Evolutionary interactions between parasitoid wasps and insect hosts have been well studied at the organismal level, but little is known about the molecular mechanisms that insects use to resist wasp ...parasitism. Here we study the interaction between a braconid wasp (Aphidius ervi) and its pea aphid host (Acyrthosiphon pisum). We first identify variation in resistance to wasp parasitism that can be attributed to aphid genotype. We then use transcriptome sequencing to identify genes in the aphid genome that are differentially expressed at an early stage of parasitism, and we compare these patterns in highly resistant and susceptible aphid host lines. We find that resistant genotypes are upregulating genes involved in carbohydrate metabolism and several key innate immune system genes in response to parasitism, but that this response seems to be weaker in susceptible aphid genotypes. Together, our results provide a first look into the complex molecular mechanisms that underlie aphid resistance to wasp parasitism and contribute to a broader understanding of how resistance mechanisms evolve in natural populations.
Insect symbionts in food webs McLean, Ailsa H. C.; Parker, Benjamin J.; Hrček, Jan ...
Philosophical transactions - Royal Society. Biological sciences,
09/2016, Letnik:
371, Številka:
1702
Journal Article
Recenzirano
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Recent research has shown that the bacterial endosymbionts of insects are abundant and diverse, and that they have numerous different effects on their hosts' biology. Here we explore how insect ...endosymbionts might affect the structure and dynamics of insect communities. Using the obligate and facultative symbionts of aphids as an example, we find that there are multiple ways that symbiont presence might affect food web structure. Many symbionts are now known to help their hosts escape or resist natural enemy attack, and others can allow their hosts to withstand abiotic stress or affect host plant use. In addition to the direct effect of symbionts on aphid phenotypes there may be indirect effects mediated through trophic and non-trophic community interactions. We believe that by using data from barcoding studies to identify bacterial symbionts, this extra, microbial dimension to insect food webs can be better elucidated.
This article is part of the themed issue ‘From DNA barcodes to biomes’.
Many insects harbour facultative symbiotic bacteria, some of which have been shown to provide resistance against natural enemies. One of the best-known protective symbionts is Hamiltonella defensa, ...which in pea aphid (Acyrthosiphon pisum) confers resistance against attack by parasitoid wasps in the genus Aphidius (Braconidae). We asked (i) whether this symbiont also confers protection against a phylogenetically distant group of parasitoids (Aphelinidae) and (ii) whether there are consistent differences in the effects of bacteria found in pea aphid biotypes adapted to different host plants. We found that some H. defensa strains do provide protection against an aphelinid parasitoid Aphelinus abdominalis. Hamiltonella defensa from the Lotus biotype provided high resistance to A. abdominalis and moderate to low resistance to Aphidius ervi, while the reverse was seen from Medicago biotype isolates. Aphids from Ononis showed no evidence of symbiont-mediated protection against either wasp species and were relatively vulnerable to both. Our results may reflect the different selection pressures exerted by the parasitoid community on aphids feeding on different host plants, and could help explain the maintenance of genetic diversity in bacterial symbionts.
1. 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. 2. 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. 3. 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. 4. 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. 5. 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.
Summary
Animals are host to a community of microbes, collectively referred to as their microbiome, that can play a key role in their hosts' biology. The bacterial endosymbionts of insects have a ...particularly strong influence on their hosts, but despite their importance we still know little about the factors that influence the composition of insect microbial communities. Here, we ask: what is the relative importance of host relatedness and host ecology in structuring symbiont communities of diverse aphid species? We used next‐generation sequencing to compare the microbiomes of 46 aphid species with known host plant affiliations. We find that relatedness between aphid species is the key factor explaining the microbiome composition, with more closely related aphid species housing more similar bacterial communities. Endosymbionts dominate the microbial communities, and we find a novel bacterium in the genus Sphingopyxis that is associated with numerous aphid species feeding exclusively on trees. The influence of ecology was less pronounced than that of host relatedness. Our results suggest that co‐adaptation between insect species and their facultative symbionts is a more important determinant of symbiont species presence in aphids than shared ecology of hosts.
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.
