The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species

In the hymenopteran parasitoid Venturia canescens, asexual (obligate thelytoky not induced by Wolbachia bacteria) and sexual (arrhenotokous) wasps coexist in field conditions despite the demographic cost incurred due to the production of males by sexual females. Arrhenotoky predominates in field conditions, whereas populations in indoor conditions (mills, granaries) are exclusively thelytokous. These differences in the relative abundance of the two modes of reproduction between environments suggest that the individuals of each reproductive mode may have developed strategies adapted to the conditions prevailing in each kind of habitat. The two environments contrast in temperature variability and in the spatial heterogeneity of host availability. In this study, we considered the combined effect of temperature and host availability on host patch exploitation by thelytokous and arrhenotokous V. canescens. As expected, arrhenotokous females were more sensitive to temperature changes. If the temperature decreased before foraging, they remained longer and exploited patches more thoroughly. This is consistent with the expected behaviour of parasitoids in response to signs of unfavourable conditions that entail increasing risk of time limitation or a reduced probability of attaining further patches. Both arrhenotokous and thelytokous females increased patch exploitation with host availability. However, unexpectedly, we found no difference in the way the two types of wasp responded to differences in host availability. Differences in the strategies adopted under different environmental conditions may indicate divergence of niche-specific life history traits between the two modes of reproduction. Niche displacement may partly account for the coexistence of these two modes of reproduction at a geographical scale.     

Utilisation of chemical signals by inquiline wasps in entering their host figs

The fig tree, Ficus curtipes, hosts an obligate pollinating wasp, an undescribed Eupristina sp., but can also be pollinated by two inquiline (living in the burrow, nest, gall, or other habitation of another animal) wasps, Diaziella yangi and an undescribed Lipothymus sp. The two inquilines are unable to independently induce galls and depend on the galls induced by the obligate pollinator for reproduction and, therefore, normally enter receptive F. curtipes figs colonised by the obligate pollinators. However, sometimes the inquilines also enter figs that are not colonised by the pollinators, despite consequent reproductive failure. It is still unknown which signal(s) the inquilines use in entering the colonised and non-colonised figs. We conducted behavioural experiments to investigate several possible signals utilised by the inquilines in entering their host receptive figs. Our investigation showed that both inquiline species enter the receptive F. curtipes figs in response to the body odours of the obligate wasps and one of the main compounds emitted by the figs, 6-methyl-5-hepten-2-one. The compound was not found in the pollinator body odours, suggesting that the two inquiline wasps can utilise two signals to enter their host figs, which is significant for the evolution of the fig-fig wasp system. These inquilines could evolve to become mutualists of the figs if they evolve the ability to independently gall fig flowers; there is, however, another possibility that a monoecious Ficus species hosting such inquilines may evolve into a dioecious one if these inquilines cannot evolve the above-mentioned ability. Additionally, this finding provides evidence for the evolution of chemical communication between plants and insects.     

Patch exploitation strategies of parasitic wasps under intraspecific competition

The optimal residence time of a forager exploiting a resourcepatch in the absence of competitors has been much studied sincethe development of the marginal value theorem. However, severalforagers are frequently observed exploiting the same patch simultaneously,and patch residence time has been surprisingly little studiedin such competitive situations. The few theoretical models developedon this topic predict that foragers should engage in a war ofattrition and stay in the patch longer than when foraging alone.We tested this prediction in Pachycrepoideus vindemmiae (Hymenoptera:Pteromalidae), a solitary parasitoid species in which femalesare known to defend the hosts they are exploiting via intraspecificfighting. By measuring the effect of direct (i.e., presenceof conspecifics) and indirect (i.e., presence of already-parasitizedhosts) competition on patch exploitation strategies, we revealedan apparent polymorphism of strategies. Indeed, in competitivesituations, some members of the population tended to retreatalmost immediately from the patch whereas other members tendedto remain, further exploit the patch, and be more involved ininteractions with conspecifics. The proportion of "retreaters"strongly depended on competition intensity and prior experienceof competition. The forager's physiological state (age) alsoaffects patch exploitation strategy and the intensity of interactionsbetween competing females. Our results highlight the necessityfor further theoretical studies that consider cases where contestsbetween foragers are costly and take into account prior experienceof competition and the forager's physiological state.     

