Spatial and temporal variation in host–parasitoid interactions: leafcutter ant hosts and their phorid parasitoids

1. Parasitoid–host interactions are important components of ecological communities. Although parasitoid–host interactions are strongly shaped by evolutionary history, the abundance of both the parasitoid and the host may have a role in determining the nature of the interaction once phylogenetic relationships are considered. 2. Leafcutter ants are hosts of phorid parasitoids and represent a well‐defined and specialised module within a larger network of ant–symbiont interactions. A low specificity host taxa and a positive association between host abundance and parasitoid interaction frequency were expected due to the close phylogenetic relatedness of the hosts. 3. The interactions among all species of leafcutter ants and their parasitoids were quantified in two localities with different species richness. This study also characterised the spatial‐temporal variability of these interactions, determined the patterns of parasitoid specificity and host selection, and tested for an association between host abundance and parasitoid interaction frequency. 4. Contrary to expectation, most parasitoid species were highly specialised and interaction frequency for parasitoid species was not related to host abundance. All host ant species were attacked by more than one phorid species. Some phorid species used more than one host species and showed preference for the same species over space and time, suggesting that there are physiological and/or behavioural restrictions on host use. 5. These results show that there is a tendency for specialisation even when hosts are highly similar in their ecology. From a biological control perspective, these parasitoids may be effective candidates, due to the high specificity of some species and little host‐use variation through time.     

Estimating parasitoid immature mortality by comparing oviposition and pupal development of Trichogramma galloi Zucchi and T. pretiosum Riley on natural and factitious hosts

Mortality during the immature development of T. galloi and T. pretiosum was estimated on UV-killed and live eggs of a factitious and a natural host, respectively. A staining technique was used to determine the actual parasitization of UV-treated eggs and was compared with the number of parasitoids that emerged per host egg (detectable parasitization). Effects of temperature as a factor of mortality during the immature development of both parasitoids on the factitious host was also assessed. The actual and detectable parasitization of live hosts was measured by recording both the parasitization behavior and the number of eggs where a parasitoid developed successfully. Our data show that mortality during immature development of both parasitoids may occur in live eggs of the natural host. No such mortality was observed when parasitoids developed on UV-killed eggs of the factitious host. Possible causes of parasitoid immature mortality and the effects of using UV-treated eggs of factitious hosts in estimating the parasitism capacity of Trichogramma in field conditions are discussed.     

Traits across trophic levels interact to influence parasitoid establishment in biological control releases

A central goal in ecology is to predict what governs a species’ ability to establish in a new environment. One mechanism driving establishment success is individual species’ traits, but the role of trait combinations among interacting species across different trophic levels is less clear. Deliberate or accidental species additions to existing communities provide opportunities to study larger scale patterns of establishment success. Biological control introductions are especially valuable because they contain data on both the successfully established and unestablished species. Here, we used a recent dataset of importation biological control introductions to explore how life‐history traits of 132 parasitoid species and their herbivorous hosts interact to affect parasitoid establishment. We find that of five parasitoid and herbivore traits investigated, one parasitoid trait—host range—weakly predicts parasitoid establishment; parasitoids with higher levels of phylogenetic specialization have higher establishment success, though the effect is marginal. In addition, parasitoids are more likely to establish when their herbivore host has had a shorter residence time. Interestingly, we do not corroborate earlier findings that gregarious parasitoids and endoparasitoids are more likely to establish. Most importantly, we find that life‐history traits of the parasitoid species and their hosts can interact to influence establishment. Specifically, parasitoids with broader host ranges are more likely to establish when the herbivore they have been released to control is also more of a generalist. These results provide insight into how multiple species’ traits and their interactions, both within and across trophic levels, can influence establishment of species of higher trophic levels.     

