Environmental stressors can be key drivers of phenotypes, including reproductive strategies and morphological traits. The response to stress may be altered by the presence of microbial associates. For example, in aphids, facultative (secondary) bacterial symbionts can provide protection against natural enemies and stress induced by elevated temperatures. Furthermore, aphids exhibit phenotypic plasticity, producing winged (rather than wingless) progeny that may be better able to escape danger, and the combination of these factors improves the response to stress. How symbionts and phenotypic plasticity, both of which shape aphids' stress response, influence one another, and together influence host fitness, remains unclear. In this study, we investigate how environmental stressors drive shifts in fecundity and winged/wingless offspring production, and how secondary symbionts influence the process. We induced production of winged offspring through distinct environmental stressors, including exposure to aphid alarm pheromone and crowding, and, in one experiment, we assessed whether the aphid response is influenced by host plant. In the winged morph, energy needed for wing maintenance may lead to trade-offs with other traits, such as reproduction or symbiont maintenance. Potential trade-offs between symbiont maintenance and fitness have been proposed but have not been tested. Thus, beyond studying the production of offspring of alternative morphs, we also explore the influence of symbionts across wing/wingless polyphenism as well as symbiont interaction with cross-generational impacts of environmental stress on reproductive output. All environmental stressors resulted in increased production of winged offspring and shifts in fecundity rates. Additionally, in some cases, aphid host-by-symbiont interactions influenced fecundity. Stress on first-generation aphids had cross-generational impacts on second-generation adults, and the impact on fecundity was further influenced by the presence of secondary symbionts and presence/absence of wings. Our study suggests a complex interaction between beneficial symbionts and environmental stressors. Winged aphids have the advantage of being able to migrate out of danger with more ease, but energy needed for wing production and maintenance may come with reproductive costs for their mothers and for themselves, where in certain cases, these costs are altered by secondary symbionts.
- MeSH
- Bacteria MeSH
- hrách setý MeSH
- křídla zvířecí MeSH
- mšice * MeSH
- symbióza MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Research Support, N.I.H., Extramural MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
Understanding interactions between herbivores and parasitoids is essential for successful biodiversity protection and monitoring and for biological pest control. Morphological identifications employ insect rearing and are complicated by insects' high diversity and crypsis. DNA barcoding has been successfully used in studies of host-parasitoid interactions as it can substantially increase the recovered real host-parasitoid diversity distorted by overlooked species complexes, or by species with slight morphological differences. However, this approach does not allow the simultaneous detection and identification of host(s) and parasitoid(s). Recently, high-throughput sequencing has shown high potential for surveying ecological communities and trophic interactions. Using mock samples comprising insect larvae and their parasitoids, we tested the potential of DNA metabarcoding for identifying individuals involved in host-parasitoid interactions to different taxonomic levels, and compared it to standard DNA barcoding and morphological approaches. For DNA metabarcoding, we targeted the standard barcoding marker cytochrome oxidase subunit I using highly degenerate primers, 2*300 bp sequencing on a MiSeq platform, and RTAX classification using paired-end reads. Additionally, using a large host-parasitoid dataset from a Central European floodplain forest, we assess the completeness and usability of a local reference library by confronting the number of Barcoding Index Numbers obtained by standard barcoding with the number of morphotypes. Overall, metabarcoding recovery was high, identifying 92.8% of the taxa present in mock samples, and identification success within individual taxonomic levels did not significantly differ among metabarcoding, standard barcoding, and morphology. Based on the current local reference library, 39.4% parasitoid and 90.7% host taxa were identified to the species level. DNA barcoding estimated higher parasitoid diversity than morphotyping, especially in groups with high level of crypsis. This study suggests the potential of metabarcoding for effectively recovering host-parasitoid diversity, together with more accurate identifications obtained from building reliable and comprehensive reference libraries, especially for parasitoids.
