The natural occurrence of secondary bacterial symbionts in aphids

1. Many insects host secondary bacterial symbionts that are known to have wide‐ranging effects on their hosts, from host‐plant use to resistance against natural enemies. This has been most widely studied in aphids, which have become a model system to study insect–bacteria interactions. 2. While there is an increasing understanding of the role of symbionts in aphids from controlled laboratory studies, we are only beginning to explore the impact of hosting these symbionts on eco‐evolutionary dynamics in natural systems. To date, many research groups have identified bacterial symbionts from various aphid species, providing us with a bank of literature on aphid–symbiont associations in natural populations. 3. The role of secondary symbionts in aphids is discussed, and the taxonomic and geographical distribution of symbionts among aphids are summarised, and the potential reasons for the patterns observed. The need to test for multiple symbiont species (and co‐infections) across many individuals and the whole distribution range of an aphid is highlighted, including sampling on all known host‐plant species. 4. It is further important also to consider variation within the symbiont, the aphid‐host and the surrounding community, e.g. host‐plants or the natural enemies, to understand how these have the potential to mediate aphid–symbiont interactions. 5. Finally, the knowledge gained from experimental work should now be used to understand the role of aphid secondary symbionts in field systems, to fully understand the potentially far‐reaching consequences of aphid endosymbionts on community and ecosystem processes.     

Effects of bacterial secondary symbionts on host plant use in pea aphids

Aphids possess several facultative bacterial symbionts that have important effects on their hosts'' biology. These have been most closely studied in the pea aphid (Acyrthosiphon pisum), a species that feeds on multiple host plants. Whether secondary symbionts influence host plant utilization is unclear. We report the fitness consequences of introducing different strains of the symbiont Hamiltonella defensa into three aphid clones collected on Lathyrus pratensis that naturally lack symbionts, and of removing symbionts from 20 natural aphid–bacterial associations. Infection decreased fitness on Lathyrus but not on Vicia faba, a plant on which most pea aphids readily feed. This may explain the unusually low prevalence of symbionts in aphids collected on Lathyrus. There was no effect of presence of symbiont on performance of the aphids on the host plants of the clones from which the H. defensa strains were isolated. Removing the symbiont from natural aphid–bacterial associations led to an average approximate 20 per cent reduction in fecundity, both on the natural host plant and on V. faba, suggesting general rather than plant-species-specific effects of the symbiont. Throughout, we find significant genetic variation among aphid clones. The results provide no evidence that secondary symbionts have a major direct role in facilitating aphid utilization of particular host plant species.     

Microbiota associated with Mollitrichosiphum aphids (Hemiptera: Aphididae: Greenideinae): diversity,host species specificity and phylosymbiosis

Symbiotic association is universal in nature, and an array of symbionts play a crucial part in host life history. Aphids and their diverse symbionts have become a good model system to study insect-symbiont interactions. Previous symbiotic diversity surveys have mainly focused on a few aphid clades, and the relative importance of different factors regulating microbial community structure is not well understood. In this study, we collected 65 colonies representing eight species of the aphid genus Mollitrichosiphum from different regions and plants in southern China and Nepal and characterized their microbial compositions using Illumina sequencing of the V3 − V4 hypervariable region of the 16S rRNA gene. We evaluated how microbiota varied across aphid species, geography and host plants and the correlation between microbial community structure and host aphid phylogeny. Heritable symbionts dominated the microbiota associated with Mollitrichosiphum, and multiple infections of secondary symbionts were prevalent. Ordination analyses and statistical tests highlighted the contribution of aphid species in shaping the structures of bacterial, symbiont and secondary symbiont communities. Moreover, we observed a significant correlation between Mollitrichosiphum aphid phylogeny and microbial community composition, providing evidence for a pattern of phylosymbiosis between natural aphid populations and their microbial associates.     

