Friend or foe? A parasitic wasp shifts the cost/benefit ratio in a nursery pollination system impacting plant fitness.

Nursery pollination systems are species interactions where pollinators also act as fruit/seed herbivores of the plant partner. While the plants depend on associated insects for pollination, the insects depend on the plants' reproductive structures for larval development. The outcome of these interactions is thus placed on a gradient between mutualism and antagonism. Less specialized interactions may fluctuate along this gradient with the ecological context, where natural enemies can play an important role. We studied whether a natural enemy may impact the level of seed consumption of a nursery pollinator and how this in turn may influence individual plant fitness. We used the plant Silene latifolia, its herbivore Hadena bicruris, and its ectoparasitoid Bracon variator as a model plant-herbivore-natural enemy system. We investigated seed output, germination, survival, and flower production as proxies for individual plant fitness. We show that B. variator decreases the level of seed consumption by H. bicruris larvae which in turn increased seed output in S. latifolia plants, suggesting that parasitism by B. variator may act as a regulator in the system. However, our results also show that plant survival and flower production decrease with higher seed densities, and therefore, an increase in seed output may be less beneficial for plant fitness than estimated from seed output alone. Our study should add another layer to the complex discussion of whether parasitoids contribute to plant fitness, as we show that taking simple proxies such as seed output is insufficient to determine the net effect of multitrophic interactions.

Egg laying rather than host quality or host feeding experience drives habitat estimation in the parasitic wasp Nasonia vitripennis.

In variable environments, sampling information on habitat quality is essential for making adaptive foraging decisions. In insect parasitoids, females foraging for hosts have repeatedly been shown to employ behavioral strategies that are in line with predictions from optimal foraging models. Yet, which cues exactly are employed to sample information on habitat quality has rarely been investigated. Using the gregarious parasitoid Nasonia vitripennis (Walker; Hymenoptera: Pteromalidae), we provided females with different cues about hosts to elucidate, which of them would change a wasp's posterior behavior suggesting a change in information status. We employed posterior clutch size decisions on a host as proxy for a female's estimation of habitat quality. Taking into account changes in physiological state of the foraging parasitoid, we tested whether different host qualities encountered previously change the subsequent clutch size decision in females. Additionally, we investigated whether other kinds of positive experiences-such as ample time to investigate hosts, host feeding, or egg laying-would increase a wasp's estimated value of habitat quality. Contrary to our expectations, quality differences in previously encountered hosts did not affect clutch size decisions. However, we found that prior egg laying experience changes posterior egg allocation to a host, indicating a change in female information status. Host feeding and the time available for host inspection, though correlated with egg laying experience, did not seem to contribute to this change in information status.

The hitchhiker's guide to Europe: the infection dynamics of an ongoing Wolbachia invasion and mitochondrial selective sweep in Rhagoletis cerasi.

Wolbachia is a maternally inherited and ubiquitous endosymbiont of insects. It can hijack host reproduction by manipulations such as cytoplasmic incompatibility (CI) to enhance vertical transmission. Horizontal transmission of Wolbachia can also result in the colonization of new mitochondrial lineages. In this study, we present a 15-year-long survey of Wolbachia in the cherry fruit fly Rhagoletis cerasi across Europe and the spatiotemporal distribution of two prevalent strains, wCer1 and wCer2, and associated mitochondrial haplotypes in Germany. Across most of Europe, populations consisted of either 100% singly (wCer1) infected individuals with haplotype HT1, or 100% doubly (wCer1&2) infected individuals with haplotype HT2, differentiated only by a single nucleotide polymorphism. In central Germany, singly infected populations were surrounded by transitional populations, consisting of both singly and doubly infected individuals, sandwiched between populations fixed for wCer1&2. Populations with fixed infection status showed perfect association of infection and mitochondria, suggesting a recent CI-driven selective sweep of wCer2 linked with HT2. Spatial analysis revealed a range expansion for wCer2 and a large transition zone in which wCer2 splashes appeared to coalesce into doubly infected populations. Unexpectedly, the transition zone contained a large proportion (22%) of wCer1&2 individuals with HT1, suggesting frequent intraspecific horizontal transmission. However, this horizontal transmission did not break the strict association between infection types and haplotypes in populations outside the transition zone, suggesting that this horizontally acquired Wolbachia infection may be transient. Our study provides new insights into the rarely studied Wolbachia invasion dynamics in field populations.

