack of mating experiences preferred paralyzed host under olfactometer test. Besides, this research has produced novel facts on the biology of parasitic wasp, B. hebetor that may guide the advancement of sustainable biological control programs to control lepidopteran pests.     

Effect of wasp size, physiological state, and prior host experience on host-searching behavior in a parasitoid wasp (Hymenoptera: Ichneumonidae)

Host-searching behavior in insects generally varies among individuals. A number of physiological and environmental factors can be involved in such individual variation. Here, a series of behavioral observations were made to highlight the importance of physiological state (i.e., number of mature eggs a female carries, amount of nutrient reserves, etc.) and learning state (i.e., prior host experience) on host-approaching behavior of parasitoids. Itoplectis naranyae (Hymenoptera: Ichneumonidae), a solitary endoparasitoid wasp attacking lepidopteran pupae and prepupae, was used as a test insect. The results show that female wasps with experience ovipositing on hosts 2 days before the test found hosts more quickly than did naïve wasps. Prior experience of host odor itself did not affect host-finding behavior, however. A single oviposition was enough for wasps to shorten time to find a host; additional experience had no significant effect on the efficiency of searching. The number of mature eggs a female carried had no effect on the time required to find a host regardless of prior host experience. The size of wasps, instead, was a significant factor when wasps had no prior host experience, and larger wasps found hosts more rapidly than did smaller wasps. Searching activity was not affected by how many hosts a female wasp had fed on before testing.     

Increased host acceptance in experienced females of the parasitoid Brachymeria intermedia: which types of oviposition behaviour contribute to experience?

Brachymeria intermedia (Nees) (Hymenoptera: Chalcididae) is a solitary endoparasitoid of the gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae). The probability that a wasp will parasitise this host is increased if she had a previous oviposition experience. We investigated which types of pre-oviposition and oviposition behaviour induced this change by comparing the acceptance behaviour of wasps with zero to five oviposition experiences as well as wasps with various partial host handling experiences (from no contact with a host to one complete oviposition sequence). The percentage of females accepting the host increased gradually with both the number of previous oviposition experiences and the amount of handling of a single host. Furthermore, the naive females were less likely (44%) to walk to the host than females with a variety of experiences (72–100%). A single antennal contact with the host was sufficient to increase the probability of walking to the host. Additional handling and additional oviposition experiences further elevated the propensity to oviposit. Thus, the modification of the acceptance behaviour through experience was essentially a gradual process in which antennal contact with a pupa was a major element. It is suggested that naive wasps learned the host odour when they first antennated a pupa. As a result, they were attracted to the host odour in subsequent encounters.