Cohabitation and roommate bias of symbiotic bacteria in insect hosts

Symbiotic interactions between insects and bacteria have long fascinated ecologists. Aphids have emerged as the model system on which to study the effect of endosymbiotic bacteria on their hosts. Aphid‐symbiont interactions are ecologically interesting as aphids host multiple secondary symbionts that can provide broad benefits, such as protection against heat stress or specialist natural enemies (parasitic wasps and entomopathogenic fungi). There are nine common aphid secondary symbionts and individual aphids host on average 1–2 symbionts. A cost‐benefit trade‐off for hosting symbionts is thought to explain why not all aphids host every possible symbiont in a population. Both positive and negative associations between various symbionts occur, and this could happen due to increased costs when cohosting certain combinations or as a consequence of competitive interactions between the symbionts within a host. In this issue of Molecular Ecology, Mathé‐Hubert, Kaech, Hertaeg, Jaenike, and Vorburger (2019) use data on the symbiont status of field‐collected aphids to inform a model on the evolution of symbiont co‐occurrence. They vary the effective female population size as well as the rate of horizontal and maternal transmission to infer the relative impact of symbiont‐symbiont interactions versus random drift. Additional data analysis revisits an association between two symbionts in a fruit fly species using a long‐term data set to highlight that such interactions are not limited to aphids.     

Examination of the success rate of secondary symbiont manipulation by microinjection methods in the pea aphid system

Insects harbor a wide range of microbial symbionts, but their influence on host phenotypes is described in a limited number of biological models. One experimental approach to gain knowledge on the effects of symbionts to their hosts is to create insect lines with and without symbionts and examine their phenotypes. However, the success rate of symbiont elimination and introduction methods is dependent on several parameters that are scarcely tested or described. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), is a model insect of symbiosis studies. It harbors a primary symbiont that supplies the host with essential amino acids, and an array of secondary symbionts whose effects have been assessed by manipulating their presence/absence in the insect. Here, we describe the influence of key parameters on the success rate of symbiont manipulation using the pea aphid–secondary symbiont system. We compared two elimination methods differing in antibiotic treatment using several aphid–symbiont combinations. We also created new aphid host–symbiont combinations by secondary symbiont introduction and examined the effects of larval stage of recipient aphids on introduction success. Our study revealed that the aphid–symbiont combination has strong influence on both symbiont introduction and elimination success rates, and that the type of antibiotics and the larval stage of recipient aphids influence the elimination and introduction success rate, respectively.     

Bacterial Communities Associated with Host-Adapted Populations of Pea Aphids Revealed by Deep Sequencing of 16S Ribosomal DNA

Associations between microbes and animals are ubiquitous and hosts may benefit from harbouring microbial communities through improved resource exploitation or resistance to environmental stress. The pea aphid, Acyrthosiphon pisum, is the host of heritable bacterial symbionts, including the obligate endosymbiont Buchnera aphidicola and several facultative symbionts. While obligate symbionts supply aphids with key nutrients, facultative symbionts influence their hosts in many ways such as protection against natural enemies, heat tolerance, color change and reproduction alteration. The pea aphid also encompasses multiple plant-specialized biotypes, each adapted to one or a few legume species. Facultative symbiont communities differ strongly between biotypes, although bacterial involvement in plant specialization is uncertain. Here, we analyse the diversity of bacterial communities associated with nine biotypes of the pea aphid complex using amplicon pyrosequencing of 16S rRNA genes. Combined clustering and phylogenetic analyses of 16S sequences allowed identifying 21 bacterial OTUs (Operational Taxonomic Unit). More than 98% of the sequencing reads were assigned to known pea aphid symbionts. The presence of Wolbachia was confirmed in A. pisum while Erwinia and Pantoea, two gut associates, were detected in multiple samples. The diversity of bacterial communities harboured by pea aphid biotypes was very low, ranging from 3 to 11 OTUs across samples. Bacterial communities differed more between than within biotypes but this difference did not correlate with the genetic divergence between biotypes. Altogether, these results confirm that the aphid microbiota is dominated by a few heritable symbionts and that plant specialization is an important structuring factor of bacterial communities associated with the pea aphid complex. However, since we examined the microbiota of aphid samples kept a few generations in controlled conditions, it may be that bacterial diversity was underestimated due to the possible loss of environmental or transient taxa.     

刺吸式昆虫次生内共生菌的研究进展

蚜虫作为典型的刺吸式昆虫,需要以取食植物韧皮部汁液来补充营养,几乎所有蚜虫均带有一种能为其提供植物韧皮部缺失营养物质的初生共生菌Buchnera aphidicola。此外,蚜虫还可携带一种或多种次生内共生菌。在众多共生菌—寄主系统中,蚜虫与其所带内共生菌间的互作研究最为透彻。虽然次生内共生菌对寄主的存活和生殖影响并不显著,但其在寄主对环境耐受力、天敌防御能力等方面作用明显。本文在查阅大量蚜虫次生内共生菌相关文献的基础上,着重对蚜虫次生内共生菌的种类及传播规律、次生内共生菌对蚜虫表型的影响、蚜虫次生内共生菌基因组学等方面的研究现状进行综述,以求为刺吸式昆虫次生内共生菌的研究提供参考。     

