Ecological host fitting of Trypanosoma cruziTcI in Bolivia: mosaic population structure, hybridization and a role for humans in Andean parasite dispersal

Messenger, L.A., Garcia, L., Vanhove, M., Huaranca, C., Bustamante, M., Torrico, M., Torrico, F., Miles, M.A. and Llewellyn, M.S. (2015) Ecological host fitting of Trypanosoma cruziTcI in Bolivia: mosaic population structure, hybridization and a role for humans in Andean parasite dispersal. Molecular Ecology, 24(10), pp. 2406-2422. (doi: 10.1111/mec.13186) (PMID:25847086)

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Abstract

An improved understanding of how a parasite species exploits its genetic repertoire to colonize novel hosts and environmental niches is crucial to establish the epidemiological risk associated with emergent pathogenic genotypes. Trypanosoma cruzi, a genetically heterogeneous, multi-host zoonosis, provides an ideal system to examine the sylvatic diversification of parasitic protozoa. In Bolivia, T. cruzi I, the oldest and most widespread genetic lineage, is pervasive across a range of ecological clines. High-resolution nuclear (26 loci) and mitochondrial (10 loci) genotyping of 199 contemporaneous sylvatic TcI clones was undertaken to provide insights into the biogeographical basis of T. cruzi evolution. Three distinct sylvatic parasite transmission cycles were identified: one highland population among terrestrial rodent and triatomine species, composed of genetically homogenous strains (Ar = 2.95; PA/L = 0.61; DAS = 0.151), and two highly diverse, parasite assemblages circulating among predominantly arboreal mammals and vectors in the lowlands (Ar = 3.40 and 3.93; PA/L = 1.12 and 0.60; DAS = 0.425 and 0.311, respectively). Very limited gene flow between neighbouring terrestrial highland and arboreal lowland areas (distance ~220 km; FST = 0.42 and 0.35) but strong connectivity between ecologically similar but geographically disparate terrestrial highland ecotopes (distance >465 km; FST = 0.016–0.084) strongly supports ecological host fitting as the predominant mechanism of parasite diversification. Dissimilar heterozygosity estimates (excess in highlands, deficit in lowlands) and mitochondrial introgression among lowland strains may indicate fundamental differences in mating strategies between populations. Finally, accelerated parasite dissemination between densely populated, highland areas, compared to uninhabited lowland foci, likely reflects passive, long-range anthroponotic dispersal. The impact of humans on the risk of epizootic Chagas disease transmission in Bolivia is discussed.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Llewellyn, Professor Martin
Authors: Messenger, L.A., Garcia, L., Vanhove, M., Huaranca, C., Bustamante, M., Torrico, M., Torrico, F., Miles, M.A., and Llewellyn, M.S.
College/School:College of Medical Veterinary and Life Sciences > School of Medicine, Dentistry & Nursing
Journal Name:Molecular Ecology
Publisher:Wiley-Blackwell Publishing Ltd.
ISSN:0962-1083
ISSN (Online):1365-294X
Copyright Holders:Copyright © 2015 The Authors
First Published:First published in Molecular Ecology 24(10):2406-2422
Publisher Policy:Reproduced under a Creative Commons License

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