MonomorphicTrypanozoon: towards reconciling phylogeny and pathologies
Authors: Oldrieve Guy , Verney Mylène , Jaron Kamil S. , Hébert Laurent , Matthews Keith 
Published: April 2021

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Trypanosoma brucei evansiandTrypanosoma brucei equiperdumare animal infective trypanosomes conventionally classified by their clinical disease presentation, mode of transmission, host range, kDNA composition and geographic distribution. Unlike other members of the subgenusTrypanozoon, they are non-tsetse transmitted and predominantly morphologically uniform (monomorphic) in their mammalian host. Their classification as independent species or subspecies has been long debated and genomic studies have found that isolates withinT. b. evansiandT. b. equiperdumhave polyphyletic origins. Since current taxonomy does not fully acknowledge these polyphyletic relationships, we re-analysed publicly available genomic data to carefully define each clade of monomorphic trypanosome. This allowed us to identify, and account for, lineage specific variation. We included a recently published isolate, IVM-t1, which was originally isolated from the genital mucosa of a horse with dourine and typed asT. equiperdum. Our analyses corroborate previous studies in identifying at least four distinct monomorphicT. bruceiclades. We also found clear lineage specific variation in the selection efficacy and heterozygosity of the monomorphic lineages, supporting their distinct evolutionary histories. The inferred evolutionary position of IVM-t1 suggests its reassignment to theT. b. evansitype B clade, challenging the relationship between theTrypanozoonspecies, the infected host, mode of transmission and the associated pathological phenotype. The analysis of IVM-t1 also provides the first evidence of the expansion ofT. b. evansitype B, or a 5thmonomorphic lineage represented by IVM-t1, outside of Africa, with important possible implications for disease diagnosis.

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Impact statement

Trypanosoma bruceiare unicellular parasites typically transmitted by tsetse flies. Subspecies ofT. bruceicause human African trypanosomiasis and the animal diseases, nagana, surra and dourine.T. b. evansiandT. b. equiperdumhave branched fromT. bruceiand, by foregoing tsetse transmission, expanded their geographic range beyond the sub-Saharan tsetse belt. These species can only reproduce asexually and exhibit morphological uniformity in their host (‘monomorphism’).T. b. evansiandT. b. equiperdumhave historically been classified based on fragmentary information on the parasites’ transmission routes, geographic distribution, kDNA composition and disease phenotypes. Our analysis of genome sequencing data from monomorphicT. bruceisupports at least four independent origins with distinct evolutionary histories. One isolate, IVM-t1, typed asT. equiperdum, is a closer relative toT. b. evansi, highlighting the risk of using pathognomonic descriptors for subspecies assignment. We show clear lineage specific variation in the selection efficacy in monomorphicT. brucei. Using the evolutionary relationships between lineages, we suggest it would be beneficial to reconcile phylogeny and pathology in monomorphic trypanosomes.

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Data summary

The data used in this study is available from the Sequence Read Archive or the Wellcome Sanger Institute. The accessions can be found in Supplementary file 1.