Animal-associated microbial communities have important effects on host phenotypes. Individuals within and among species differ in the strains and species of microbes that they harbour, but how natural selection shapes the distribution and abundance of symbionts in natural populations is not well understood. Symbionts can be beneficial in certain environments but also impose costs on their hosts. Consequently, individuals that can or cannot associate with symbionts will be favoured under different ecological circumstances. As a result, we predict that individuals within a species vary in terms of how well they accept and maintain symbionts. In pea aphids, the frequency of endosymbionts varies among host-plant-associated populations ('biotypes'). We show that aphid genotypes from different biotypes vary in how well they accept and maintain symbionts after horizontal transfer. We find that aphids from biotypes that frequently harbour symbionts are better able to associate with novel symbionts than those from biotypes that less frequently harbour symbionts. Intraspecific variation in the ability of hosts to interact with symbionts is an understudied factor explaining patterns of host-symbiont association.
- MeSH
- genotyp MeSH
- mšice MeSH
- přenos genů horizontální MeSH
- symbióza * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
The microbial symbionts of eukaryotes influence disease resistance in many host-parasite systems. Symbionts show substantial variation in both genotype and phenotype, but it is unclear how natural selection maintains this variation. It is also unknown whether variable symbiont genotypes show specificity with the genotypes of hosts or parasites in natural populations. Genotype by genotype interactions are a necessary condition for coevolution between interacting species. Uncovering the patterns of genetic specificity among hosts, symbionts, and parasites is therefore critical for determining the role that symbionts play in host-parasite coevolution. Here, we show that the strength of protection conferred against a fungal pathogen by a vertically transmitted symbiont of an aphid is influenced by both host-symbiont and symbiont-pathogen genotype by genotype interactions. Further, we show that certain symbiont phylogenetic clades have evolved to provide stronger protection against particular pathogen genotypes. However, we found no evidence of reciprocal adaptation of co-occurring host and symbiont lineages. Our results suggest that genetic variation among symbiont strains may be maintained by antagonistic coevolution with their host and/or their host's parasites.
- MeSH
- fylogeneze MeSH
- genetická variace MeSH
- genotyp * MeSH
- houby patogenita MeSH
- mšice parazitologie MeSH
- symbióza * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Eukaryotes commonly host communities of heritable symbiotic bacteria, many of which are not essential for their hosts' survival and reproduction. There is laboratory evidence that these facultative symbionts can provide useful adaptations, such as increased resistance to natural enemies. However, we do not know how symbionts affect host fitness when the latter are subject to attack by a natural suite of parasites and pathogens. Here, we test whether two protective symbionts, Regiella insecticola and Hamiltonella defensa, increase the fitness of their host, the pea aphid (Acyrthosiphon pisum), under natural conditions. We placed experimental populations of two pea aphid lines, each with and without symbionts, in five wet meadow sites to expose them to a natural assembly of enemy species. The aphids were then retrieved and mortality from parasitoids, fungal pathogens and other causes assessed. We found that both Regiella and Hamiltonella reduce the proportion of aphids killed by the specific natural enemies against which they have been shown to protect in laboratory and cage experiments. However, this advantage was nullified (Hamiltonella) or reversed (Regiella) by an increase in mortality from other natural enemies and by the cost of carrying the symbiont. Symbionts therefore affect community structure by altering the relative success of different natural enemies. Our results show that protective symbionts are not necessarily advantageous to their hosts, and may even behave more like parasites than mutualists. Nevertheless, bacterial symbionts may play an important role in determining food web structure and dynamics.
- MeSH
- Enterobacteriaceae fyziologie MeSH
- genetická zdatnost MeSH
- houby fyziologie MeSH
- interakce hostitele a parazita MeSH
- interakce hostitele a patogenu * MeSH
- mšice genetika mikrobiologie parazitologie fyziologie MeSH
- sršňovití fyziologie MeSH
- symbióza * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interacting with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.