Diversity of the Most Commonly Reported Facultative Symbionts in Two Closely-Related Aphids with Different Host Ranges

Richness and abundance of facultative symbionts vary strongly with aphid species and genotype, symbiont strain, host plant, biogeography, and a number of abiotic factors. Despite indications that aphids in the same ecological niche show similar levels of facultative symbiont richness, existing reports do not consider the potential role of host plants on aphid microbial community. Little is known about how oligophagy and polyphagy may be influenced by secondary symbiont distribution, mainly because studies on secondary symbiont diversity are biased towards polyphagous aphids from the Northern Hemisphere. Here, we demonstrate the richness and abundance of the most common aphid-associated facultative symbionts in two tropical aphid species, the oligophagous Aphis (Toxoptera) citricidus (Kirkaldy) (Hemiptera: Aphididae) and the polyphagous Aphis aurantii (Boyer de Fonscolombe) (Hemiptera: Aphididae). Aphis citricidus is restricted to Citrus sp. host plants and closely related genera, whereas A. aurantii successfully exploits a wide variety of host plants from different families. Both were collected in the same ecological niche and our data basically indicated the same richness of secondary symbionts, but the abundance at which secondary symbionts occurred was very distinct between the two species. Spiroplasma was the most abundant facultative symbiont associated with A. citricidus and A. aurantii in the ecological niche studied. Single and multiple secondary symbiont infections were observed, but diversity of multiple infections was particularly high in A. citricidus. We discuss our findings and suggest hypotheses to explain causes and consequences of the differences in secondary symbiont diversity observed between these two aphid species.     

An ecological cost associated with protective symbionts of aphids

Beneficial symbioses are widespread and diverse in the functions they provide to the host ranging from nutrition to protection. However, these partnerships with symbionts can be costly for the host. Such costs, so called “direct costs”, arise from a trade‐off between allocating resources to symbiosis and other functions such as reproduction or growth. Ecological costs may also exist when symbiosis negatively affects the interactions between the host and other organisms in the environment. Although ecological costs can deeply impact the evolution of symbiosis, they have received little attention. The pea aphid Acyrthosiphon pisum benefits a strong protection against its main parasitoids from protective bacterial symbionts. The ecological cost of symbiont‐mediated resistance to parasitism in aphids was here investigated by analyzing aphid behavior in the presence of predatory ladybirds. We showed that aphids harboring protective symbionts expressed less defensive behaviors, thus suffering a higher predation than symbiont‐free aphids. Consequently, our study indicates that this underlined ecological cost may affect both the coevolutionary processes between symbiotic partners and the prevalence of such beneficial bacterial symbionts in host natural populations.     

Horizontal transfer of facultative endosymbionts is limited by host relatedness

Heritable microbial symbionts can have important effects on many aspects of their hosts’ biology. Acquisition of a novel symbiont strain can provide fitness benefits to the host, with significant ecological and evolutionary consequences. We measured barriers to horizontal transmission by artificially transferring facultative symbionts from the grain aphid, Sitobion avenae, and five other aphid species into two clonal genotypes of S. avenae. We found the symbiont Hamiltonella defensa establishes infections more easily following a transfer from the same host species and that such infections are more stable. Infection success was also higher when the introduced symbiont strain was more closely related to the strain that was originally present in the host (but which had previously been removed). There were no differences among successfully established symbiont strains in their effect on aphid fecundity. Hamiltonella defensa did not confer protection against parasitoids in our S. avenae clones, although it often does in other aphid hosts. However, strains of the symbiont Regiella insecticola originating from two host species protected grain aphids against the pathogenic fungus Pandora neoaphidis. This study helps describe the extent to which facultative symbionts can act as a pool of adaptations that can be sampled by their eukaryote hosts.     

