Comparative phylogeography of Trypanosoma rangeli and Rhodnius (Hemiptera: Reduviidae) supports a long coexistence of parasite lineages and their sympatric vectors

Abstract

To make reliable interpretations about evolutionary relationships between Trypanosoma rangeli lineages and their insect vectors (triatomine bugs of the genus Rhodnius ) and, thus, about the determinant factors of lineage segregation within T. rangeli , we compared phylogenies of parasite isolates and vector species. Sixty-one T. rangeli isolates from invertebrate and vertebrate hosts were initially evaluated in terms of polymorphism of the spliced-leader gene (SL). Further analysis based on SL and SSUrRNA sequences from 33 selected isolates, representative of the overall phylogenetic diversity and geographical range of T. rangeli , supported four phylogenetic lineages within this species. By comparing the phylogeny of Rhodnius species with that inferred for T. rangeli isolates and through analysis of the geographical range of the isolates, we showed that there is a very significant overlap in the distribution of Rhodnius species and T. rangeli lineages. Congruence between phylogeographical analysis of both T. rangeli lineages and complexes of Rhodnius species are consistent with the hypothesis of a long coexistence of parasites and their vectors, with lineage divergence associated with sympatric species of Rhodnius apparently without association with particular vertebrate hosts. Separation of T. rangeli isolates from vectors of distinct complexes living in sympatry favours the absence of gene flow between the lineages and suggests evolution of T. rangeli lineages in independent transmission cycles, probably associated to specific Rhodnius spp. ecotopes. A polymerase chain reaction assay based on SL intergenic sequences was developed for simultaneous identification and lineage genotyping of T. rangeli in epidemiological surveys.Keywords : evolution, phylogeography, Rhodnius , ribosomal gene, spliced-leader gene, Trypanosoma rangeli Received 4 March 2007; revision received 4 March 2007; accepted 12 April 2007 IntroductionThe family Trypanosomatidae (Euglenozoa: Kinetoplastida) comprises eight genera of protozoan parasites of vertebrates, invertebrates and plants. The genus Trypanosoma harbours parasites of all vertebrate classes and the life cycle of these parasites involves alternation between two hosts: vertebrates and diverse haematophagous invertebrates (vectors). This genus includes only three Trypanosoma species that infect man: T. cruzi and T. rangeli in Latin America and T. brucei in Africa (Stevens et al . 2001).Trypanosoma rangeli infects humans, and domestic, and sylvatic mammals from Central America to southern South America sharing with T. cruzi the same mammalian hosts and triatomine vectors in overlapping areas. A high & Saravia 1999;Guhl & Vallejo 2003). In Brazil, only three human cases have been reported in Amazonia (Coura et al . 1996), whereas infection of sylvatic mammals and triatomines is very common in this region (Miles et al . 1983; Maia da Silva et al . 2004a, b) and has also been reported in southern, southeastern and central regions (Steindel et al . 1991;Ramirez et al . 2002...

Susceptibilidad de diferentes especies de Rhodnius (Hemiptera, Reduviidae, Triatominae) a una cepa brasileña de Trypanosoma rangeli (SC58/KP1-)

“…Vallejo, et al (10), characterized two major lineages of T. rangeli in Latin America based on the presence or absence of a minicircle of kDNA (KP1+ and KP1-, respectively). T. rangeli presents an extensive genetic variability demonstrated by kDNA and nuclear DNA analysis (7,9,11,12). Moreover, analysis of the karyotype profiles permitted the division of the T. rangeli strains into two groups coinciding with the KP1+ and KP1− genotypes (13).…”

Genes de cisteíno proteases (Catepsina L-like) de Trypanosoma rangeli: polimorfismo, relações filogenéticas e alvos para diagnóstico e genotipagem.

“…Esse gene tem sido utilizado para diagnóstico e em estudos taxonômicos de tripanossomatídeos devido ao número de cópias e a seqüências com diferentes graus de conservação. As unidades de repetição do gene SL são constituídas por um exon de 39 nucleotídeos, altamente conservado; um intron de 50-100 nucleotídeos, moderadamente conservadoe uma região intergênica espaçadora que apresenta variações em tamanho e seqüência entre espécies e isolados de tripanossomatídeos (AGABIAN, 1990;GIBSON et al, 2000;VENTURA et al, 2001;MAIA DA SILVA et al, 2007).…”

Spliced Leader (SL) RNA: análises de genes e regiões intergênicas com aportes na filogenia, taxonomia e genotipagem de <i>Trypanosoma</i> spp. de todas as classes de vertebrados.

“…Maia da Silva et al, 2007), T. vivax (Ventura et al, 2000 e T. theileri (Rodrigues et al, 2010). A análise do polimorfismo da região intergênica tem permitido também avaliar o repertório de genótipos de uma determinada espécie, como descrito para: T. rangeli (Grisard et al, 1999;Maia da Silva et al, 2007;T.…”

“…A análise do polimorfismo da região intergênica tem permitido também avaliar o repertório de genótipos de uma determinada espécie, como descrito para: T. rangeli (Grisard et al, 1999;Maia da Silva et al, 2007;T. vivax (Ventura et al, 2000); T. theileri (Rodrigues et al, 2010;Garcia et al, 2011) e T. cruzi (Souto et al, 1996;Nunez et al, 1997;Fernandes et al, 1998Fernandes et al, , 2001Brisse et al, 2001;O'Connor et al, 2007;Herrera et al, 2009Herrera et al, , 2013Cura et al, 2010;Lima et al, 2015b).…”

“…Embora T. brucei seja a espécie mais estudada quanto à regulação da expressão do gene SL, sabe-se muito pouco sobre o repertório e estrutura dos genes SL das demais espécies de tripanossomas africanos, contando-se apenas com dados obtidos pela amplificação do gene e determinação do seu tamanho (Garside, Gibson, 1995 (Maslov et al, 1993;Gibson et al, 2000;Maia da Silva et al, 2007;Rodrigues et al, 2010;Lima et al, 2013Lima et al, , 2015a. Em espécies como T. brucei e T. cruzi, que não apresentam a associação SL-5S rRNA, os genes 5S rRNA estão organizados em tandem, enquanto que em L. major estão dispersos inteiramente no genoma e sempre associados com os genes tRNA (Martinez-Calvillo et al, 2010).…”