Many insects host vertically transmitted microbes, which can confer benefits to their hosts but are costly to maintain and regulate. A key feature of these symbioses is variation: for example, ...symbiont density can vary among host and symbiont genotypes. However, the evolutionary forces maintaining this variation remain unclear. We studied variation in symbiont density using the pea aphid (Acyrthosiphon pisum) and the bacterium Regiella insecticola, a symbiont that can protect its host against fungal pathogens. We found that relative symbiont density varies both between two Regiella phylogenetic clades and among aphid “biotypes.” Higher density symbiont infections are correlated with stronger survival costs, but variation in density has little effect on the protection Regiella provides against fungi. Instead, we found that in some aphid genotypes, a dramatic decline in symbiont density precedes the loss of a symbiont infection. Together, our data suggest that the optimal density of a symbiont infection is likely different from the perspective of aphid and microbial fitness. Regiella might prevent loss by maintaining high within‐host densities, but hosts do not appear to benefit from higher symbiont numbers and may be advantaged by losing costly symbionts in certain environments. The standing variation in symbiont density observed in natural populations could therefore be maintained by antagonistic coevolutionary interactions between hosts and their symbiotic microbes.
Summary
Symbiotic bacteria can act to protect their host against natural enemies. Where this protection is asymmetric against different natural enemies, protection conferred by symbionts has the ...potential to mediate interactions between natural enemies, as well as between enemies and the host.
In pea aphids (Acyrthosiphon pisum), resistance against parasitoid wasps can be conferred by facultative symbiotic bacteria. We investigated whether the outcome of competition between two parasitoid species can be influenced by the presence of a defensive symbiont in the host.
We exposed pea aphids from a single clonal line, with and without a strain of the protective endosymbiont Hamiltonella defensa, to multiparasitism by the parasitoid wasps Aphelinus abdominalis (Aphelinidae) and Aphidius ervi (Braconidae), and recorded the outcome. The symbiont strain is known to impact A. abdominalis more strongly than A. ervi.
We found that the presence of a strain of the protective endosymbiont H. defensa can reverse the outcome of competition between the wasps. In the absence of the symbiont, A. ervi gains very little success when attacking an aphid previously parasitized by A. abdominalis. However, where the aphids possessed the symbiont, A. abdominalis did not develop successfully, and the success rate of A. ervi was significantly increased.
Our results show that defensive facultative symbionts are able to influence community interactions at the trophic level above their host.
A lay summary is available for this article.
Lay Summary
Microbial symbionts commonly protect their hosts from natural enemies, but it is unclear how protective symbionts influence the evolution of host immunity to pathogens. One possibility is that ...‘extrinsic’ protection provided by symbionts allows hosts to reduce investment in ‘intrinsic’ immunological resistance mechanisms. We tested this idea using pea aphids (Acyrthosiphon pisum) and their facultative bacterial symbionts that increase host resistance to the fungal pathogen Pandora neoaphidis. The pea aphid taxon is composed of multiple host plant associated populations called biotypes, which harbor characteristic communities of symbionts. We found that biotypes that more frequently carry protective symbionts have higher, rather than lower, levels of intrinsic resistance. Within a biotype there was no difference in intrinsic resistance between clones that did and did not carry a protective symbiont. The host plant on which an aphid feeds did not strongly influence intrinsic resistance. We describe a simple conceptual model of the interaction between intrinsic and extrinsic resistance and suggest that our results may be explained by selection favoring both the acquisition of protective symbionts and enhanced intrinsic resistance in habitats with high pathogen pressure. Such combined protection is potentially more robust than intrinsic resistance alone.
An experiment was conducted to test whether parasitoid resistance within a single clonal line of pea aphid (Acyrthosiphon pisum) might increase after exposure to the parasitoid wasp Aphidius ervi. ...Any change in resistance was expected to occur through an increase in the density of protective symbiotic bacteria rather than genetic change within the aphid or the bacterial symbiont. Six aphid lineages were exposed to high parasitoid attack rates over nine generations, each line being propagated from individuals that had survived attack; a further six lineages were maintained without parasitoids as a control. At the end of the experiment the strength of resistance of aphids from treatment and control lines were compared. No differences in resistance were found.
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