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Endogenous viral elements (EVEs) are widespread across animal genomes, yet the processes governing EVE evolution and diversification remain poorly understood. Here, we characterize the evolution of densoviral EVEs and exogenous densoviruses across the aphid tribe Macrosiphini, an agriculturally important group in which exogenous densoviruses and their endogenous derivatives have been linked to the plastic production of wings. Using new genome assemblies, transcriptomics, and phylogenetic analysis, we find that EVE content varies extensively across species. Moreover, we discovered a novel densovirus that is vertically transmitted, but phylogenetic incongruence between other densoviruses and their hosts suggests that horizontal transmission may also occur. Finally, we show that EVE-mediated regulation of wing plasticity extends across species that use different environmental signals to induce winged offspring. Our study shows that in this system, the evolution of EVEs is highly variable and lineage-specific, generating genomic patterns that cannot be predicted from host evolutionary relationships. 

ABSTRACT Heritable microbes shape host phenotypes and serve as important drivers of evolution. While interactions between insects and bacterial symbionts have been extensively studied, the prevalence and evolution of insect-viral symbioses remain poorly understood. We discovered multiple new species of iflaviruses in aphids, an important model for research on symbiosis, and found these microbes to be widespread across aphid species. We show that iflaviruses are persistently maintained in asexual host lines without apparent fitness costs while being transmitted vertically from mothers to offspring. Using field data and phylogenetic evidence, we found that aphid iflaviruses move horizontally among host species, but laboratory experiments showed that horizontal transmission does not result in persistent infections. Using quantitative PCR and immunohistochemistry, we discovered that viral infections localize in the host fat bodies and developing embryos. Surprisingly, we also found viral infections inside bacteria-housing cells called bacteriocytes, along with a positive correlation between viral and bacterial symbiont density. Together, our work suggests that iflaviruses are widespread heritable symbionts in aphids. IMPORTANCEIn recent years, the rise of metatranscriptome sequencing has led to the rapid discovery of novel viral sequences in insects. However, few studies have carefully investigated the dynamics of insect-virus interactions to produce a general understanding of viral symbiosis. Aphids are an important model for understanding the evolution and molecular basis of symbiosis, but whether viruses are forming persistent symbiotic relationships with aphids remains unclear. Here, we show that heritable iflaviruses are a widespread but previously unrecognized part of the aphid heritable microbiome. Aphid iflaviruses are transmitted alongside bacteria from mothers to offspring, potentially via specialized bacteriocytes that house symbiotic microbes. Our findings suggest that aphids establish persistent relationships with iflaviruses and are likely coevolving with these viral symbionts. 

Metatranscriptome sequencing has emerged as a powerful tool for uncovering viral diversity in insects and their associated microbes. To explore viruses linked to the pea aphid (Acyrthosiphon pisum), we performed metatranscriptome sequencing on field-collected samples. In addition to several known plant viruses, we assembled the genome of a new virus homologous to species in the familyMitoviridae, which are positive-sense single-stranded RNA viruses that encode only an RNA-dependent RNA polymerase and typically replicate in mitochondria. Given the frequent association of mitoviruses with fungi and the presence of entomopathogenic fungal reads in our dataset, we conducted 18S amplicon sequencing and PCR screening on individual aphids. These analyses identified two fungal entomopathogens and uncovered an association between the mitovirus andZoophthora radicans, a generalist aphid pathogen. Our findings shed light on the hidden microbial diversity in natural pea aphid populations and emphasize the utility of metatranscriptomics in identifying novel virus-host associations. 

Recent studies using metatranscriptome sequencing have revealed a diversity of viruses associated with insects. Researchers have used various approaches to establish patterns of transmission of insect-specific viruses and have shown that insects often harbor viruses that are inherited from parents to offspring. It remains unclear, however, whether heritable viral symbioses can be understood in the same ecological and evolutionary framework that has been established for bacterial symbiosis. We review studies showing beneficial and pathogenic effects of heritable viruses on their hosts, and we discuss additional ways that heritable viruses shape insect evolution. We also compare bacterial and viral symbiosis and review ways that this emerging field can be used for biocontrol of pests and insect-borne pathogens. Heritable viruses are a key part of the ecology and evolution of insects. A framework for studying symbiosis between insects and these microbes is important for a comprehensive understanding of insect biology. 

