Effects of Salivary Gland Hypertrophy Virus on the Reproductive Behavior of the Housefly, Musca domestica

Abstract

Pathological studies demonstrated that the salivary gland hypertrophy virus of houseflies (MdSGHV) shuts down reproduction in infected females. The mechanism that underlay the disruption of reproduction functioned on several levels. Females infected at the previtellogenic stage did not produce eggs, reflecting a block in the gonadotropic cycle. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis and Western blot analysis of hemolymph samples demonstrated that MdSGHV infection reduced the levels of both the female-specific hexamerin and egg yolk proteins. Furthermore, reverse transcriptase quantitative real-time PCR data demonstrated that infection blocked hexamerin and yolk protein gene transcription. When females were allowed to develop eggs prior to infection (postvitellogenic stage), the outcome of mating attempts depended upon when mating took place. If egg-containing, virus-infected females were mated within 24 h of infection, they copulated and deposited a single batch of fertilized eggs. However, if mating was delayed for a longer period, the egg-containing females refused to copulate with healthy males. Both of these results suggested that a virusinduced signal influenced the central nervous system, shutting down female receptivity and egg production. All experiments demonstrated that MdSGHV-infected males did not display azoospermia and were fertile. Both healthy females mated with infected males, and the resulting F1 progeny were free of salivary gland hypertrophy symptoms, which suggests that the virus is not sexually or vertically transmitted.In the early 1990s, an insect virus was detected and isolated from hypertrophied salivary glands of male and female houseflies, Musca domestica L., in Florida. The virus was described initially as a nonoccluded, enveloped, rod-shaped, doublestranded DNA virus (7). Feeding bioassays demonstrated that the virus could be transmitted per os to healthy adult houseflies and that infection with the virus was responsible for the salivary gland hypertrophy (SGH) symptoms. In these experiments, 95% of the female houseflies with symptoms of SGH showed no sign of ovarian development (7). A similar virus causing symptoms of SGH has been reported in the narcissus bulb fly, Merodon equestris (Fabricius) (3), and in various species of tsetse flies, Glossina spp. (3, 11). Comparisons of the different virus-host fly systems have demonstrated that the different viruses have several morphological and pathological properties in common (3,7,8,11,15,16,19). Electron microscopic observation of virus particles either in thin sections of hypertrophied salivary glands or from sucrose density gradientpurified, negatively stained preparations showed enveloped bacilliform virions. In all three fly groups, the virus replicates in the salivary gland tissue of male and female flies. Additionally, infected adults do not exhibit any external disease symptoms, and morphogenesis occurs in the nuclei, resulting in nuclear SGH.The most thoroughly studied SGH viruses (SGHVs) are those associated...

Two viruses that cause salivary gland hypertrophy in Glossina pallidipes and Musca domestica are related and form a distinct phylogenetic clade

“…The tissue tropism differs between these viruses. MdSGHV appears to only replicate in the salivary gland tissue and only sterilizes female house flies (Lietze et al, 2007;Geden et al, 2008). No morphological aberrations have been observed in female accessory glands, in spermathecae, or in the male ejaculatory tract, and testes of infected males contain viable sperm (Lietze et al, 2007).…”

“…The viral infection of M. domestica salivary gland hypertrophy virus (MdSGHV) and Glossina pallipides salivary gland hypertrophy virus (GpSGHV) is known to reduce reproduction in the house fly and tsetse fly, respectively (Sang et al, 1998(Sang et al, , 1999Lietze et al, 2007).…”

Analysis of transcripts from predicted open reading frames of Musca domestica salivary gland hypertrophy virus

“…Pupae were transferred to 72-ounce plastic jars provisioned with deionized water and maintained under constant conditions (26 uC, 12 h light : 12 h dark, 40 % relative humidity). Newly emerged adults received injections of filter-sterilized viraemic salivary gland homogenate, as described by Lietze et al (2007). Briefly, one infectedgland-pair equivalent (IGE) was dissected from an infected house fly, homogenized in 0.5 ml sterile saline solution (0.85 % NaCl), filtered through a 0.45 mm filter unit, and stored in aliquots at 235 uC until used for injection.…”

“…), and the narcissus bulb fly (Merodon equestris) (Amargier et al, 1979;Coler et al, 1993;Gouteux, 1987;Jaenson, 1978;Minter-Goedbloed & Minter, 1989;Otieno et al, 1980;Shaw & Moloo, 1993). Infection by these viruses both induces SGH and reduces reproductive fitness (Lietze et al, 2007;Sang et al, 1998Sang et al, , 1999. Currently, our lab is using the M. domestica SGHV (MdSGHV) to study the replicative pathway and mode of action of this unique virus group.…”

Entomopathogens in control of urban pests

“…israelensis in poultry farms suggest that Bti warrants further study (56). House fly salivary gland hypertrophy virus (MdSGHV) has the appealing property of shutting down reproductive development in adult flies but attempts to develop infective baits have been hampered by the refractoriness of older flies to oral infection (15,16,32). Space sprays to treat flies directly may have more potential for delivering MdSGHV into fly populations (33,34).…”