Asymmetric biparental but inefficient horizontal transmission of paralysis-causing sigmavirus in Queensland fruit fly

Abstract

Insects are associated with diverse RNA viruses, including vertically transmitted viruses that form persistent infections without apparent symptoms. One of the first documented vertically transmitted viruses is sigmavirus (Rhabdoviridae) affecting fitness of Drosophila. Sigmaviruses and related rhabdoviruses have also been detected in pest fruit flies and other arthropods. However, their prevalence, transmission, tissue localisation and fitness effects remain poorly known, despite their potentially common infections in diverse hosts. We investigated Sigmavirus tryoni (BtSV) prevalence, load, transmission across multiple generations and host effects in Queensland fruit fly (Bactrocera tryoni), Australias most significant horticultural pest, which carries BtSV at low prevalence (13.7%) across field populations. We detected BtSV in 6 of 12 laboratory populations (prevalence 12.5% to 80.4%) where it was transmitted biparentally within embryos. Although incomplete, maternal transmission was more reliable and resulted in higher BtSV load than paternal transmission. Paternally transmitted BtSV was almost entirely lost after two generations. BtSV became detectable in most uninfected individuals cohabiting with infected flies, but this resulted in a low load that was subsequently transmitted to only few offspring. BtSV occurred across developmental stages, digestive and reproductive tissues, albeit its viral load was lower in reproductive tissues when received paternally than maternally, and lower in testes than ovaries. Furthermore, BtSV-infected individuals suffered paralysis and mortality when exposed to high CO2 concentrations, a Rhabdoviridae effect previously reported for several Drosophila species, a muscid fly and mosquitoes. Our study suggests that sigmavirus transmission dynamics and fitness effects may apply broadly to arthropod hosts and affect their management.