Shared species of crocodilian trypanosomes carried by tabanid flies in Africa and South America, including the description of a new species from caimans, Trypanosoma kaiowa n. sp.

Bruno R Fermino,Marta M G Teixeira,Erney P Camargo,Herakles A Garcia,Carla M F Rodrigues,Desie Sheferaw,Marta Campaner,Carmen S A Takata,Fernando Paiva,John J Kisakye,Laerte B Viola,Agapitus Kato,Carlos A G S Jared

doi:10.1186/s13071-019-3463-2

Abstract

BackgroundThe genus Trypanosoma Gruby, 1843 is constituted by terrestrial and aquatic phylogenetic lineages both harboring understudied trypanosomes from reptiles including an increasing diversity of crocodilian trypanosomes. Trypanosoma clandestinus Teixeira & Camargo, 2016 of the aquatic lineage is transmitted by leeches to caimans. Trypanosoma grayi Novy, 1906 of the terrestrial lineage is transmitted by tsetse flies to crocodiles in Africa, but the vectors of Neotropical caiman trypanosomes nested in this lineage remain unknown.ResultsOur phylogenetic analyses uncovered crocodilian trypanosomes in tabanids from South America and Africa, and trypanosomes other than T. grayi in tsetse flies. All trypanosomes found in tabanids clustered in the crocodilian clade (terrestrial lineage) forming six clades: Grayi (African trypanosomes from crocodiles and tsetse flies); Ralphi (trypanosomes from caimans, African and Brazilian tabanids and tsetse flies); Terena (caimans); Cay03 (caimans and Brazilian tabanids); and two new clades, Tab01 (Brazilian tabanid and tsetse flies) and Kaiowa. The clade Kaiowa comprises Trypanosoma kaiowa n. sp. and trypanosomes from African and Brazilian tabanids, caimans, tsetse flies and the African dwarf crocodile. Trypanosoma kaiowa n. sp. heavily colonises tabanid guts and differs remarkably in morphology from other caiman trypanosomes. This species multiplied predominantly as promastigotes on log-phase cultures showing scarce epimastigotes and exhibited very long flagellates in old cultures. Analyses of growth behavior revealed that insect cells allow the intracellular development of Trypanosoma kaiowa n. sp.ConclusionsPrior to this description of Trypanosoma kaiowa n. sp., no crocodilian trypanosome parasitic in tabanid flies had been cultured, morphologically examined by light, scanning and transmission microscopy, and phylogenetically compared with other crocodilian trypanosomes. Additionally, trypanosomes thought to be restricted to caimans were identified in Brazilian and African tabanids, tsetse flies and the dwarf crocodile. Similar repertoires of trypanosomes found in South American caimans, African crocodiles and tabanids from both continents support the recent diversification of these transcontinental trypanosomes. Our findings are consistent with trypanosome host-switching likely mediated by tabanid flies between caimans and transoceanic migrant crocodiles co-inhabiting South American wetlands at the Miocene.

Highlights

The genus Trypanosoma Gruby, 1843 is constituted by terrestrial and aquatic phylogenetic lineages both harboring understudied trypanosomes from reptiles including an increasing diversity of crocodilian trypanosomes
Tabanids from Brazil and Africa and tsetse flies harbour trypanosomes from the crocodilian clade Two species of tabanids, Phaeotabanus fervens Linnaeus (48 flies) and Tabanus occidentalis Linnaeus (3 flies), identified by cox1 barcoding, were caught while feeding on Ca. yacare captured in the Miranda River, in the Pantanal biome, Brazil (Fig. 1)
To the best of our knowledge, data gathered in the present study provide the first evidence that tabanids can cyclically transmit trypanosomes to caimans and crocodiles in the Neotropic and Afrotropic

Summary

Introduction

The genus Trypanosoma Gruby, 1843 is constituted by terrestrial and aquatic phylogenetic lineages both harboring understudied trypanosomes from reptiles including an increasing diversity of crocodilian trypanosomes. Trypanosoma grayi Novy, 1906 of the terrestrial lineage is transmitted by tsetse flies to crocodiles in Africa, but the vectors of Neotropical caiman trypanosomes nested in this lineage remain unknown. Previous phylogenies, including T. grayi from tsetse flies and crocodiles [3, 8, 9] and trypanosomes from South American caimans [10,11,12] enabled the description of three additional species: Trypanosoma terena Teixeira & Camargo, 2013, Trypanosoma ralphi Teixeira & Camargo, 2013, and Trypanosoma clandestinus Teixeira & Camargo, 2016. Trypanosomes of land mammals, bats, birds, snakes and lizards, nest in the terrestrial lineage, together with the crocodilian trypanosomes T. grayi, T. terena and T. ralphi [4, 9,10,11,12, 20,21,22,23]

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