Abstract
The vertically transmitted endosymbionts (Sodalis glossinidius and Wigglesworthia glossinidia) of the tsetse fly (Diptera: Glossinidae) are known to supplement dietary deficiencies and modulate the reproductive fitness and the defense system of the fly. Some tsetse fly species are also infected with the bacterium, Wolbachia and with the Glossina hytrosavirus (GpSGHV). Laboratory-bred G. pallidipes exhibit chronic asymptomatic and acute symptomatic GpSGHV infection, with the former being the most common in these colonies. However, under as yet undefined conditions, the asymptomatic state can convert to the symptomatic state, leading to detectable salivary gland hypertrophy (SGH+) syndrome. In this study, we investigated the interplay between the bacterial symbiome and GpSGHV during development of G. pallidipes by knocking down the symbionts with antibiotic. Intrahaemocoelic injection of GpSGHV led to high virus titre (109 virus copies), but was not accompanied by either the onset of detectable SGH+, or release of detectable virus particles into the blood meals during feeding events. When the F1 generations of GpSGHV-challenged mothers were dissected within 24 h post-eclosion, SGH+ was observed to increase from 4.5% in the first larviposition cycle to >95% in the fourth cycle. Despite being sterile, these F1 SGH+ progeny mated readily. Removal of the tsetse symbiome, however, suppressed transgenerational transfer of the virus via milk secretions and blocked the ability of GpSGHV to infect salivary glands of the F1 progeny. Whereas GpSGHV infects and replicates in salivary glands of developing pupa, the virus is unable to induce SGH+ within fully differentiated adult salivary glands. The F1 SGH+ adults are responsible for the GpSGHV-induced colony collapse in tsetse factories. Our data suggest that GpSGHV has co-evolved with the tsetse symbiome and that the symbionts play key roles in the virus transmission from mother to progeny.
Highlights
Tsetse flies (Glossina spp.), obligatory blood-feeders, are distributed throughout tropical sub-Saharan Africa and are vectors of Trypanosoma spp. that cause African animal trypanosomosis (AAT) or nagana in livestock and human African trypanosomosis (HAT) or sleeping sickness in humans [1,2]
The virus copy numbers present in the filtrate were estimated by quantitative PCR using a standard prepared by amplified GpSGHV ORF005 amplicons as previously described [42]
Haemocoelic injection of the GpSGHV into adults did not increase the incidence of SGH+ in those flies (Table 1); we expected that bypassing both the cuticle and gut barriers would have induced heavy infections and high incidence of SGH+ in virus-injected adults
Summary
Tsetse flies (Glossina spp.), obligatory blood-feeders, are distributed throughout tropical sub-Saharan Africa and are vectors of Trypanosoma spp. that cause African animal trypanosomosis (AAT) or nagana in livestock and human African trypanosomosis (HAT) or sleeping sickness in humans [1,2]. In many parts of sub-Saharan Africa, AAT and the presence of tsetse are considered as major obstacles to the development of more efficient and sustainable livestock production systems and represent one of the most important root causes of hunger and poverty [3,4]. The use of sterile insects as part of an areawide integrated pest management (AW-IPM) [7,8] approach is considered a very powerful control tactic for the sustainable eradication of tsetse flies as amply demonstrated on the island of Unguja, Zanzibar [9]. The efficient implementation of sterile insect technology (SIT) for tsetse control depends on the successful establishment of tsetse factories to produce high quality males capable of competing with wild males for mating with wild tsetse females [10]
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