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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. 

Vesicular stomatitis virus (VSV) is an arthropod-borne virus affecting livestock. In the United States, sporadic outbreaks result in significant economic losses. During epizootics, Culicoides biting midges are biological vectors and key to the geographic expansion of outbreaks. Additionally, Culicoides may play a role in VSV overwintering because females and males are capable of highly efficient venereal transmission, despite their relatively low virus titers. We hypothesized that VSV propagated within a midge has increased fitness for subsequent midge infections. To evaluate the potential host-specific fitness increase, we propagated three viral isolates of VSV in porcine skin fibroblasts and Culicoides cell lines. We then evaluated the viral infection dynamics of the different cell-source groups in Culicoides sonorensis. Our results indicate that both mammalian- and insect-derived VSV replicate well in midges inoculated via intrathoracic injection, thereby bypassing the midgut barriers. However, when the virus was required to infect and escape the midgut barrier to disseminate after oral acquisition, the insect-derived viruses had significantly higher titers, infection, and dissemination rates than mammalian-derived viruses. Our research suggests that VSV replication in Culicoides cells increases viral fitness, facilitating midge-to-midge transmission and subsequent replication, and further highlights the significance of Culicoides midges in VSV maintenance and transmission dynamics.