Abstract

Obligate hematophagous ectoparasitic flies of the superfamily Hippoboscoidea are distributed worldwide, but their role as vectors and reservoirs of viruses remains understudied. We examined hippoboscoid bat flies (family Nycteribiidae) parasitizing Angolan soft-furred fruit bats (Lissonycteris angolensis ruwenzorii) from Bundibugyo District, Uganda. Using metagenomic methods, we detected 21 variants of the rhabdovirid genus Ledantevirus, which contains medically important “bat-associated” viruses. These 21 viruses, representing at least two divergent viral lineages, infected 26 bat flies from 8 bats in a single roost. Cophylogenetic analyses of viruses and bat flies resulted in strong evidence of virus-host codivergence, indicating vertical transmission of bat fly ledanteviruses. Examination of oral swabs from bats revealed ledantevirus RNA in the saliva of 1 out of 11 bats, with no evidence of insect genetic material in the mouth of this bat. These data demonstrate that bat flies can harbor diverse ledanteviruses even in a single roost and that the predominant mode of transmission is likely vertical (among bat flies), but that bats can become infected and shed viruses orally. In conclusion, bat flies may serve as ectoparasitic reservoirs of “bat-associated” viruses that only transiently or sporadically infect bats.

Highlights

  • Flies of the superfamily Hippoboscoidea are globally distributed obligate dipteran ectoparasites of vertebrates

  • We examined the degree of co-divergence between viruses and bat fly mitochondrial genome DNA (mtDNA) using Procrustes application to cophylogenetic analysis (PACo) [28] implemented in R [29]

  • Metagenomic sequencing of bat flies revealed the presence of viruses of the rhabdovirid genus Ledantevirus in 21 of 26 of the flies (80.7%)

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Summary

Introduction

Flies of the superfamily Hippoboscoidea are globally distributed obligate dipteran ectoparasites of vertebrates. Diverse viruses have been discovered in nycteribiid bat flies. Mahlapitsi virus (MAHLV), a fusogenic orthoreovirus (Reoviridae: Spinareovirinae), was detected in the nycteribiid Eucampsipoda africana Theodor, 1955 parasitizing Egyptian rousettes 1810) in Limpopo Province, South Africa [2]. Two novel orthobunyaviruses (Bunyavirales: Peribunyaviridae) were detected in Eucampsipoda africana parasitizing Egyptian rousettes in South Africa (Wolkberg virus [WBV]) [3] and Eucampsipoda sundaica Theodor, 1955 parasitizing Leschenault’s rousettes (Rousettus leschenaultii Desmarest, 1820) in Yúnnán Province, China (Kaeng Khoi virus; KKV) [4,5]. We previously described Kanyawara virus (KYAV), a member of genus Ledantevirus (Mononegavirales: Rhabdoviridae) in unspecified dipseliopod nycteribiid bat flies parasitizing unspecified collared fruit bats (Myonycteris sp.) in Kabarole District, Uganda [6]

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