Spatio-temporal distribution of Spiroplasma infections in the tsetse fly (Glossina fuscipes fuscipes) in northern Uganda

Abstract

DIS) ¶ These authors contributed equally to this work. AbstractTsetse flies (Glossina spp.) are vectors of parasitic trypanosomes, which cause human (HAT) and animal African trypanosomiasis (AAT) in sub-Saharan Africa. In Uganda, Glossina fuscipes fuscipes (Gff) is the main vector of HAT, where it transmits Gambiense disease in the northwest and Rhodesiense disease in central, southeast and western regions. Endosymbionts can influence transmission efficiency of parasites through their insect vectors via conferring a protective effect against the parasite. It is known that the bacterium Spiroplasma is capable of protecting its Drosophila host from infection with a parasitic nematode. This endosymbiont can also impact its host's population structure via altering host reproductive traits. Here, we used field collections across 26 different Gff sampling sites in northern and western Uganda to investigate the association of Spiroplasma with geographic origin, seasonal conditions, Gff genetic background and sex, and trypanosome infection status. We also investigated the influence of Spiroplasma on Gff vector competence to trypanosome infections under laboratory conditions. Generalized linear models (GLM) showed that Spiroplasma probability was correlated with the geographic origin of Gff host and with the season of collection, with higher prevalence found in flies within the Albert Nile (0.42 vs 0.16) and Achwa River (0.36 vs 0.08) watersheds and with higher prevalence detected in flies collected in the intermediate than wet season. In contrast, there was no significant correlation of Spiroplasma prevalence with Gff host genetic background or sex once geographic origin was accounted for in generalized linear models. Additionally, we found a potential negative correlation of Spiroplasma with trypanosome infection, with only 2% of Spiroplasma infected flies harboring trypanosome co-infections. We also found that in a laboratory line of Gff, parasitic trypanosomes are less likely to colonize the midgut in individuals that harbor Spiroplasma infection. These results indicate that Spiroplasma infections in tsetse may be maintained by not only maternal but also via horizontal transmission routes, and Spiroplasma infections may also have important effects on trypanosome transmission efficiency of the host tsetse. Potential functional effects of Spiroplasma infection in Gff could have impacts on vector control approaches to reduce trypanosome infections. Author SummaryWe investigated the association of symbiotic Spiroplasma with the tsetse fly host Glossina fuscipes fuscipes (Gff) to assess if Spiroplasma infections are correlated withGff genetic background, geography, or season and its interaction with trypanosome parasites. We analyzed distribution and prevalence of Spiroplasma infections across different Gff sampling sites in northern and western Uganda, and found that the symbiont is unevenly distributed and infections have not reached fixation within these sampling sites. We tested for associations with geographic origin ...

Rapid molecular evolution ofSpiroplasmasymbionts ofDrosophila

“…Although independent findings discussed above suggest that Spiroplasma symbionts may evolve quickly, this has never been quantified, and it has remained unclear how substitution rates compare to those of other symbionts. However, rates and patterns of evolutionary change may have important implications for Spiroplasma evolutionary ecology, and for its potential use in biological control programmes (Clark and Whitcomb, 1984;Schneider et al, 2019).…”

Interactions between Glossina pallidipes Salivary Gland Hypertrophy Virus and tsetse endosymbionts in wild tsetse populations

“…Tsetse ies (Glossina spp.) accommodate various types of bacteria, including two gut-associated bacterial symbionts, the obligate Wigglesworthia glossinidia, and the commensal Sodalis glossinidius, the widespread symbiont Wolbachia pipientis, and a recently discovered Spiroplasma endosymbiont [7][8][9][10][11][12][13]. In addition, tsetse ies can house different types of viral infection, including the salivary gland hypertrophy virus (GpSGHV), i avirus, and negevirus, besides trypanosome parasites [14][15][16][17].…”

Interactions between Glossina pallidipes salivary gland hypertrophy virus and tsetse endosymbionts in wild tsetse populations

“…Tsetse flies (Glossina spp.) accommodate various types of bacteria, including two gut-associated bacterial symbionts, the obligate Wigglesworthia glossinidia and the commensal Sodalis glossinidius, the widespread symbiont Wolbachia pipientis, and a recently discovered Spiroplasma endosymbiont [7][8][9][10][11][12][13]. In addition, tsetse flies can house different types of viral infection, including the salivary gland hypertrophy virus (GpSGHV), iflavirus, and negevirus, besides trypanosome parasites [14][15][16][17].…”

“…They also live considerably longer than other vector insects, which somewhat compensates for their slow reproduction rate [40]. The ability to nourish larvae on the milk gland secretion, although limiting the number of larvae produced per female lifetime (8)(9)(10)(11)(12), facilitates the transmition of endosymbitic bacteria and pathogens from females to larvae such as Wigglesworthia, Sodalis, Wolbachia, Spiroplasma, and GpSGHV [8,10,13,41]. Moreover, as strictly hematophagous, tsetse rely on the associated endosymbionts to obtain essential nutrients for female reproduction.…”