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

Daniela I Schneider,Maria G Onyango,Elizabeth Opiyo,Brian L Weiss,T J Johnson,Serap Aksoy,Kirstin Dion,Michelle O’Neill,Norah Saarman,Danielle Bloch,Robert Opiro,Richard Echodu,Chaz Hyseni,Adalgisa Caccone,Aurélien Vigneron,Guy Caljon

doi:10.1371/journal.pntd.0007340

Abstract

Tsetse 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.

Highlights

Tsetse flies (Glossina spp.) are vectors of parasitic African trypanosomes that cause human African trypanosomiasis (HAT, commonly referred to as sleeping sickness) and African animal trypanosomiasis (AAT, known as Nagana in cattle) [1,2,3]
We investigated the association of symbiotic Spiroplasma with the tsetse fly host Glossina fuscipes fuscipes (Gff) to assess if Spiroplasma infections are correlated with Gff genetic background, geography, or season and its interaction with trypanosome parasites
We tested for associations with geographic origin of the collections, seasonal environmental conditions at the time of collection, Gff host genetic background and sex, plus trypanosome coinfections

Summary

Introduction

Tsetse flies (Glossina spp.) are vectors of parasitic African trypanosomes that cause human African trypanosomiasis (HAT, commonly referred to as sleeping sickness) and African animal trypanosomiasis (AAT, known as Nagana in cattle) [1,2,3]. Several major HAT epidemics in sub-Saharan Africa have occurred during the last century, with the most recent one resulting in over half a million deaths in the 1980s [4,5,6,7]. An ambitious campaign led by WHO and international partners has reduced the prevalence of HAT in west Africa [8] to a threshold considered irrelevant for epidemiological considerations, but millions continue to live at risk of contracting HAT in tsetse inhabited areas [9,10,11]. Despite calls for elimination of HAT by 2030, there is a lack of effective tools for long-term control of the disease (e.g., vaccines and field-ready diagnostic assays). The presence of animal reservoirs threatens disease elimination efforts going forward, in East Africa (reviewed in [12]) and necessitates the inclusion of vector control applications. Biological approaches that reduce vector reproduction as well as vector competency have emerged as promising means to reduce disease transmission [19]

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Conclusion