You stay,but I Hop: Host shifting near and far co‐dominated the evolution of Enchenopa treehoppers

The importance and prevalence of phylogenetic tracking between hosts and dependent organisms caused by co‐evolution and shifting between closely related host species have been debated for decades. Most studies of phylogenetic tracking among phytophagous insects and their host plants have been limited to insects feeding on a narrow range of host species. However, narrow host ranges can confound phylogenetic tracking (phylogenetic tracking hypothesis) with host shifting between hosts of intermediate relationship (intermediate hypothesis). Here, we investigated the evolutionary history of the Enchenopa binotata complex of treehoppers. Each species in this complex has high host fidelity, but the entire complex uses hosts across eight plant orders. The phylogenies of E. binotata were reconstructed to evaluate whether (1) tracking host phylogeny; or (2) shifting between intermediately related host plants better explains the evolutionary history of E. binotata. Our results suggest that E. binotata primarily shifted between both distant and intermediate host plants regardless of host phylogeny and less frequently tracked the phylogeny of their hosts. These findings indicate that phytophagous insects with high host fidelity, such as E. binotata, are capable of adaptation not only to closely related host plants but also to novel hosts, likely with diverse phenology and defense mechanisms.     

Physiological and biochemical aspects of interactions between insect parasitoids and their hosts

In the present review, available literary data on physiological and biochemical interactions between parasitoids and their hosts are analyzed. In order to achieve successful development inside or on their hosts, parasitoids widely use various strategies aimed at suppressing host immunity. Suppression agents used by parasitoids include venom and ovarian fluid components as well as symbiotic microorganisms. The influence of parasitoids on the host organism is complicated, covering many physiological functions and inducing changes of the host metabolism and behavior. The influence of ecto- and endoparasitoids on the host organism is analyzed separately.     

Host Niches and Defensive Extended Phenotypes Structure Parasitoid Wasp Communities

Oak galls are spectacular extended phenotypes of gallwasp genes in host oak tissues and have evolved complex morphologies that serve, in part, to exclude parasitoid natural enemies.Parasitoids and their insect herbivore hosts have coevolved to produce diverse communities comprising about a third of all animal species. The factors structuring these communities, however, remain poorly understood. An emerging theme in community ecology is the need to consider the effects of host traits, shaped by both natural selection and phylogenetic history, on associated communities of natural enemies. Here we examine the impact of host traits and phylogenetic relatedness on 48 ecologically closed and species-rich communities of parasitoids attacking gall-inducing wasps on oaks. Gallwasps induce the development of spectacular and structurally complex galls whose species- and generation-specific morphologies are the extended phenotypes of gallwasp genes. All the associated natural enemies attack their concealed hosts through gall tissues, and several structural gall traits have been shown to enhance defence against parasitoid attack. Here we explore the significance of these and other host traits in predicting variation in parasitoid community structure across gallwasp species. In particular, we test the “Enemy Hypothesis,” which predicts that galls with similar morphology will exclude similar sets of parasitoids and therefore have similar parasitoid communities. Having controlled for phylogenetic patterning in host traits and communities, we found significant correlations between parasitoid community structure and several gall structural traits (toughness, hairiness, stickiness), supporting the Enemy Hypothesis. Parasitoid community structure was also consistently predicted by components of the hosts'' spatiotemporal niche, particularly host oak taxonomy and gall location (e.g., leaf versus bud versus seed). The combined explanatory power of structural and spatiotemporal traits on community structure can be high, reaching 62% in one analysis. The observed patterns derive mainly from partial niche specialisation of highly generalist parasitoids with broad host ranges (>20 hosts), rather than strict separation of enemies with narrower host ranges, and so may contribute to maintenance of the richness of generalist parasitoids in gallwasp communities. Though evolutionary escape from parasitoids might most effectively be achieved via changes in host oak taxon, extreme conservatism in this trait for gallwasps suggests that selection is more likely to have acted on gall morphology and location. Any escape from parasitoids associated with evolutionary shifts in these traits has probably only been transient, however, due to subsequent recruitment of parasitoid species already attacking other host galls with similar trait combinations.     

Evolutionary patterns of host utilization by ichneumonoid parasitoids (Hymenoptera: Ichneumonidae and Braconidae)*