Stress‐induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid

Bacterial endosymbionts can drive evolutionary novelty by conferring adaptive benefits under adverse environmental conditions. Among aphid species there is growing evidence that symbionts influence tolerance to various forms of stress. However, the extent to which stress inflicted on the aphid host has cascading effects on symbiont community dynamics remains poorly understood. Here we simultaneously quantified the effect of host‐plant induced and xenobiotic stress on soybean aphid (Aphis glycines) fitness and relative abundance of its three bacterial symbionts. Exposure to soybean defensive stress (Rag1 gene) and a neurotoxic insecticide (thiamethoxam) substantially reduced aphid composite fitness (survival × reproduction) by 74 ± 10% and 92 ± 2%, respectively, which in turn induced distinctive changes in the endosymbiont microbiota. When challenged by host‐plant defenses a 1.4‐fold reduction in abundance of the obligate symbiont Buchnera was observed across four aphid clonal lines. Among facultative symbionts of Rag1‐stressed aphids, Wolbachia abundance increased twofold and Arsenophonus decreased 1.5‐fold. A similar pattern was observed under xenobiotic stress, with Buchnera and Arsenophonus titers decreasing (1.3‐fold) and Wolbachia increasing (1.5‐fold). Furthermore, variation in aphid virulence to Rag1 was positively correlated with changes in Arsenophonus titers, but not Wolbachia or Buchnera. A single Arsenophonus multi‐locus genotype was found among aphid clonal lines, indicating strain diversity is not primarily responsible for correlated host‐symbiont stress levels. Overall, our results demonstrate the nature of aphid symbioses can significantly affect the outcome of interactions under stress and suggests general changes in the microbiome can occur across multiple stress types.     

Diversity and geographic variation of endosymbiotic bacteria in natural populations of the pea aphid (Acyrthosiphon pisum) in China

Bacterial symbionts in aphids are known to benefit the insect host and associated with aphid’s ecological adaptation. The pea aphid (Acyrthosiphon pisum), an important legume pest worldwide, carries at least eight endosymbionts, providing a model system to study insect–bacteria interactions. However, species diversity and geographic variations of endosymbionts are unknown in Chinese populations; therefore, we characterized symbiont communities and diversity of 27 pea aphid samples from 13 geographic populations of China. Via amplicon high-throughput sequencing and diagnostic PCR, we found that bacterial communities of Chinese populations were dominated by Proteobacteria and Firmicutes. Among eight known endosymbionts, five (Buchnera, Serratia, Hamiltonella, Regiella, and Rickettsia) were detected by both methods, with a specific geographical distribution. The obligate symbiont, Buchnera, was present in all aphid samples, while the four facultative symbionts showed a significant geographic variation. Each population was randomly infected with distinct endosymbionts, ranging from three to five species. Serratia and Rickettsia showed relatively higher abundance in central regions of China, Regiella was predominant in eastern and western China, whereas Hamiltonella showed an extremely low abundance and was absent in four populations. Samples grouped by altitudes showed a significant diversity difference, whereas there was no significant difference between red and green body colors. Bacterial community structures of the Chinese pea aphid populations were mainly influenced by environmental factors, other than body colors. These data can guide the development of potential biocontrol techniques against this aphid.     

Molecular phylogeny and divergence times of Hormaphidinae (Hemiptera: Aphididae) indicate Late Cretaceous tribal diversification

The aphid subfamily Hormaphidinae is a good candidate for the study of the evolution of insect – plant relationships. Most hormaphidine species depend on woody primary host plants and woody or herbaceous secondary host plants, and represent high host specificity, especially to their primary hosts. No detailed molecular phylogeny of Hormaphidinae has been reported, and the taxonomic positions of some taxa in this group remain unclear. To reconstruct major phylogenetic relationships and to understand the evolution of host association patterns for major lineages, we present the first detailed molecular phylogeny of Hormaphidinae, as inferred from nuclear and mitochondrial DNA sequences, using maximum parsimony, maximum likelihood, and Bayesian methods. The monophyly of Hormaphidinae and its three traditional tribes was supported, and a sister relationship between Hormaphidini and Nipponaphidini was suggested. Most inner relationships within tribes were also supported, and some novel relationships were revealed. Two subtribes of Cerataphidini are proposed. Divergence times estimated using a Bayesian approach indicate that tribal diversifications occurred during the Late Cretaceous and were coincident with the appearance of their primary host plants. The current pattern of secondary host association for the three tribes may have evolved in different time ranges. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 165 , 73–87.     

Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study

In order to reduce parasite‐induced mortality, hosts may be involved in mutualistic interactions in which the partner contributes to resistance against the parasite. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), harbours secondary bacterial endosymbionts, some of which have been reported to confer resistance against aphid parasitoids. Although this resistance often results in death of the developing parasitoid larvae, some parasitoid individuals succeed in developing into adults. Whether these individuals suffer from fitness reduction compared to parasitoids developing in pea aphid clones without symbionts has not been tested so far. Using 30 pea aphid clones that differed in their endosymbiont complement, we studied the effects of these endosymbionts on aphid resistance against the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae), host–parasitoid physiological interactions, and fitness of emerging adult parasitoids. The number of symbiont species in an aphid clone was positively correlated with a number of resistance measurements but there were also clear symbiont‐specific effects on the host–parasitoid interaction. As in previous studies, pea aphid clones infected with Hamiltonella defensa Moran et al. showed resistance against the parasitoid. In addition, pea aphid clones infected with Regiella insecticola Moran et al. and co‐infections of H. defensa–Spiroplasma, R. insecticola–Spiroplasma, and R. insecticola–H. defensa showed reduced levels of parasitism and mummification. Parasitoids emerging from symbiont‐infected aphid clones often had a longer developmental time and reduced mass. The number of teratocytes was generally lower when parasitoids oviposited in aphid clones with a symbiont complement. Interestingly, unparasitized aphids infected with Serratia symbiotica Moran et al. and R. insecticola had a higher fecundity than unparasitized aphids of uninfected pea aphid clones. We conclude that in addition to conferring resistance, pea aphid symbionts also negatively affect parasitoids that successfully hatch from aphid mummies. Because of the link between aphid resistance and the number of teratocytes, the mechanism underlying resistance by symbiont infection may involve interference with teratocyte development.     

The Combined Effects of Bacterial Symbionts and Aging on Life History Traits in the Pea Aphid,Acyrthosiphon pisum

While many endosymbionts have beneficial effects on hosts under specific ecological conditions, there can also be associated costs. In order to maximize their own fitness, hosts must facilitate symbiont persistence while preventing symbiont exploitation of resources, which may require tight regulation of symbiont populations. As a host ages, the ability to invest in such mechanisms may lessen or be traded off with demands of other life history traits, such as survival and reproduction. Using the pea aphid, Acyrthosiphon pisum, we measured survival, lifetime fecundity, and immune cell counts (hemocytes, a measure of immune capacity) in the presence of facultative secondary symbionts. Additionally, we quantified the densities of the obligate primary bacterial symbiont, Buchnera aphidicola, and secondary symbionts across the host''s lifetime. We found life history costs to harboring some secondary symbiont species. Secondary symbiont populations were found to increase with host age, while Buchnera populations exhibited a more complicated pattern. Immune cell counts peaked at the midreproductive stage before declining in the oldest aphids. The combined effects of immunosenescence and symbiont population growth may have important consequences for symbiont transmission and maintenance within a host population.     

The microbial flora of Aphis gossypii: Patterns across host plants and geographical space

The cotton aphid, Aphis gossypii, has a worldwide distribution and causes damage to numerous economically important crops. The bacterial symbionts associated with cotton aphids, sampled mainly from malvaceous and cucurbitaceous plants within Japan and Australia, were characterised using molecular profiling approaches. The goal was to document the aphid symbionts present and determine if patterns of microbial diversity are consistent with the existence of host plant related cryptic species in A. gossypii. The bacterial profiles of the aphids are diverse and reflect local geography more than host plant use.     

Intraspecific variation in immune gene expression and heritable symbiont density

Host genetic variation plays an important role in the structure and function of heritable microbial communities. Recent studies have shown that insects use immune mechanisms to regulate heritable symbionts. Here we test the hypothesis that variation in symbiont density among hosts is linked to intraspecific differences in the immune response to harboring symbionts. We show that pea aphids (Acyrthosiphon pisum) harboring the bacterial endosymbiont Regiella insecticola (but not all other species of symbionts) downregulate expression of key immune genes. We then functionally link immune expression with symbiont density using RNAi. The pea aphid species complex is comprised of multiple reproductively-isolated host plant-adapted populations. These ‘biotypes’ have distinct patterns of symbiont infections: for example, aphids from the Trifolium biotype are strongly associated with Regiella. Using RNAseq, we compare patterns of gene expression in response to Regiella in aphid genotypes from multiple biotypes, and we show that Trifolium aphids experience no downregulation of immune gene expression while hosting Regiella and harbor symbionts at lower densities. Using F1 hybrids between two biotypes, we find that symbiont density and immune gene expression are both intermediate in hybrids. We propose that in this system, Regiella symbionts are suppressing aphid immune mechanisms to increase their density, but that some hosts have adapted to prevent immune suppression in order to control symbiont numbers. This work therefore suggests that antagonistic coevolution can play a role in host-microbe interactions even when symbionts are transmitted vertically and provide a clear benefit to their hosts. The specific immune mechanisms that we find are downregulated in the presence of Regiella have been previously shown to combat pathogens in aphids, and thus this work also highlights the immune system’s complex dual role in interacting with both beneficial and harmful microbes.     

