Tsetse blood-meal sources, endosymbionts and trypanosome-associations in the Maasai Mara National Reserve, a wildlife-human-livestock interface

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.

Overview of paratransgenesis as a strategy to control pathogen transmission by insect vectors

“…There is also evidence that some Sodalis genotypes can favour the establishment of trypanosme infections in tsetse flies by inhibiting the trypanocidal activity of the Glossina midgut lectin (e.g. [ 269 , 274 , 296 – 298 ]), although this varies with species, location and study [ 271 , 276 ].…”

Blood meal analysis of tsetse flies (Glossina pallidipes: Glossinidae) reveals higher host fidelity on wild compared with domestic hosts

“…The distance between traps at each site was 200–500 m. Trapped flies were collected at 17.00 pm each day, which has been found to be the highest interaction period between hosts and tsetse flies 26 . The number of flies we aimed to capture was aound 100 samples based on prevous studies which have used 100–200 flies 35 , 40 . Whole flies were preserved in 95% ethanol and storage at -80°C.…”

Parasites and blood-meal hosts of the tsetse fly in Tanzania: a metagenomics study

“…For example, humans, cattle, dogs, bush pigs, African buffaloes, warthogs, greater kudus, rats, and bats were confirmed as the blood-meal sources of tsetse flies in Zambia, using 12S ribosomal RNA (rRNA) gene deep sequencing [ 7 ]. Analysis of tsetse flies using vertebrate cytochrome c oxidase I (COX1) and cytochrome b gene polymerase chain reaction (PCR) revealed that humans are the most common vertebrate hosts [ 8 ]. This also indicated that other wild species, such as hippopotamuses, African buffaloes, African savannah elephants, and giraffes, may be involved in trypanosomiasis transmission.…”