Intraspecific variability in associative learning in the parasitic wasp Nasonia vitripennis.

The ability to learn is key to behavioral adaptation to changing environments. Yet, learning rate and memory retention can vary greatly across or even within species. While interspecific differences have been attributed to ecological context or life history constraints, intraspecific variability in learning behavior is rarely studied and more often, ignored: inferences of the cognitive abilities of a species are most of the time made from experiments using individuals of a single population. Here, we show that learning of host-associated cues in the parasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) shows considerable interpopulation variability, which is at least partly, genetically determined. The strengths of the learning response differed predictably between populations and also varied with the rewarding stimulus. We tested memory retention in a genetically diverse strain and in an iso-female line, bearing a low genetic variability. In addition, we compared our findings with published studies on a third strain using a meta-analytical approach. Our findings suggest that all three strains differ in memory formation from each other. We conclude that, even though the associative learning of host cues is most likely under strong natural selection in parasitoid wasps, considerable genetic variability is maintained at the population as well as at the species level in N. vitripennis.

Genetic incompatibility drives mate choice in a parasitic wasp.

INTRODUCTION: Allelic incompatibility between individuals of the same species should select for mate choice based on the genetic make-up of both partners at loci that influence offspring fitness. As a consequence, mate choice may be an important driver of allelic diversity. A complementary sex determination (CSD) system is responsible for intraspecific allelic incompatibility in many species of ants, bees, and wasps. CSD may thus favour disassortative mating and in this, resembles the MHC of the vertebrate immune system, or the self-incompatibility (SI) system of higher plants. RESULTS: Here we show that in the monogamous parasitic wasp Bracon brevicornis (Wesmael), females are able to reject partners with incompatible alleles. Forcing females to accept initially rejected partners resulted in sex ratio distortion and partial infertility of offspring. CONCLUSIONS: CSD-disassortative mating occurred independent of kin recognition and inbreeding avoidance in our experiment. The fitness consequences of mate choice are directly observable, not influenced by environmental effects, and more severe than in comparable systems (SI or MHC), on individuals as well as at the population level. Our results thus demonstrate the strong potential of female mate choice for maintaining high offspring fitness in this species.

Does kin recognition and sib-mating avoidance limit the risk of genetic incompatibility in a parasitic wasp?

BACKGROUND: When some combinations of maternal and paternal alleles have a detrimental effect on offspring fitness, females should be able to choose mates on the basis of their genetic compatibility. In numerous Hymenoptera, the sex of an individual depends of the allelic combination at a specific locus (single-locus Complementary Sex Determination), and in most of these species individuals that are homozygous at this sexual locus develop into diploid males with zero fitness. METHODS AND FINDINGS: In this paper, we tested the hypothesis of genetic incompatibility avoidance by investigating sib-mating avoidance in the solitary wasp parasitoid, Venturia canescens. In the context of mate choice we show, for the first time in a non-social hymenopteran species, that females can avoid mating with their brothers through kin recognition. In "no-choice" tests, the probability a female will mate with an unrelated male is twice as high as the chance of her mating with her brothers. In contrast, in choice tests in small test arenas, no kin discrimination effect was observed. Further experiments with male extracts demonstrate that chemical cues emanating from related males influence the acceptance rate of unrelated males. CONCLUSIONS: Our results are compatible with the genetic incompatibility hypothesis. They suggest that the female wasps recognize sibs on the basis of a chemical signature carried or emitted by males possibly using a "self-referent phenotype matching" mechanism.