- MeSH
- biodiverzita MeSH
- biologické modely MeSH
- býložravci fyziologie MeSH
- dieta * MeSH
- ekosystém MeSH
- fylogeneze MeSH
- hmyz klasifikace fyziologie MeSH
- hostitelská specificita MeSH
- Lepidoptera klasifikace fyziologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
Plant-insect food webs tend to be dominated by interactions resulting from diffuse co-evolution between plants and multiple lineages of herbivores rather than by reciprocal co-evolution and co-cladogenesis. Plants therefore require defence strategies effective against a broad range of herbivore species. In one extreme, plants could develop a single universal defence effective against all herbivorous insects, or tailor-made strategies for each herbivore species. The evolution and ecology of plant defence has to be studied with entire insect assemblages, rather than small subsets of pairwise interactions. The present study examines whether specialists and generalists in three coexisting insect lineages, forming the leaf-chewing guild, respond uniformly to plant phylogeny, secondary metabolites, nutrient content and mechanical antiherbivore defences of their hosts, thus permitting universal plant defence strategies against specialized and generalist folivorous insects from various taxa. The extensive data on folivorous assemblages comprising three insect orders and 193 species are linked with plant phylogeny, secondary chemistry (salicylates, flavonoids and tannins), leaf morphological traits [specific leaf area (SLA) and trichome coverage], nutrient (C : N) content and growth form of eight willow (Salix) and one aspen (Populus) species growing in sympatry. Generalists responded to overall host plant chemistry and trichomes, whilst specialists responded to host plant phylogeny and secondary metabolites that are unique to willows and that are capable of being utilized as an antipredator protection. We did not find any significant impact of other plant traits, that is SLA, C : N ratio, flavonoids, tannins and growth form, on the composition of leaf-chewing communities. Our results show that the response to plant traits is differential among specialists and generalists. This finding constrains the ability of plants to develop defensive traits universally effective against herbivores and may lead to diversification of plant defensive mechanisms into several complementary syndromes, required for effective protection against generalists and specialists from multiple insect taxa comprising most leaf-chewing assemblages. These results point to the necessity of broad studies of plant-herbivore interactions, across multiple insect taxa and guilds.
- MeSH
- biologická evoluce MeSH
- býložravci * MeSH
- flavonoidy analýza MeSH
- fylogeneze MeSH
- hmyz fyziologie MeSH
- listy rostlin anatomie a histologie chemie MeSH
- Populus anatomie a histologie chemie MeSH
- salicylany analýza MeSH
- Salix anatomie a histologie chemie genetika MeSH
- taniny analýza MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
The processes maintaining the enormous diversity of herbivore-parasitoid food webs depend on parasitism rate and parasitoid host specificity. The two parameters have to be evaluated in concert to make conclusions about the importance of parasitoids as natural enemies and guide biological control. We document parasitism rate and host specificity in a highly diverse caterpillar-parasitoid food web encompassing 266 species of lepidopteran hosts and 172 species of hymenopteran or dipteran parasitoids from a lowland tropical forest in Papua New Guinea. We found that semi-concealed hosts (leaf rollers and leaf tiers) represented 84% of all caterpillars, suffered a higher parasitism rate than exposed caterpillars (12 vs. 5%) and their parasitoids were also more host specific. Semi-concealed hosts may therefore be generally more amenable to biological control by parasitoids than exposed ones. Parasitoid host specificity was highest in Braconidae, lower in Diptera: Tachinidae, and, unexpectedly, the lowest in Ichneumonidae. This result challenges the long-standing view of low host specificity in caterpillar-attacking Tachinidae and suggests higher suitability of Braconidae and lower suitability of Ichneumonidae for biological control of caterpillars. Semi-concealed hosts and their parasitoids are the largest, yet understudied component of caterpillar-parasitoid food webs. However, they still remain much closer in parasitism patterns to exposed hosts than to what literature reports on fully concealed leaf miners. Specifically, semi-concealed hosts keep an equally low share of idiobionts (2%) as exposed caterpillars.