The four major biological strategies of ichneumonoid parasitoids, koinobiont and idiobiont, ecto-and endoparasitism, are discussed and the evolutionary radiations of the two families Ichneumonidae and Braconidae compared in an attempt to relate differences in patterns of host utilization to differences in evolutionary history. The most primitive members of both families are idiobiont ectoparasitoids of hosts concealed in plant tissue. Idiobiont ectoparasitic braconids are all still primarily associated with such hosts, but idiobiont ectoparasitic ichneumonids have radiated to attack hosts in other situations, such as in aculeate nests or in cocoons. A shift in emphasis between the behavioural steps, host habitat location and host location, is envisaged as being important in such evolutionary change. Idiobiont endoparasitism is postulated as having arisen amongst ectoparasitoids attacking cocooned hosts, as an adaptation that allows them to exploit pupae and puparia in relatively exposed positions; it is a fairly common strategy in the Ichneumonidae, but virtually unknown in the Braconidae. Koinobiosis is perceived as having evolved in association with hosts which feed in a relatively weakly concealed position, but pupate in a more secluded and safe location. The strategy is advantageous as it allows a parasitoid to oviposit on an easily discoverable host, but to use the host's pupation concealment to complete its own development. The evolution of koinobiosis has allowed parasitoids to exploit hosts that feed in exposed positions, and to attack hosts at a younger and numerically more common stage in the host's life cycle. Koinobiont ectoparasitism is envisaged, in some braconid and ichneumonid groups, to occupy an evolutionary transitional position between idiobiosis and endoparasitic koinobiosis; only in the Ichneumonidae have large radiations of koinobiont ectoparasitoids occurred. Endoparasitic koinobiosis is hypothesized as having arisen in the Braconidae in association with lepidopterous/coleopterous hosts, whilst in the major lineage of endoparasitic koinobiont ichneumonids, this habit is hypothesized as having arisen in association with symphytan hosts. The great majority of braconids are koinobiont endoparasitoids, but only about 50% of the Ichneumonidae have this habit. Very few koinobiont braconids develop as endoparasitoids of hymenopterous hosts, although many endoparasitic ichneumonids attack Hymenoptera. However, lineages of the Braconidae have radiated to exploit adult insects and exopterygote nymphs; ichneumonids do not utilize such hosts.     

Responses of a generalist and a specialist parasitoid (Hymenoptera: Eucoilidae) to Drosophilid larval kairomones

Foraging parasitoids are thought to need more specific information than generalists on the presence, identity, availability, and suitability of their insect host species. In the present paper, we compare responses to host kairomones by two phylogenetically related parasitoid species that attack Drosophilidae and that differ in the width of their host range. As predicted, the behavioral response of the parasitoids to host kairomones reflected their difference in host range. The response of the specialist parasitoid Leptopilina boulardiwas restricted to contact kairomones from its natural hosts and one closely related species. In contrast, the generalist parasitoid Leptopilina heterotomaresponded to contact kairomones of a variety of Drosophilidae species.     

Abundance,not diversity,of host beetle communities determines abundance and diversity of parasitoids in deadwood

Most parasites and parasitoids are adapted to overcome defense mechanisms of their specific hosts and hence colonize a narrow range of host species. Accordingly, an increase in host functional or phylogenetic dissimilarity is expected to increase the species diversity of parasitoids. However, the local diversity of parasitoids may be driven by the accessibility and detectability of hosts, both increasing with increasing host abundance. Yet, the relative importance of these two mechanisms remains unclear. We parallelly reared communities of saproxylic beetle as potential hosts and associated parasitoid Hymenoptera from experimentally felled trees. The dissimilarity of beetle communities was inferred from distances in seven functional traits and from their evolutionary ancestry. We tested the effect of host abundance, species richness, functional, and phylogenetic dissimilarities on the abundance, species richness, and Shannon diversity of parasitoids. Our results showed an increase of abundance, species richness, and Shannon diversity of parasitoids with increasing beetle abundance. Additionally, abundance of parasitoids increased with increasing species richness of beetles. However, functional and phylogenetic dissimilarity showed no effect on the diversity of parasitoids. Our results suggest that the local diversity of parasitoids, of ephemeral and hidden resources like saproxylic beetles, is highest when resources are abundant and thereby detectable and accessible. Hence, in some cases, resources do not need to be diverse to promote parasitoid diversity.     

