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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. 

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.