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      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.

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          Abstract

          Background

          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 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.

          Results

          Our 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.

          Conclusions

          Prior 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.

          Electronic supplementary material

          The online version of this article (10.1186/s13071-019-3463-2) contains supplementary material, which is available to authorized users.

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          Most cited references53

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          PHYLOGENETICAPPROACHESTOWARDCROCODYLIANHISTORY

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            The Late Miocene paleogeography of the Amazon Basin and the evolution of the Amazon River system

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              Trypanosomatids Are Much More than Just Trypanosomes: Clues from the Expanded Family Tree.

              Trypanosomes and leishmanias are widely known parasites of humans. However, they are just two out of several phylogenetic lineages that constitute the family Trypanosomatidae. Although dixeny - the ability to infect two hosts - is a derived trait of vertebrate-infecting parasites, the majority of trypanosomatids are monoxenous. Like their common ancestor, the monoxenous Trypanosomatidae are mostly parasites or commensals of insects. This review covers recent advances in the study of insect trypanosomatids, highlighting their diversity as well as genetic, morphological and biochemical complexity, which, until recently, was underappreciated. The investigation of insect trypanosomatids is providing an important foundation for understanding the origin and evolution of parasitism, including colonization of vertebrates and the appearance of human pathogens.
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                Author and article information

                Contributors
                brunorf@usp.br
                fernando.paiva@ufms.b
                laerte.viola@arcadislogos.com.br
                cmonadeli@hotmail.com
                heraklesantonio@gmail.com
                camp@usp.br
                ctakata@usp.br
                mereba480@gmail.com
                jjmkisakye@gmail.com
                agapituskato@gmail.com
                carlos.jared@butantan.gov.br
                mmgteix@icb.usp.br
                erney@usp.br
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                14 May 2019
                14 May 2019
                2019
                : 12
                : 225
                Affiliations
                [1 ]ISNI 0000 0004 1937 0722, GRID grid.11899.38, Department of Parasitology, Institute of Biomedical Sciences, , University of São Paulo, ; São Paulo, SP Brazil
                [2 ]ISNI 0000 0001 2163 5978, GRID grid.412352.3, Biological Institute, , Federal University of Mato Grosso do Sul, ; Campo Grande, Mato Grosso do Sul Brazil
                [3 ]Department of Environment, Arcadis, São Paulo, Brazil
                [4 ]Instituto Nacional de Ciência e Tecnologia, EpiAmo, Porto Velho, Rondônia Brazil
                [5 ]ISNI 0000 0000 8953 2273, GRID grid.192268.6, Department of Veterinary Medicine, , Hawassa University, ; Hawassa, Ethiopia
                [6 ]ISNI 0000 0004 0620 0548, GRID grid.11194.3c, Department of Zoology, Entomology and Fisheries Sciences, , Makerere University, ; Kampala, Uganda
                [7 ]ISNI 0000 0004 1790 6116, GRID grid.415861.f, Uganda Virus Research Institute, ; Entebbe, Uganda
                [8 ]ISNI 0000 0004 0615 8175, GRID grid.419716.c, Instituto Butantan, , Secretaria da Saúde, ; São Paulo, Brazil
                Article
                3463
                10.1186/s13071-019-3463-2
                6515670
                31088523
                1e147ab4-6bb9-463f-873d-b767ccc6c45d
                © The Author(s) 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 4 October 2018
                : 29 April 2019
                Funding
                Funded by: FAPESP
                Award ID: 2016/07487-0)
                Award Recipient :
                Funded by: CNPq-PROAFRICA
                Funded by: Instituto Nacional de Ciência e Tecnologia
                Award ID: EpiAmo
                Award Recipient :
                Funded by: CAPES (BR)
                Award ID: PNIPB
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Parasitology
                tabanids,tsetse flies,crocodile,caiman,evolution,taxonomy,morphology,transoceanic dispersal
                Parasitology
                tabanids, tsetse flies, crocodile, caiman, evolution, taxonomy, morphology, transoceanic dispersal

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