Evolution of parasitoid host preference and performance in response to an invasive host acting as evolutionary trap

The invasion of a novel host species can create a mismatch in host choice and offspring survival (performance) when native parasitoids attempt to exploit the invasive host without being able to circumvent its resistance mechanisms. Invasive hosts can therefore act as evolutionary trap reducing parasitoids'' fitness and this may eventually lead to their extinction. Yet, escape from the trap can occur when parasitoids evolve behavioral avoidance or a physiological strategy compatible with the trap host, resulting in either host‐range expansion or a complete host‐shift. We developed an individual based model to investigate which conditions promote parasitoids to evolve behavioral preference that matches their performance, including host‐trap avoidance, and which conditions lead to adaptations to the unsuitable hosts. The model was inspired by solitary endo‐parasitoids attacking larval host stages. One important aspect of these conditions was reduced host survival during incompatible interaction, where a failed parasitization attempt by a parasitoid resulted not only in death of her offspring but also in host killing. This non‐reproductive host mortality had a strong influence on the likelihood of establishment of novel host–parasitoid relationship, in some cases constraining adaptation to the trap host species. Moreover, our model revealed that host‐search efficiency and genetic variation in host‐preference play a key role in the likelihood that parasitoids will include the suboptimal host in their host range, or will evolve behavioral avoidance resulting in specialization and host‐range conservation, respectively. Hence, invasive species might change the evolutionary trajectory of native parasitoid species, which is important for predicting biocontrol ability of native parasitoids towards novel hosts.     

WASP‐ASSOCIATED FACTORS ACT IN INTERSPECIES COMPETITION DURING MULTIPARASITISM

Coexistence or displacement of parasitoids in hosts during intrinsic competitive interactions between different parasitoid species (multiparasitism) may depend on their life history traits and behavior. Intense competition for possession of hosts may lead to the elimination of the inferior competitor through physical attack and/or physiological suppression. However, the mechanisms of physiological suppression during multiparasitism remain unclear. Previous work has shown that first instar larvae of the solitary endoparasitoid Meteorus pulchricornis possess well‐developed mandibles that are used to kill competitors. Two gregarious endoparasitoids, Cotesia kariyai and C. rufricus, share host resources especially when the time gap of oviposition is short. Here, we investigated the physiological influence of wasp‐regulatory factors of the three endoparasitoids, M. pulchricornis, C. kariyai, and C. ruficrus, in their common host Mythimna separata. We found that MpVLP alone (or with venom) deleteriously affected the development of the two gregarious species. Similarly, CkPDV plus venom had toxic effect on M. pulchricornis eggs and immature larvae, although they were not harmful to immature stages of C. ruficrus. Cotesia kariyai and C. ruficrus were able to coexist mainly through the expression of regulatory factors and both could successfully emerge from a multiparasitized host. The injection of CkPDV plus venom after oviposition in L5 host larvae facilitated C. ruficrus development and increased the rate of successful parasitism from 9% to 62%. This suggests that the two gregarious parasitoid wasps exhibit strong phylogenetic affinity, favoring their coexistence and success in multiparasitized hosts.     

The Impact of Plant Enemies Shows a Phylogenetic Signal

The host ranges of plant pathogens and herbivores are phylogenetically constrained, so that closely related plant species are more likely to share pests and pathogens. Here we conducted a reanalysis of data from published experimental studies to test whether the severity of host-enemy interactions follows a similar phylogenetic signal. The impact of herbivores and pathogens on their host plants declined steadily with phylogenetic distance from the most severely affected focal hosts. The steepness of this phylogenetic signal was similar to that previously measured for binary-response host ranges. Enemy behavior and development showed similar, but weaker phylogenetic signal, with oviposition and growth rates declining with evolutionary distance from optimal hosts. Phylogenetic distance is an informative surrogate for estimating the likely impacts of a pest or pathogen on potential plant hosts, and may be particularly useful in early assessing risk from emergent plant pests, where critical decisions must be made with incomplete host records.     

Phytophagy on phylogenetically isolated trees: why hosts should escape their relatives

Hosts belonging to the same species suffer dramatically different impacts from their natural enemies. This has been explained by host neighbourhood, that is, by surrounding host-species diversity or spatial separation between hosts. However, even spatially neighbouring hosts may be separated by many million years of evolutionary history, potentially reducing the establishment of natural enemies and their impact. We tested whether phylogenetic isolation of oak hosts from neighbouring trees within a forest canopy reduces phytophagy. We found that an increase in phylogenetic isolation by 100 million years corresponded to a 10-fold decline in phytophagy. This was not due to poorer living conditions for phytophages on phylogenetically isolated oaks. Neither species diversity of neighbouring trees nor spatial distance to the closest oak affected phytophagy. We suggest that reduced pressure by natural enemies is a major advantage for individuals within a host species that leave their ancestral niche and grow among distantly related species.     