A<sc>bstract</sc> Heritable microbes shape host phenotypes and are important drivers of evolution. While interactions between insects and bacterial symbionts have been extensively studied, the prevalence and consequences of insect-viral symbiosis are an open question. We show that viral symbionts in the familyIflaviridaeare widespread among aphids, an important model for research on bacterial symbiosis. We discovered multiple new species of iflaviruses that are maintained in asexual lines without apparent fitness costs and are transmitted vertically from mothers to offspring. Using field data and phylogenetic evidence, we further show that aphid iflaviruses likely move horizontally across species, but through laboratory experiments, we demonstrated that horizontal transfer among species infesting the same host plants does not persist throughout clonal lineages. Using quantitative PCR and immunohistochemistry, we discovered that viral infections localize in the host fat bodies and developing embryos. Surprisingly, we also found viral infections inside bacteria-housing cells called bacteriocytes, with a positive correlation between viral and bacterial symbiont density, indicating a mechanism for vertical transmission. Together, our work suggests that iflaviruses are an important but previously unrecognized piece of aphid symbiosis and sets the stage to use this model to answer new questions about host-microbe associations. I<sc>mportance</sc>In recent years, the rise of metatranscriptome sequencing has led to the rapid discovery of novel viral sequences in insects. However, few studies have carefully investigated the dynamics of insect-virus interactions to produce a general understanding of viral symbiosis. Aphids are a significant agricultural pest but also an important model for understanding the evolution of host-microbe interactions and the molecular basis of bacterial symbiosis. We show that heritable iflaviruses are an important but previously unrecognized part of the aphid heritable microbiome, with viral symbionts transmitted alongside bacteria from mothers to offspring, potentially via specialized bacteriocytes that house symbiotic microbes. Our findings have important implications for furthering the understanding of insect-microbe symbiosis and the potential for biocontrol of agriculturally relevant pest species. 

Aulacorthum solani is a worldwide agricultural pest aphid capable of feeding on a wide range of host plants. This insect is a vector of plant viruses and causes injury to crops including stunted growth from the loss of phloem. We found that the publicly available genome for A. solani is contaminated with another aphid species, and we produced a new genome using a barcoded isogenic laboratory line. We generated Oxford Nanopore and Illumina reads to assemble a draft genome, and we sequenced RNA to aid in the annotation of our assembly. Our A. solani genome is 671 Mb containing 7,020 contigs with an N50 length of 196 kb with a BUSCO completeness of 98.6%. Out of the 24,981 genes predicted by EGAPx, 22,804 were annotated with putative functions based on homology to other aphid species. This genome will provide a useful resource for the community of researchers studying aphids from agricultural and genomic perspectives. 

Fireflies are iconic insects that are under threat from environmental change. Knowledge of the viral diversity associated with natural firefly populations is important to our understanding of the basic biology of these insects and could be relevant to firefly conservation. We performed metatranscriptome sequencing of the Common Eastern Firefly (Photinus pyralis) and assembled genomes for two new species of virus in the families Iflaviridae and Partitiviridae. We surveyed multiple individuals for these viruses using PCR, and we showed that both viruses are found at intermediate frequences in a natural population. 

Abstract Aphids are hosts to diverse viruses and are important vectors of plant pathogens. The spread of viruses is heavily influenced by aphid movement and behaviour. Consequently, wing plasticity (where individuals can be winged or wingless depending on environmental conditions) is an important factor in the spread of aphid‐associated viruses. We review several fascinating systems where aphid‐vectored plant viruses interact with aphid wing plasticity, both indirectly by manipulating plant physiology and directly through molecular interactions with plasticity pathways. We also cover recent examples where aphid‐specific viruses and endogenous viral elements within aphid genomes influence wing formation. We discuss why unrelated viruses with different transmission modes have convergently evolved to manipulate wing formation in aphids and whether this is advantageous for both host and virus. We argue that interactions with viruses are likely shaping the evolution of wing plasticity within and across aphid species, and we discuss the potential importance of these findings for aphid biocontrol. 

ABSTRACT Bacteria shape interactions between hosts and fungal pathogens. In some cases, bacteria associated with fungi are essential for pathogen virulence. In other systems, host-associated microbiomes confer resistance against fungal pathogens. We studied an aphid-specific entomopathogenic fungus calledPandora neoaphidisin the context of both host and pathogen microbiomes. Aphids host several species of heritable bacteria, some of which confer resistance againstPandora. We first found that spores that emerged from aphids that harbored protective bacteria were less virulent against subsequent hosts and did not grow on plate media. We then used 16S amplicon sequencing to study the bacterial microbiome of fungal mycelia and spores during plate culturing and host infection. We found that the bacterial community is remarkably stable in culture despite dramatic changes in pathogen virulence. Last, we used an experimentally transformed symbiont of aphids to show thatPandoracan acquire host-associated bacteria during infection. Our results uncover new roles for bacteria in the dynamics of aphid-pathogen interactions and illustrate the importance of the broader microbiological context in studies of fungal pathogenesis. IMPORTANCEEntomopathogenic fungi play important roles in the population dynamics of many insect species. Understanding the factors shaping entomopathogen virulence is critical for agricultural management and for the use of fungi in pest biocontrol. We show that heritable bacteria in aphids, which confer protection to their hosts against fungal entomopathogens, influence virulence against subsequent hosts. Aphids reproduce asexually and are typically surrounded by genetically identical offspring, and thus these effects likely shape the dynamics of fungal disease in aphid populations. Furthermore, fungal entomopathogens are known to rapidly lose virulence in lab culture, complicating their laboratory use. We show that this phenomenon is not driven by changes in the associated bacterial microbiome. These results contribute to our broader understanding of the aphid model system and shed light on the biology of the Entomophthorales—an important but understudied group of fungi.