Host relatedness influences the composition of aphid microbiomes.

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

Facultative Symbiont Infections Affect Aphid Reproduction

Some bacterial symbionts alter their hosts reproduction through various mechanisms that enhance their transmission in the host population. In addition to its obligatory symbiont Buchnera aphidicola, the pea aphid Acyrthosiphon pisum harbors several facultative symbionts influencing several aspects of host ecology. Aphids reproduce by cyclical parthenogenesis whereby clonal and sexual reproduction alternate within the annual life cycle. Many species, including the pea aphid, also show variation in their reproductive mode at the population level, with some lineages reproducing by cyclical parthenogenesis and others by permanent parthenogenesis. While the role of facultative symbionts has been well studied during the parthenogenetic phase of their aphid hosts, very little is known on their possible influence during the sexual phase. Here we investigated whether facultative symbionts modulate the capacity to produce sexual forms in various genetic backgrounds of the pea aphid with controlled symbiont composition and also in different aphid genotypes from natural populations with previously characterized infection status and reproductive mode. We found that most facultative symbionts exhibited detrimental effects on their hosts fitness under sex-inducing conditions in comparison with the reference lines. We also showed that the loss of sexual phase in permanently parthenogenetic lineages of A. pisum was not explained by facultative symbionts. Finally, we demonstrated that Spiroplasma infection annihilated the production of males in the host progeny by inducing a male-killing phenotype, an unexpected result for organisms such as aphids that reproduce primarily through clonal reproduction

Cascading effects of defensive endosymbionts

Defensive endosymbionts are now understood to be widespread among insects, targeting many different threats, including predators, parasites and disease. The effects on natural enemies can be significant, resulting in dramatic changes in the outcome of interactions between insects and their attackers. Evidence is now emerging from laboratory and field work that defensive symbionts can have important effects on the surrounding insect community, as well as on vulnerable enemy species; for example, by reducing prey available for the trophic level above the enemy. However, there is a need for more experimental work across a greater taxonomic range of species in order to understand the different ways in which defensive symbionts influence insect communities

Effects of the maternal and pre-adult host plant on adult performance and preference in the pea aphid, Acyrthosiphon pisum

1. The taxon known as the pea aphid, Acyrthosiphon pisum, is composed of a series of host plant associated populations and is widely used as a model system to explore ecological speciation and the evolution of specialisation. It is thus important to know how maternal and pre-adult experience influences host plant utilisation in this species. 2. The relative importance of the maternal and pre-adult host plant for adult fecundity and host preference was investigated using three aphid clones collected from Lathyrus pratensis and maintained on Lathyrus or Vicia faba. 3. No significant effects of the maternal host plant on offspring fecundity were detected. 4. The host plant on which the aphid grew up influenced adult fecundity, although in a complex way that depended on both the adult host plant species and when after transfer to the test plant fecundity was assessed. 5. All three clones preferred to colonise Lathyrus over Vicia, and this preference was stronger for aphids raised on Lathyrus. 6. The significance of the results for studies of the evolution of specialisation and speciation that employ A. pisum is discussed. © 2009 The Royal Entomological Society

Symbionts modify interactions between insects and natural enemies in the field

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.</p

Symbionts modify interactions between insects and natural enemies in the the field

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.</p

Symbionts modify interactions between insects and natural enemies in the field

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.</p

Establishment and maintenance of aphid endosymbionts after horizontal transfer is dependent on host genotype

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