The evolution of host use and unusual reproductive strategies in Achrysocharoides parasitoid wasps

We studied host selection and exploitation, two crucial aspects of parasite ecology, in Achrysocharoides parasitoid wasps, which show remarkable host specificity and unusual offspring sex allocation. We estimated a molecular phylogeny of 15 Achrysocharoides species and compared this with host (plant and insect) phylogenies. This tri-trophic phylogenetic comparison provides no evidence for cospeciation, but parasitoids do show phylogenetic conservation of the use of plant genera. Patterns of sequence divergence also suggest that the parasitoids radiated more recently (or evolved much faster) than their insect hosts. Three main categories of brood production occur in parasitoids: (1) solitary offspring, (2) mixed sex broods and (3) separate (split) sex broods. Split sex broods are very rare and virtually restricted to Achrysocharoides, while the other types occur very widely. Our phylogeny suggests that split sex broods have evolved twice and provides evidence for a transition from solitary to mixed sex broods, via split sex broods, as predicted by theory.     

Molecular phylogenies of figs and their pollinator wasps

Abstract. We collected and analysed nucleotide sequence and protein electrophoretic data in order to estimate phylogenies of figs and fig-pollinating wasps at several taxonomic scales. The relatively conserved chloroplast gene coding rbCl allowed the estimation of the taxonomic position of Ficus relative to other genera within the Moraceae. Further, in conjunction with chloroplast tRNA spacer genes, rbcL sequences allowed the partial resolution of the phylogenetic associations of fig species from different parts of the world with representatives from all the recognized subgenera of Ficus . The phylogeny of the corresponding wasp species that pollinate most of those taxa was estimated using mitochondrial COI-COII and 12S ribosomal genes. At a fine scale, the phylogenies of species within two subgenera of figs growing in Panama ( Urostigma , and Pharmacosycea) were estimated by using protein electrophoretic data. The phylogeny of the corresponding pollinator wasp species was estimated using COII sequence data. Although we need to extend the taxa sampled and augment the molecular database, the host and pollinator phylogenies show a high degree of congruence and the results support the predominance of strict-sense co-evolution between figs and their pollinator wasps at both global and fine scales.     

Seasonal dynamic shifts in patch exploitation by parasitic wasps

We developed and tested predictions of a dynamic life historymodel that is concerned with how temperate-zone parasitic waspsadjust patch residence time and tendency to superparasitizewhen expectation of life and habitat quality varies. The theorypredicts that wasps with short life expectancy should continueto search longer and superparasitize more frequently than similarwasps with long life expectancy. Similarly, wasps with longlife expectancy that forage in habitats where patches are alreadyheavily exploited should continue to search longer and superparasitizemore frequently than similar wasps foraging in habitats wherepatches are relatively unexploited. In contrast, the theorypredicts that wasps with short life expectancy will be insensitiveto habitat quality. We tested the predictions on Drosophilaparasitoids (Lep-topilina heterotoma) by (1) rearing wasps underfall and summer photoperiod (i.e., short versus long life expectancy)and (2) giving wasps foraging experience on different qualitypatches (i.e., exploited versus unexploited habitats). Resultsof the experiments corroborated our predictions. We discusshow parasitic wasp behavior can be shaped by globally predictableand locally unpredictable events.     

Chemosensory attraction of fig wasps to substances produced by receptive figs

In the mutualism between figs (Ficus spp., Moraceae) and their species-specific fig wasp pollinators (Hymenoptera: Agaonidae), location of a receptive host tree by the adult insect is a critical step. The adult female wasp lives only a few days, and must usually fly to a different tree than her natal tree to locate receptive figs. Trees in receptive phase often occur at very low densities. Reproductive success of both fig and wasp depends on trasmission of a very strong signal by the plant. Some evidence exists for the role of olfaction in location of receptive hosts by fig wasps, but very little work has been done on the chemical ecology of host location and host specificity. Here the first experimental evidence is presented for long-distance olfactory attraction of wasps by volatile substances produced by receptive figs, and for short-distance or contact chemostimulation by host volatiles that elicit entry of the wasp into the fig. In studies usingFicus carica L., pentane extracts of receptive-phase figs attract the pollinatorBlastophaga psenes L. from distances of at least 5 m in the field. Short-distance chemostimulation was demonstrated in laboratory bioassays. Pentane extracts of receptive figs, when painted onto the ostiole of non-receptive figs, elicit entry of pollinator wasps. Figs emit volatile compounds attractive to pollinating wasps only during the period of receptivity; pentane extracts of non-receptive figs are not attractive. A simple reliable procedure is described to compare the attractivity of different types of extracts (total, internal, and external extracts) and of different fractions, in the first step towards identifying attractant substances.     

