Increased fluctuation in a butterfly metapopulation leads to diploid males and decline of a hyperparasitoid.
ABSTRACT: Climate change can increase spatial synchrony of population dynamics, leading to large-scale fluctuation that destabilizes communities. High trophic level species such as parasitoids are disproportionally affected because they depend on unstable resources. Most parasitoid wasps have complementary sex determination, producing sterile males when inbred, which can theoretically lead to population extinction via the diploid male vortex (DMV). We examined this process empirically using a hyperparasitoid population inhabiting a spatially structured host population in a large fragmented landscape. Over four years of high host butterfly metapopulation fluctuation, diploid male production by the wasp increased, and effective population size declined precipitously. Our multitrophic spatially structured model shows that host population fluctuation can cause local extinctions of the hyperparasitoid because of the DMV. However, regionally it persists because spatial structure allows for efficient local genetic rescue via balancing selection for rare alleles carried by immigrants. This is, to our knowledge, the first empirically based study of the possibility of the DMV in a natural host-parasitoid system.
Project description:A fragmented habitat becomes increasingly fragmented for species at higher trophic levels, such as parasitoids. To persist, these species are expected to possess life-history traits, such as high dispersal, that facilitate their ability to use resources that become scarce in fragmented landscapes. If a specialized parasitoid disperses widely to take advantage of a sparse host, then the parasitoid population should have lower genetic structure than the host. We investigated the temporal and spatial genetic structure of a hyperparasitoid (fourth trophic level) in a fragmented landscape over 50 × 70 km, using microsatellite markers, and compared it with the known structures of its host parasitoid, and the butterfly host which lives as a classic metapopulation. We found that population genetic structure decreases with increasing trophic level. The hyperparasitoid has fewer genetic clusters (K = 4), than its host parasitoid (K = 15), which in turn is less structured than the host butterfly (K = 27). The genetic structure of the hyperparasitoid also shows temporal variation, with genetic differentiation increasing due to reduction of the population size, which reduces the effective population size. Overall, our study confirms the idea that specialized species must be dispersive to use a fragmented host resource, but that this adaptation has limits.
Project description:Agricultural intensification (AI) is currently a major driver of biodiversity loss and related ecosystem functioning decline. However, spatio-temporal changes in community structure induced by AI, and their relation to ecosystem functioning, remain largely unexplored. Here, we analysed 16 quantitative cereal aphid-parasitoid and parasitoid-hyperparasitoid food webs, replicated four times during the season, under contrasting AI regimes (organic farming in complex landscapes vs. conventional farming in simple landscapes). High AI increased food web complexity but also temporal variability in aphid-parasitoid food webs and in the dominant parasitoid species identity. Enhanced complexity and variability appeared to be controlled bottom-up by changes in aphid dominance structure and evenness. Contrary to the common expectations of positive biodiversity-ecosystem functioning relationships, community complexity (food-web complexity, species richness and evenness) was negatively related to primary parasitism rates. However, this relationship was positive for secondary parasitoids. Despite differences in community structures among different trophic levels, ecosystem services (parasitism rates) and disservices (aphid abundances and hyperparasitism rates) were always higher in fields with low AI. Hence, community structure and ecosystem functioning appear to be differently influenced by AI, and change differently over time and among trophic levels. In conclusion, intensified agriculture can support diverse albeit highly variable parasitoid-host communities, but ecosystem functioning might not be easy to predict from observed changes in community structure and composition.
Project description:Parasitoids are hyperdiverse and can contain morphologically and functionally cryptic species, making them challenging to study. Parasitoid speciation can arise from specialisation on niches or diverging hosts. However, which process dominates is unclear because cospeciation across multiple parasitoid and host species has rarely been tested. Host specificity and trophic interactions of the parasitoids of psyllids (Hemiptera) remain mostly unknown, but these factors are fundamentally important for understanding of species diversity, and have important applied implications for biological control.We sampled diverse parasitoid communities from eight Eucalyptus-feeding psyllid species in the genera Cardiaspina and Spondyliaspis, and characterised their phylogenetic and trophic relationships using a novel approach that forensically linked emerging parasitoids with the presence of their DNA in post-emergence insect mummies. We also tested whether parasitoids have cospeciated with their psyllid hosts. The parasitoid communities included three Psyllaephagus morphospecies (two primary and, unexpectedly, one heteronomous hyperparasitoid that uses different host species for male and female development), and the hyperparasitoid, Coccidoctonus psyllae. However, the number of genetically delimited Psyllaephagus species was three times higher than the number of recognisable morphospecies, while the hyperparasitoid formed a single generalist species. In spite of this, cophylogenetic analysis revealed unprecedented codivergence of this hyperparasitoid with its primary parasitoid host, suggesting that this single hyperparasitoid species is possibly diverging into host-specific species. Overall, parasitoid and hyperparasitoid diversification was characterised by functional conservation of morphospecies, high host specificity and some host switching between sympatric psyllid hosts.We conclude that host specialisation, host codivergence and host switching are important factors driving the species diversity of endoparasitoid communities of specialist host herbivores. Specialisation in parasitoids can also result in heteronomous life histories that may be more common than appreciated. A host generalist strategy may be rare in endoparasitoids of specialist herbivores despite the high conservation of morphology and trophic roles, and endoparasitoid species richness is likely to be much higher than previously estimated. This also implies that the success of biological control requires detailed investigation to enable accurate identification of parasitoid-host interactions before candidate parasitoid species are selected as biological control agents for target pests.