Decision-making dynamics in parasitoids of Drosophila.

Drosophilids and their associated parasitoids live in environments that vary in resource availability and quality within and between generations. The use of information to adapt behavior to the current environment is a key feature under such circumstances and Drosophila parasitic wasps are excellent model systems to study learning and information use. They are among the few parasitoid model species that have been tested in a wide array of situations. Moreover, several related species have been tested under similar conditions, allowing the analysis of within and between species variability, the effect of natural selection in a typical environment, the current physiological status, and previous experience of the individual. This holds for host habitat and host location as well as for host choice and search time allocation. Here, we review patterns of learning and memory, of information use and updating mechanisms, and we point out that information use itself is under strong selective pressure and thus, optimized by parasitic wasps.

Spatial aggregation across ephemeral resource patches in insect communities: an adaptive response to natural enemies?

Although an increase in competition is a common cost associated with intraspecific crowding, spatial aggregation across food-limited resource patches is a widespread phenomenon in many insect communities. Because intraspecific aggregation of competing insect larvae across, e.show $132#g. fruits, dung, mushrooms etc., is an important means by which many species can coexist (aggregation model of species coexistence), there is a strong need to explore the mechanisms that contribute to the maintenance of this kind of spatial resource exploitation. In the present study, by using Drosophila-parasitoid interactions as a model system, we tested the hypothesis whether intraspecific aggregation reflects an adaptive response to natural enemies. Most of the studies that have hitherto been carried out on Drosophila-parasitoid interactions used an almost two-dimensional artificial host environment, where host larvae could not escape from parasitoid attacks, and have demonstrated positive density-dependent parasitism risk. To test whether these studies captured the essence of such interactions, we used natural breeding substrates (decaying fruits). In a first step, we analysed the parasitism risk of Drosophila larvae on a three-dimensional substrate in natural fly communities in the field, and found that the risk of parasitism decreased with increasing host larval density (inverse density dependence). In a second step, we analysed the parasitism risk of Drosophila subobscura larvae on three breeding substrate types exposed to the larval parasitoids Asobara tabida and Leptopilina heterotoma. We found direct density-dependent parasitism on decaying sloes, inverse density dependence on plums, and a hump-shaped relationship between fly larval density and parasitism risk on crab apples. On crab apples and plums, fly larvae benefited from a density-dependent refuge against the parasitoids. While the proportion of larvae feeding within the fruit tissues increased with larval density, larvae within the fruit tissues were increasingly less likely to become victims of parasitoids than those exposed at the fruit surface. This suggests a facilitating effect of group-feeding larvae on reaching the spatial refuge. We conclude that spatial aggregation in Drosophila communities can at least in part be explained as a predator avoidance strategy, whereby natural enemies act as selective agents maintaining spatial patterns of resource utilisation in their host communities.

An evolutionary explanation of the aggregation model of species coexistence.

In ecology, the 'aggregation model of coexistence' provides a powerful concept to explain the unexpectedly high species richness of insects on ephemeral resources like dung pats, fruits, etc. It suggests that females aggregate their eggs across resource patches, which leads to an increased intraspecific competition within occupied patches and a relatively large number of patches that remain unoccupied. This provides competitor-free patches for heterospecifics, facilitating species coexistence. At first glance, deliberately causing competition among the females' own offspring and leaving resources to heterospecific competitors seems altruistic and incompatible with individual fitness maximization, raising the question of how natural selection operates in favour of egg aggregation on ephemeral resource patches. Allee effects that lead to fitness maxima at intermediate egg densities have been suggested, but not yet detected. Using drosophilid flies on decaying fruits as a study system, we demonstrate a hump-shaped relationship between egg density and individual survival probability, with maximum survivorship at intermediate densities. This pattern clearly selects for egg aggregation and resolves the possible conflict between the ecological concept of species coexistence on ephemeral resources and evolutionary theory.