Patterns of diversification of Afrotropical Otiteselline fig wasps: phylogenetic study reveals a double radiation across host figs and conservatism of host association

We studied the phylogenetic relationships of Otiteselline fig waSPS associated with Ficus in the Afrotropical region using rDNA sequences. African fig species usually host two species of Otiteselline fig waSPS. Phylogenetic analyses reveal that this pattern of association results from the radiation of two clades of waSPS superimposed on the fig system. Within each clade, wasp species generally cluster according to their host classification. The phylogenies of the two clades are also generally more congruent than expected by chance. Together these results suggest that Otiteselline wasp speciation is largely constrained by the diversification of their hosts. Finally, we show a difference in ovipositor length between the two Otiteselline species coexisting in the same Ficus species, which probably corresponds to ecological differences. The diversification of ecological niches within the fig is probably, with cospeciation, one of the key factors explaining the diversification and maintenance of species of parasites of the fig/pollinator system.     

Vibratory stimuli in host location by parasitic wasps

Parasitic wasps use a broad spectrum of different stimuli for host location and host acceptance. Here we review the published evidence for the use of mechanical stimuli, i.e. substrate born vibrations which are invariably regarded as vibrotaxis. We propose a set of criteria to class behavioural reactions as vibrotaxis or vibrokinesis and characterize 14 studies reporting the use of host-associated vibrations by parasitoids. The studies are compared concerning (i) experimental design; (ii) characterisation of vibrational signals; and (iii) progress of the parasitoid towards the host.The recent experimental development based on new measurement techniques shows the growing body of evidence that host-associated vibrations are exploited by parasitic wasps. Nevertheless a definite proof for vibrotaxis is still lacking. To assess the exact mechanisms by which parasitoids use vibrations bioassays comparing reactions to natural and artificially generated signals are needed. Vibrotaxis as well as vibrokinesis are both helpful host location strategies for parasitoids foraging in a multimodal environment. At the community level they may lead to niche differentiation.     

Different host exploitation strategies in two zebra mussel-trematode systems: adjustments of host life history traits

The zebra mussel is the intermediate host for two digenean trematodes, Phyllodistomum folium and Bucephalus polymorphus, infecting gills and the gonad respectively. Many gray areas exist relating to the host physiological disturbances associated with these infections, and the strategies used by these parasites to exploit their host without killing it. The aim of this study was to examine the host exploitation strategies of these trematodes and the associated host physiological disturbances. We hypothesized that these two parasite species, by infecting two different organs (gills or gonads), do not induce the same physiological changes. Four cellular responses (lysosomal and peroxisomal defence systems, lipidic peroxidation and lipidic reserves) in the host digestive gland were studied by histochemistry and stereology, as well as the energetic reserves available in gonads. Moreover, two indices were calculated related to the reproductive status and the physiological condition of the organisms. Both parasites induced adjustments of zebra mussel life history traits. The host-exploitation strategy adopted by P. folium would occur during a short-term period due to gill deformation, and could be defined as "virulent." Moreover, this parasite had significant host gender-dependent effects: infected males displayed a slowed-down metabolism and energetic reserves more allocated to growth, whereas females displayed better defences and would allocate more energy to reproduction and maintenance. In contrast, B. polymorphus would be a more "prudent" parasite, exploiting its host during a long-term period through the consumption of reserves allocated to reproduction.     

The expression of virulence during double infections by different parasites with conflicting host exploitation and transmission strategies

In many natural populations, hosts are found to be infected by more than one parasite species. When these parasites have different host exploitation strategies and transmission modes, a conflict among them may arise. Such a conflict may reduce the success of both parasites, but could work to the benefit of the host. For example, the less‐virulent parasite may protect the host against the more‐virulent competitor. We examine this conflict using the waterflea Daphnia magna and two of its sympatric parasites: the blood‐infecting bacterium Pasteuria ramosa that transmits horizontally and the intracellular microsporidium Octosporea bayeri that can concurrently transmit horizontally and vertically after infecting ovaries and fat tissues of the host. We quantified host and parasite fitness after exposing Daphnia to one or both parasites, both simultaneously and sequentially. Under conditions of strict horizontal transmission, Pasteuria competitively excluded Octosporea in both simultaneous and sequential double infections, regardless of the order of exposure. Host lifespan, host reproduction and parasite spore production in double infections resembled those of single infection by Pasteuria. When hosts became first vertically (transovarilly) infected with O. bayeri, Octosporea was able to withstand competition with P. ramosa to some degree, but both parasites produced less transmission stages than they did in single infections. At the same time, the host suffered from reduced fecundity and longevity. Our study demonstrates that even when competing parasite species utilize different host tissues to proliferate, double infections lead to the expression of higher virulence and ultimately may select for higher virulence. Furthermore, we found no evidence that the less‐virulent and vertically transmitting O. bayeri protects its host against the highly virulent P. ramosa.     