Evolution of host breadth in broad interactions: mycorrhizal specificity in East Asian and North American rattlesnake plantains (Goodyera spp.) and their fungal hosts

Host breadth is often assumed to have no evolutionary significance in broad interactions because of the lack of cophylogenetic patterns between interacting species. Nonetheless, the breadth and suite of hosts utilized by one species may have adaptive value, particularly if it underlies a common ecological niche among hosts. Here, we present a preliminary assessment of the evolution of mycorrhizal specificity in 12 closely related orchid species (genera Goodyera and Hetaeria) using DNA‐based methods. We mapped specificity onto a plant phylogeny that we estimated to infer the evolutionary history of the mycorrhiza from the plant perspective, and hypothesized that phylogeny would explain a significant portion of the variance in specificity of plants on their host fungi. Sampled plants overwhelmingly associated with genus Ceratobasidium, but also occasionally with some ascomycetes. Ancestral mycorrhizal specificity was narrow in the orchids, and broadened rarely as Goodyera speciated. Statistical tests of phylogenetic inertia suggested some support for specificity varying with increasing phylogenetic distance, though only when the phylogenetic distance between suites of fungi interacting with each plant taxon were taken into account. These patterns suggest a role for phylogenetic conservatism in maintaining suits of fungal hosts among plants. We stress the evolutionary importance of host breadth in these organisms, and suggest that even generalists are likely to be constrained evolutionarily to maintaining associations with their symbionts.     

Biological control of tortricidae in tea fields in Japan using insect viruses and parasitoids

Tea is a perennial and evergreen plant. Cultivated tea trees provide a habitat for insect pests and their natural enemies. In Japan, granuloviruses (GVs) have successfully controlled two of the most important pests of tea, Adoxophyes honmai and Homona magnanima (Tortricidae: Lepidoptera). The GVs are produced in vivo and a single application sustains pesticidal efficacy throughout a year, which encompasses 4 to 5 discrete generations of both species. A. honmai and H. magnanima also have various natural enemies, especially hymenopteran parasitoids. Such resident natural enemies also play a role in reducing the pest density in virus-controlled fields, but the effect of virus infection on parasitoids sharing the same host larva has not been well studied. Survival of one of the major parasitoids ofA. honmai, Ascogaster reticulata (Braconidae: Hymenoptera), is reduced by virus infection of the host. Viruses, including GV and entomopoxvirus (EPV), and certain koinobiont endoparasitoids, including A. reticulata, are both known to regulate host endocrinology. However, the GV and EPV have distinct host regulation mechanisms, and consequently have different impacts on the survival of A. retuculata, when A. reticulata parasitizes a host that is infected with either GV or EPV. These additional effects on host regulation displayed by both viruses and parasitoids affect the outcome of virus-parasitoid interactions.     

Endophyte-mediated tritrophic interactions between a grass-feeding caterpillar and two parasitoid species with different life histories

Plant secondary chemicals can alter herbivore suitability for parasitoids by weakening or stunting the host, delaying its development, or when larval parasitoids encounter ingested phytotoxins in the body of their host. Experiments with different parasitoids that exploit the same host species feeding on the same plant may provide insight about how parasitoid life history affects the strength of such interactions. The encyrtid wasp Copidosoma bakeri, a slow-developing polyembryonic egg-larval parasitoid, and the tachinid fly Linnaemya comta, a fast-developing solitary species, both parasitize Agrotis ipsilon, a generalist noctuid. We tested the hypothesis that of the two parasitoid species, the encyrtid, because of its more prolonged developmental association with the host, would suffer greater fitness costs when A. ipsilon feeds on perennial ryegrass containing an alkaloid-producing fungal endophyte. Indeed, fewer parasitized cutworms yielded C. bakeri broods, and those host mummies were smaller, formed more slowly, and contained fewer adults when the hosts fed on endophytic as opposed to endophyte-free grass. In contrast, L. comta fitness parameters were similar regardless of the type of grass upon which their host fed. Our results highlight that the outcome of endophyte-mediated tritrophic interactions may differ for different parasitoid species. Implications for integrating the use of endophytic grasses and biological control are discussed.     