Project description:Molecular approaches are increasingly being used to analyse host-parasitoid food webs as they overcome several hurdles inherent to conventional approaches. However, such studies have focused primarily on the detection and identification of aphids and their aphidiid primary parasitoids, largely ignoring primary parasitoid-hyperparasitoid interactions or limiting these to a few common species within a small geographical area. Furthermore, the detection of bacterial secondary endosymbionts has not been considered in such assays despite the fact that endosymbionts may alter aphid-parasitoid interactions, as they can confer protection against parasitoids. Here we present a novel two-step multiplex PCR (MP-PCR) protocol to assess cereal aphid-primary parasitoid-hyperparasitoid-endosymbiont interactions. The first step of the assay allows detection of parasitoid DNA at a general level (24 primary and 16 hyperparasitoid species) as well as the species-specific detection of endosymbionts (3 species) and cereal aphids (3 species). The second step of the MP-PCR assay targets seven primary and six hyperparasitoid species that commonly occur in Central Europe. Additional parasitoid species not covered by the second-step of the assay can be identified via sequencing 16S rRNA amplicons generated in the first step of the assay. The approach presented here provides an efficient, highly sensitive, and cost-effective (~consumable costs of 1.3 € per sample) tool for assessing cereal aphid-parasitoid-endosymbiont interactions.
Project description:Understanding how climate change affects host-parasite systems and predicting the consequences for ecosystems, economies, and human health has emerged as an important task for science and society. Some basic insight into this complex problem can be gained by comparing the thermal physiology of interacting host and parasite species. In this study, we compared upper thermal tolerance among three component species in a natural host-parasitoid-hyperparasitoid system from Virginia, USA. To assess the ecological relevance of our results, we also examined a record of maximum daily air temperatures collected near the study site in the last 124 years. We found that the caterpillar host Manduca sexta had a critical thermal maximum (CTmax) about 4°C higher than the parasitic wasp, Cotesia congregata, and the hyperparasitic wasp, Conura sp., had a CTmax about 6°C higher than its host, C. congregata. We also found significant differences in CTmax among instars and between parasitized and non-parasitized M. sexta. The highest maximum daily air temperature recorded near the study in the last 124 years was 42°C, which equals the average CTmax of one species (C. congregata) but is several degrees lower than the average CTmax of the other two species (M. sexta, Conura sp.) in this study. Our results combined with other studies suggest that significant differences in thermal performance within and among interacting host and parasite species are common in nature and that climate change may be largely disruptive to these systems with responses that are highly variable and complex.
Project description:Facultative bacterial endosymbionts can protect their aphid hosts from natural enemies such as hymenopteran parasitoids. As such, they have the capability to modulate interactions between aphids, parasitoids and hyperparasitoids. However, the magnitude of these effects in natural aphid populations and their associated parasitoid communities is currently unknown. Moreover, environmental factors such as plant fertilization and landscape complexity are known to affect aphid-parasitoid interactions but it remains unclear how such environmental factors affect the interplay between aphids, parasitoids and endosymbionts. Here, we tested whether facultative endosymbionts confer protection to parasitoids in natural populations of the English grain aphid, Sitobion avenae, and if this is affected by plant fertilization and landscape complexity. Furthermore, we examined whether the effects of facultative endosymbionts can cascade up to the hyperparasitoid level and increase primary-hyperparasitoid food web specialization. Living aphids and mummies were collected in fertilized and unfertilized plots within 13 wheat fields in Central Germany. We assessed the occurrence of primary parasitoid, hyperparasitoid and endosymbiont species in aphids and mummies using a newly established molecular approach. Facultative endosymbiont infection rates were high across fields (~80%), independent of whether aphids were parasitized or unparasitized. Aphid mummies exhibited a significantly lower share of facultative endosymbiont infection (~38%). These findings suggest that facultative endosymbionts do not affect parasitoid oviposition behaviour, but decrease parasitoid survival in the host. Facultative endosymbiont infection rates were lower in mummies collected from fertilized compared to unfertilized plants, indicating that plant fertilization boosts the facultative endosymbiont protective effect. Furthermore, we found strong evidence for species-specific and negative cascading effects of facultative endosymbionts on primary and hyperparasitoids, respectively. Facultative endosymbionts impacted parasitoid assemblages and increased the specialization of primary-hyperparasitoid food webs: these effects were independent from and much stronger than other environmental factors. The current findings strongly suggest that facultative endosymbionts act as a driving force in aphid-parasitoid-hyperparasitoid networks: they shape insect community composition at different trophic levels and modulate, directly and indirectly, the interactions between aphids, parasitoids and their environment.