Happens in the best of subfamilies: establishment and repeated replacements of co‐obligate secondary endosymbionts within Lachninae aphids

Virtually all aphids maintain an obligate mutualistic symbiosis with bacteria from the Buchnera genus, which produce essential nutrients for their aphid hosts. Most aphids from the Lachninae subfamily have been consistently found to house additional endosymbionts, mainly Serratia symbiotica. This apparent dependence on secondary endosymbionts was proposed to have been triggered by the loss of the riboflavin biosynthetic capability by Buchnera in the Lachninae last common ancestor. However, an integral large‐scale analysis of secondary endosymbionts in the Lachninae is still missing, hampering the interpretation of the evolutionary and genomic analyses of these endosymbionts. Here, we analysed the endosymbionts of selected representatives from seven different Lachninae genera and nineteen species, spanning four tribes, both by FISH (exploring the symbionts’ morphology and tissue tropism) and 16S rRNA gene sequencing. We demonstrate that all analysed aphids possess dual symbiotic systems, and while most harbour S. symbiotica, some have undergone symbiont replacement by other phylogenetically‐distinct bacterial taxa. We found that these secondary associates display contrasting cell shapes and tissue tropism, and some appear to be lineage‐specific. We propose a scenario for symbiont establishment in the Lachninae, followed by changes in the symbiont's tissue tropism and symbiont replacement events, thereby highlighting the extraordinary versatility of host‐symbiont interactions.     

Cowpea aphid (Aphis craccivora) associated with different host plants has different facultative endosymbionts

Maternally inherited facultative endosymbiotic bacteria are common among insects, including many polyphagous insect herbivores. To investigate whether symbiont infection is structured by host plant in the polyphagous aphid Aphis craccivora Koch, pyrosequencing and diagnostic PCR were performed on 26 populations from two different host plants, alfalfa (Medicago sativa) or black locust (Robinia pseudoacacia). Results indicated that Aphis craccivora harbours distinctly different microbial communities in alfalfa versus locust. The facultative symbiont Hamiltonella was found only in aphids collected from alfalfa, and the facultative symbiont Arsenophonus was found only in aphids from locust. Hamiltonella is known to protect aphids against hymenopteran parasitoids, whereas the phenotypic effects of Arsenophonus in aphids are unknown. Correspondingly, a screen of the aphid samples for hymenopteran DNA indicated that Hamiltonella‐bearing alfalfa populations of A. craccivora experienced lower parasitism than Arsenophonus‐bearing locust populations. This study contributes to the growing body of evidence that correlative associations between bacterial endosymbionts and host plants may be a common phenomenon in polyphagous herbivores, and suggests that microbial symbionts have the potential to act as drivers for observed ecological differences among host‐associated populations of polyphagous insects.     

Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids

Ecological specialisation on different host plants occurs frequently among phytophagous insects and is normally assumed to have a genetic basis. However, insects often carry microbial symbionts, which may play a role in the evolution of specialisation. The bacterium Regiella insecticola is a facultative symbiont of pea aphids (Acyrthosiphon pisum) where it is found most frequently in aphid clones feeding on Trifolium giving rise to the hypothesis that it may improve aphid performance on this plant. A study in which R. insecticola was eliminated from a single naturally infected aphid clone supported the hypothesis, but a second involving two aphid clones did not find the same effect. We created a series of new pea aphid–R. insecticola associations by injecting different strains of bacteria into five aphid clones uninfected by symbionts. For all aphid clones, the bacteria decreased the rate at which aphids accepted Vicia faba as a food plant and reduced performance on this plant. Their effect on aphids given Trifolium pratense was more complex: R. insecticola negatively affected acceptance by all aphid clones, had no effect on the performance of four aphid clones, but increased performance of a fifth, thus demonstrating genetic variation in the effect of R. insecticola on pea aphid host use. We discuss how these results may explain the distribution and frequency of this symbiont across different aphid populations. Julia Ferrari and Claire L. Scarborough contributed equally to the work.