Abstract

African trypanosomiasis (AT) is a neglected disease of both humans and animals caused by Trypanosoma parasites, which are transmitted by obligate hematophagous tsetse flies (Glossina spp.). Knowledge on tsetse fly vertebrate hosts and the influence of tsetse endosymbionts on trypanosome presence, especially in wildlife-human-livestock interfaces, is limited. We identified tsetse species, their blood-meal sources, and correlations between endosymbionts and trypanosome presence in tsetse flies from the trypanosome-endemic Maasai Mara National Reserve (MMNR) in Kenya. Among 1167 tsetse flies (1136 Glossina pallidipes, 31 Glossina swynnertoni) collected from 10 sampling sites, 28 (2.4%) were positive by PCR for trypanosome DNA, most (17/28) being of Trypanosoma vivax species. Blood-meal analyses based on high-resolution melting analysis of vertebrate cytochrome c oxidase 1 and cytochrome b gene PCR products (n = 354) identified humans as the most common vertebrate host (37%), followed by hippopotamus (29.1%), African buffalo (26.3%), elephant (3.39%), and giraffe (0.84%). Flies positive for trypanosome DNA had fed on hippopotamus and buffalo. Tsetse flies were more likely to be positive for trypanosomes if they had the Sodalis glossinidius endosymbiont (P = 0.0002). These findings point to complex interactions of tsetse flies with trypanosomes, endosymbionts, and diverse vertebrate hosts in wildlife ecosystems such as in the MMNR, which should be considered in control programs. These interactions may contribute to the maintenance of tsetse populations and/or persistent circulation of African trypanosomes. Although the African buffalo is a key reservoir of AT, the higher proportion of hippopotamus blood-meals in flies with trypanosome DNA indicates that other wildlife species may be important in AT transmission. No trypanosomes associated with human disease were identified, but the high proportion of human blood-meals identified are indicative of human African trypanosomiasis risk. Our results add to existing data suggesting that Sodalis endosymbionts are associated with increased trypanosome presence in tsetse flies.

Highlights

  • African trypanosomes, cyclically transmitted by the tsetse fly vector, cause a group of diseases known as African trypanosomiasis (AT)

  • We found that Glossina pallidipes was the major tsetse fly vector and that Trypanosoma vivax was the main trypanosome species circulating in the region

  • Field sampling was performed between June and July 2016, within the Maasai Mara National Reserve (MMNR) (1 ̊29024@S 35 ̊ 8038@E, 1500 m above sea level), located in southwest region of Kenya, which is contiguous with the Serengeti National Park (SNP) in Tanzania (Fig 1)

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Summary

Introduction

African trypanosomes (genus Trypanosoma), cyclically transmitted by the tsetse fly vector (genus Glossina), cause a group of diseases known as African trypanosomiasis (AT). Reduced productivity due to chronic disease in humans and animals and loss of livestock through death threatens food security, quality of living, and economic stability, in regions where pastoralism is the main economic activity [3,4,5]. To address the limitations associated with chemotherapy, disruption of trypanosomes transmission through vector control is crucial. Tsetse fly blood-meal sources are highly variable, especially in wildlife areas. Identification of tsetse fly blood-meal host sources in specific regions can help to elucidate wildlife species that are potentially involved in AT transmission and provide a baseline for research towards improving vector-control strategies, in wildlife-human-livestock interfaces that serve as hotspots for the emergence and re-emergence of AT

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