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

PLoS Negl Trop Dis. 2021 Jan 6;15(1):e0008267. doi: 10.1371/journal.pntd.0008267. eCollection 2021 Jan.

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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Animals, Wild / parasitology*
  • Artiodactyla / parasitology
  • Blood
  • Buffaloes / parasitology
  • Ecosystem
  • Elephants / parasitology
  • Enterobacteriaceae
  • Humans
  • Insect Vectors / parasitology*
  • Kenya
  • Livestock / parasitology*
  • Polymerase Chain Reaction
  • Symbiosis / physiology*
  • Trypanosoma / genetics
  • Trypanosoma / physiology*
  • Trypanosoma vivax
  • Trypanosomiasis, African / parasitology
  • Tsetse Flies / parasitology*

Supplementary concepts

  • Sodalis glossinidius

Grants and funding

We are grateful for the financial support for this research from the United States Agency for International Development (USAID), Partnerships for Enhanced Engagement in Research (USAID-PEER), https://www.usaid.gov/what-we-do/GlobalDevLab/international-research-science-programs/peer, funding cycle 4 under the USAID grant No. AID-OAA-A-11-00012, sub-awarded to LW and a supplementary grant to JV by the American National Academy of Sciences (NAS), http://www.nasonline.org, under agreement No. 2000006204, and icipe institutional funding from the UK’s Department for International Development (DFID), the Swedish International Development Cooperation Agency (SIDA), the Swiss Agency for Development and Cooperation (SDC), and the Kenyan Government. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.