- MeSH
- Diptera fyziologie MeSH
- ekosystém MeSH
- fyziologie rostlin MeSH
- Hymenoptera fyziologie MeSH
- interakce hostitele a parazita MeSH
- larva parazitologie MeSH
- můry parazitologie MeSH
- potravní řetězec * MeSH
- společenstvo * MeSH
- stravovací zvyklosti MeSH
- tropické klima MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Geografické názvy
- Papua Nová Guinea MeSH
Classical niche theory explains the coexistence of species through their exploitation of different resources. Assemblages of herbivores coexisting on a particular plant species are thus expected to be dominated by species from host-specific guilds with narrow, coexistence-facilitating niches rather than by species from generalist guilds. Exactly the opposite pattern is observed for folivores feeding on trees in New Guinea. The least specialized mobile chewers were the most species rich, followed by the moderately specialized semiconcealed and exposed chewers. The highly specialized miners and mesophyll suckers were the least species-rich guilds. The Poisson distribution of herbivore species richness among plant species in specialized guilds and the absence of a negative correlation between species richness in different guilds on the same plant species suggest that these guilds are not saturated with species. We show that herbivore assemblages are enriched with generalists because these are more completely sampled from regional species pools. Herbivore diversity increases as a power function of plant diversity, and the rate of increase is inversely related to host specificity. The relative species diversity among guilds is thus scale dependent, as the importance of specialized guilds increases with plant diversity. Specialized insect guilds may therefore comprise a larger component of overall diversity in the tropics (where they are also poorly known taxonomically) than in the temperate zone, which has lower plant diversity.
- MeSH
- biodiverzita MeSH
- biologická adaptace fyziologie MeSH
- biologické modely MeSH
- druhová specificita MeSH
- hmyz fyziologie MeSH
- interakce hostitele a parazita MeSH
- potravní řetězec MeSH
- stromy parazitologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Geografické názvy
- Nová Guinea MeSH
Previously, host-parasitoid links have been unveiled almost exclusively by time-intensive rearing, while molecular methods were used only in simple agricultural host-parasitoid systems in the form of species-specific primers. Here, we present a general method for the molecular detection of these links applied to a complex caterpillar-parasitoid food web from tropical rainforest of Papua New Guinea. We DNA barcoded hosts, parasitoids and their tissue remnants and matched the sequences to our extensive library of local species. We were thus able to match 87% of host sequences and 36% of parasitoid sequences to species and infer subfamily or family in almost all cases. Our analysis affirmed 93 hitherto unknown trophic links between 37 host species from a wide range of Lepidoptera families and 46 parasitoid species from Hymenoptera and Diptera by identifying DNA sequences for both the host and the parasitoid involved in the interaction. Molecular detection proved especially useful in cases where distinguishing host species in caterpillar stage was difficult morphologically, or when the caterpillar died during rearing. We have even detected a case of extreme parasitoid specialization in a pair of Choreutis species that do not differ in caterpillar morphology and ecology. Using the molecular approach outlined here leads to better understanding of parasitoid host specificity, opens new possibilities for rapid surveys of food web structure and allows inference of species associations not already anticipated.
- MeSH
- Diptera genetika MeSH
- DNA primery genetika MeSH
- druhová specificita MeSH
- fylogeneze MeSH
- Hymenoptera genetika MeSH
- interakce hostitele a parazita genetika MeSH
- larva parazitologie MeSH
- Lepidoptera genetika parazitologie MeSH
- molekulární sekvence - údaje MeSH
- potravní řetězec MeSH
- sekvence nukleotidů MeSH
- sekvenční analýza DNA MeSH
- shluková analýza MeSH
- taxonomické DNA čárové kódování MeSH
- tropické klima MeSH
- výpočetní biologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Geografické názvy
- Papua Nová Guinea MeSH
