Musca domestica Salivary Gland Hypertrophy Virus, a Globally Distributed Insect Virus That Infects and Sterilizes Female Houseflies

Abstract

The housefly, Musca domestica, is a cosmopolitan pest of livestock and poultry and is of economic, veterinary, and public health importance. Populations of M. domestica are naturally infected with M. domestica salivary gland hypertrophy virus (MdSGHV), a nonoccluded double-stranded DNA virus that inhibits egg production in infected females and is characterized by salivary gland hypertrophy (SGH) symptoms. MdSGHV has been detected in housefly samples from North America, Europe, Asia, the Caribbean, and the southwestern Pacific. In this study, houseflies were collected from various locations and dissected to observe SGH symptoms, and infected gland pairs were collected for MdSGHV isolation and amplification in laboratory-reared houseflies. Differences among the MdSGHV isolates were examined by using molecular and bioassay approaches. Approximately 600-bp nucleotide sequences from each of five open reading frames having homology to genes encoding DNA polymerase and partial homology to the genes encoding four per os infectivity factor proteins (p74, pif-1, pif-2, and pif-3) were selected for phylogenetic analyses. Nucleotide sequences from 16 different geographic isolates were highly homologous, and the polymorphism detected was correlated with geographic source. The virulence of the geographic MdSGHV isolates was evaluated by per os treatment of newly emerged and 24-h-old houseflies with homogenates of infected salivary glands. In all cases, 24-h-old flies displayed a resistance to oral infection that was significantly greater than that displayed by newly eclosed adults. Regardless of the MdSGHV isolate tested, all susceptible insects displayed similar degrees of SGH and complete suppression of oogenesis. Salivary gland hypertrophy virus (SGHV) ofMusca domestica L. (Diptera: Muscidae) (MdSGHV) was originally detected in adult houseflies collected from dairies located in north Florida (2). Since the original description of this virus, a series of studies have detailed its molecular and biological properties. The circular double-stranded DNA (dsDNA) genome of MdSGHV consists of 124,279 bp and contains over 100 open reading frames (ORFs) (6,16). The virus, which replicates in the salivary glands of adult flies, is readily transmitted per os to healthy conspecific animals (15). During feeding, high numbers of infectious virus particles are deposited on the solid food substrate that is fed upon by healthy houseflies. The development of viremia in female houseflies leads to a shutdown of egg production (7,14). Associated with female sterility is the downregulation of egg protein gene transcription in the fat body (14). In feral housefly populations, the incidence of infection may peak at 34% at selected sites (7), although at any given sampling time the incidence typically ranges from 1 to 10%. As expected with an orally transmitted virus, infection frequency is positively correlated with housefly density.Recently, we initiated a program directed at expanding the current collection of SGHVs associated with M. domestica. ...

Disease Dynamics and Persistence of Musca domestica Salivary Gland Hypertrophy Virus Infections in Laboratory House Fly (Musca domestica) Populations

“…Bioassay 1 compared transmission of MdSGHV03 at two different ratios of infected donor to uninfected exposed flies (40:60 and 10:90). Bioassay 2 compared transmission of three different geographical strains, MdSGHV03 (Florida), MdSGHV07 (New Zealand), and MdSGHV15 (Denmark), reported previously to express different levels of infectivity (31), at a 40:60 ratio of donor flies to exposed flies. For both bioassays, marked, injected donor flies (n ϭ 40 or 10 flies at a 1:1 gender ratio) were transferred to a wire-screened cage (30 ϫ 30 ϫ 20 cm 3 ) containing water and food.…”

“…Most experiments were conducted using the Florida type virus strain (MdSGHV03); in experiments examining transmission within small fly populations, additional strains from Denmark and New Zealand (MdSGHV15 and MdSGHV07, respectively) were included (31). These strains are maintained as part of the Insect Pathology Lab Virus Collection at the University of Florida, Entomology and Nematology Department, Gainesville, FL, and are stored in ready-to-use aliquots at Ϫ70°C (31).…”

“…If transmission and disease spread occur at sufficiently high rates, introduction of MdSGHV into fly populations may lead to an epizootic and result in a population collapse. However, our field surveys have not indicated such dynamics but instead suggest that MdSGHV infections are of a chronic (i.e., long-lasting) nature, accounting for persistent (i.e., long-term) low-level infection rates in fly populations (12,13,31).…”

“…During one short feeding event (lasting 2 to 3 s), an infected fly releases roughly 10 6 virions, and the released virus is infectious when consumed by healthy flies (12,23). However, flies subjected to forcefeeding assays develop resistance to oral infection within 24 h after eclosion (31). Because feral flies are unlikely to commence foraging and feeding activities during this time window, the per os infection route alone does not appear to explain viral transmission and disease manifestation under natural conditions.…”

“…usca domestica salivary gland hypertrophy virus (MdSGHV) is a globally distributed, insect-pathogenic virus that infects adult house flies exclusively (13,21,31). This enveloped, nonoccluded, double-stranded DNA (dsDNA) virus causes symptomatic salivary gland hypertrophy (SGH) in both genders of M. domestica flies and suppresses ovarian development in infected females (7,22).…”