Project description:The cotton aphid, Aphis gossypii (Hemiptera: Aphididae), is a serious pest of cotton across the globe, particularly in the cotton agroecosystems of northern China. Parasitic wasps are deemed to be important natural enemies of A. gossypii, but limited information exists about their species composition, richness and seasonal dynamics in northern China. In this study, we combine sampling over a broad geographical area with intensive field trials over the course of three cropping seasons to describe parasitoid-hyperparasitoid communities in cotton crops. We delineate a speciose complex of primary parasitoids and hyperparasitoids associated with A. gossypii. Over 90% of the primary parasitoids were Binodoxys communis. Syrphophagus sp. and Pachyneuron aphidis made up most of the hyperparasitoids. Parasitism rates changed in a similar way following the fluctuation of the aphid population. Early in the growing period, there were more hyperparasitoids, while later, the primary parasitoids provided control of A. gossypii. The first systematic report of this cotton aphid parasitoid complex and their population dynamics in association with their hosts presented a comprehensive assessment of cotton parasitoid species and provided important information for the establishment and promotion of their biological control of cotton aphids.
Project description:Although consumers often rely on chemical information to optimize their foraging strategies, it is poorly understood how top carnivores above the third trophic level find resources in heterogeneous environments. Hyperparasitoids are a common group of organisms in the fourth trophic level that lay their eggs in or on the body of other parasitoid hosts. Such top carnivores use herbivore-induced plant volatiles (HIPVs) to find caterpillars containing parasitoid host larvae. Hyperparasitoids forage in complex environments where hosts of different quality may be present alongside non-host parasitoid species, each of which can develop in multiple herbivore species. Because both the identity of the herbivore species and its parasitization status can affect the composition of HIPV emission, hyperparasitoids encounter considerable variation in HIPVs during host location. Here, we combined laboratory and field experiments to investigate the role of HIPVs in host selection of hyperparasitoids that search for hosts in a multi-parasitoid multi-herbivore context. In a wild Brassica oleracea-based food web, the hyperparasitoid Lysibia nana preferred HIPVs emitted in response to caterpillars parasitized by the gregarious host Cotesia glomerata over the non-host Hyposoter ebeninus. However, no plant-mediated discrimination occurred between the solitary host C. rubecula and the non-host H. ebeninus. Under both laboratory and field conditions, hyperparasitoid responses were not affected by the herbivore species (Pieris brassicae or P. rapae) in which the three primary parasitoid species developed. Our study shows that HIPVs are an important source of information within multitrophic interaction networks allowing hyperparasitoids to find their preferred hosts in heterogeneous environments.
Project description:Aphid-parasitoid interactions have been widely used as a model system in research studies on the structure and functions of arthropod food web. Research on aphid-parasitoid food webs is hindered by their micromorphological characteristics and the high amount of labor associated with their development. Species-specific primers for cotton aphids and their parasitoids were designed and integrated into two multiplex PCRs and six singleplex PCRs, and all PCRs were optimized to achieve high specificity and sensitivity (100-10,000 DNA copies). One cotton aphid (Aphis gossypii) as well as three primary parasitoid and seven hyperparasitoid species or genera were detected using this molecular approach. This group comprises all the primary parasitoids and 97.2-99.6% of the hyperparasitoids reported in cotton fields in northern China. A tritrophic aphid-primary parasitoid-hyperparasitoid food web was then established. The described method constitutes an efficient tool for quantitatively describing the aphid-primary parasitoid-hyperparasitoid food webs and assessing the efficiency of the biological control of parasitoids in cotton fields in northern China.
Project description:A new species, Cheiloneurus nankingensis sp. nov., from Eastern China is described. It is similar to C. arabiacus Hayat but distinct from it in a number of morphological characters. It is a hyperparasitoid with the encyrtid wasp Aenasius arizonensis Girault, 1915 as the primary host and the cotton mealybug Phenacoccus solenopsis Tinsley, 1898 (Hemiptera: Pseudococcidae) as the secondary host. A key to all seven species of Cheiloneurus known from China is presented.