Fitness-related changes in laboratory populations of the egg parasitoid <Emphasis Type="Italic">Trichogramma galloi</Emphasis> and the implications of rearing on factitious hosts

In this study, we used the specialist egg parasitoid Trichogramma galloi Zucchi, 1988 (Hymenoptera: Trichogrammatidae) to test whether development over multiple generations on a factitious host would later influence performance on the target pest. We also investigated possible adaptations to laboratory rearing conditions by monitoring over 50 and 46 generations life history traits of T. galloi populations maintained on the natural [Diatraea saccharalis (Fabr., 1794) (Lepidoptera: Crambidae)] and factitious host [Ephestia kuehniella (Zeller, 1879) (Lepidoptera: Pyralidae)], respectively. We detected a possible sign of adaptation to rearing conditions in early generations on the emergence of the population maintained on the natural host. We also verified a reduction in fecundity and emergence of parasitoids maintained on the factitious host when fitness was evaluated on the natural host, confirming the prediction that the use of factitious hosts can lower fitness on the target pest. The importance of these results for the effectiveness of biological control programs is discussed.     

Phylogenetic signal in module composition and species connectivity in compartmentalized host-parasite networks

Abstract Across different taxa, networks of mutualistic or antagonistic interactions show consistent architecture. Most networks are modular, with modules being distinct species subsets connected mainly with each other and having few connections to other modules. We investigate the phylogenetic relatedness of species within modules and whether a phylogenetic signal is detectable in the within- and among-module connectivity of species using 27 mammal-flea networks from the Palaearctic. In the 24 networks that were modular, closely related hosts co-occurred in the same module more often than expected by chance; in contrast, this was rarely the case for parasites. The within- and among-module connectivity of the same host or parasite species varied geographically. However, among-module but not within-module connectivity of host and parasites was somewhat phylogenetically constrained. These findings suggest that the establishment of host-parasite networks results from the interplay between phylogenetic influences acting mostly on hosts and local factors acting on parasites, to create an asymmetrically constrained pattern of geographic variation in modular structure. Modularity in host-parasite networks seems to result from the shared evolutionary history of hosts and by trait convergence among unrelated parasites. This suggests profound differences between hosts and parasites in the establishment and functioning of bipartite antagonistic networks.     

Does mother really know best? Oviposition preference reduces reproductive performance in the generalist parasitoid Aphidius ervi

The reproductive success of female parasitoids is dependent on their ability to accurately assess the suitability of a host for larval development. For generalist parasitoids, which utilize a broad range of species and instars as hosts, a set of assessment criteria determines whether a host is accepted or rejected. The suitability of a host, however, can only be imperfectly assessed by the female parasitoid, which can result in the selection of lesser quality hosts for oviposition. In this study we explored the disparity between host quality and host preference using the generalist koinobiotic parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae) and the host Aulacorthum solani (Harris) (Homoptera: Aphididae), the foxglove aphid. The second instar hosts produced the highest level of reproductive success, while third and fourth instars resulted in a substantially reduced reproductive performance. When given a choice of host instars, parasitoids preferred the older hosts for oviposition disregarding their reduced suitability for larval development. Results are discussed in context of mechanisms involved in A. ervi host selection and biases in the criteria used to assess hosts that may arise when parasitoids transfer host species between generations.     

'Divergent male ontogenies' in Aphelinidae (Hymenoptera: Ghalcidoidea): a simplified classification and a suggested evolutionary sequence

A classification of the different types of divergent male ontogeny in Aphelinidae is proposed to replace the little known and cumbersome systems previously published. All the Aphelinidae in which conspecific males and females have different host relationships, i.e. those that have divergent ontogenies, are here designated heteronomous parasitoids. Females of these species are primary endoparasitoids of Homoptera. The males of (i) diphagous parasitoids are primary ectoparasitoids of the same host species exploited by their females, (ii) heteronomous hyperparasitoids develop hyperparasitically, and (iii) heterotrophic species are endoparasitoids of lepidopterous eggs. Heteronomous hyperparasitoids can be classified further as obligate autoparasitoids, facultative autoparasitoids or alloparasitoids. All the species of heteronomous aphelinids whose biologies are known are listed according to the new classification, and the evolutionary sequence of these unusual host relationships is discussed.