Parasitic wasps attracted by the sex pheromone of their coccid host

Sticky traps baited with live virgin females of the California red scale, placed in citrus groves to capture male scales, also attracted parasitic wasps ofAphytis spp. The number of wasps captured per trap (>500) reached up to 75 % of all insects caught in some citrus groves not treated with pesticides. Laboratory experiments withAphytis melinus andA. coheni and other wasps, carried out simultaneously in two different olfactometers, showed that the two species ofAphytis were highly responsive to the sex pheromone of California female red scales.     

Host-feeding strategies of parasitoid wasps

Summary Three models of the evolution of host-feeding behaviour in parasitoid wasps are developed. The first assumes that the wasp host feeds purely to obtain resources to mature eggs (limited resource model) while the second assumes that host feeding provides energy for maintenance (pro-ovigenic model). The third model assumes that host feeding provides resources for both maintenance and egg maturation (resource pool model). Two variants of the third model are examined: the first assumes that the risk of mortality is constant and state-independent, the second that resource-depleted individuals suffer a higher risk of mortality. The models are analysed using a combination of stochastic dynamic programming and analytical techniques. The models make different predictions about the relationships between the probability of host feeding and egg load and host density. The available experimental evidence best supports the resource pool model.     

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.     

Coyness,philandering and stable strategies

An example put forward by Dawkins to describe the evolution of strategies in the conflict of the sexes over parental investment is discussed by means of a simple dynamic system. It is shown that the equilibrium of the strategies is not evolutionarily stable, but equal to the time average of the endlessly oscillating strategies.     

Perturbation and exploitation of host cell cytoskeleton by periodontal pathogens

Some periodontal pathogens disrupt epithelial barriers and cellular adhesion to the extracellular matrix, which affects the cytoskeleton. Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans exploit the cytoskeleton during their uptake by epithelial cells. Treponema denticola perturbs actin and actin-regulating pathways in host cells. Cytoskeletal dysfunction due to pathogenic bacteria may impair physiologic remodeling and wound repair in the periodontium.     

The use of visual cues in host evaluation by aphidiid wasps

We examined host evaluation behaviour in three species of aphid parasitoids, Ephedrus californicus Baker, Monoctonus paulensis (Ashmead), and Praon pequodorum Viereck (Hymenoptera: Aphidiidae). Mated females were provided with pairwise choices among three kinds of hosts in the laboratory: (green) pea aphid, Acyrthosiphon pisum (Harris), and a green and a pink colour morph of alfalfa aphid, Macrosiphum creelii Davis. Patterns of attack and host acceptance were species-specific. Females of E. californicus did not respond to the presence of aphids prior to making antennal contact. Variations in rates of parasitization (pea aphid>green alfalfa aphid>pink alfalfa aphid) were consistent with differences in aphid defensive behaviours; no ‘preference’ for any host type was evident when aphids were anaesthetized with carbon dioxide. In M. paulensis, the order of preference (pea aphid>green alfalfa aphid>pink alfalfa aphid) did not vary when aphids were immobilized, or presented in the dark, or both. Host movement did not influence the rate of attack by M. paulensis. In contrast, the ranked order of preference in P. pequodorum varied with circumstance. In the light, females attacked pea aphid and green alfalfa aphid with equal frequency, but parasitized significantly more of the former; both kinds of aphids were attacked and parasitized at higher rates than pink alfalfa aphid. In the dark, P. pequodorum females parasitized green and pink alfalfa aphids equally and at higher rates than pea aphids. Whereas E. californicus was more successful ovipositing in immobilized hosts, P. pequodorum females attacked and laid more eggs in normal than anaesthetized aphids. Patterns of host recognition and evaluation are compared across six species representing four genera in the family Aphidiidae.