New insights into the evolution of the Trypanosoma cruzi clade provided by a new trypanosome species tightly linked to Neotropical Pteronotus bats and related to an Australian lineage of trypanosomes.

Luciana Lima,Oneida Espinosa-Álvarez,Julio C Carranza,Burton K Lim,Erney P Camargo,Manzelio Cavazzana,Carmen S A Takata,Ana Carolina Pavan,Patrick B Hamilton,Marta M G Teixeira,Marta Campaner,C Miguel Pinto

doi:10.1186/s13071-015-1255-x

Abstract

BackgroundBat trypanosomes are implicated in the evolution of the T. cruzi clade, which harbours most African, European and American trypanosomes from bats and other trypanosomes from African, Australian and American terrestrial mammals, including T. cruzi and T. rangeli, the agents of the American human trypanosomiasis. The diversity of bat trypanosomes globally is still poorly understood, and the common ancestor, geographical origin, and evolution of species within the T. cruzi clade remain largely unresolved.MethodsTrypanosome sequences were obtained from cultured parasites and from museum archived liver/blood samples of bats captured from Guatemala (Central America) to the Brazilian Atlantic Coast. Phylogenies were inferred using Small Subunit (SSU) rRNA, glycosomal glyceraldehyde phosphate dehydrogenase (gGAPDH), and Spliced Leader (SL) RNA genes.ResultsHere, we described Trypanosoma wauwau n. sp. from Pteronotus bats (Mormoopidae) placed in the T. cruzi clade, then supporting the bat-seeding hypothesis whereby the common ancestor of this clade likely was a bat trypanosome. T. wauwau was sister to the clade T. spp-Neobats from phyllostomid bats forming an assemblage of trypanosome species exclusively of Noctilionoidea Neotropical bats, which was sister to an Australian clade of trypanosomes from indigenous marsupials and rodents, which possibly evolved from a bat trypanosome. T. wauwau was found in 26.5 % of the Pteronotus bats examined, and phylogeographical analysis evidenced the wide geographical range of this species. To date, this species was not detected in other bats, including those that were sympatric or shared shelters with Pteronotus. T. wauwau did not develop within mammalian cells, and was not infective to Balb/c mice or to triatomine vectors of T. cruzi and T. rangeli.ConclusionsTrypanosoma wauwau n. sp. was linked to Pteronotus bats. The positioning of the clade T. wauwau/T.spp-Neobats as the most basal Neotropical bat trypanosomes and closely related to an Australian lineage of trypanosomes provides additional evidence that the T. cruzi clade trypanosomes likely evolved from bats, and were dispersed in bats within and between continents from ancient to unexpectedly recent times.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-015-1255-x) contains supplementary material, which is available to authorized users.

Highlights

Bat trypanosomes are implicated in the evolution of the T. cruzi clade, which harbours most African, European and American trypanosomes from bats and other trypanosomes from African, Australian and American terrestrial mammals, including T. cruzi and T. rangeli, the agents of the American human trypanosomiasis
The positioning of the clade T. wauwau/ T.spp-Neobats as the most basal Neotropical bat trypanosomes and closely related to an Australian lineage of trypanosomes provides additional evidence that the T. cruzi clade trypanosomes likely evolved from bats, and were dispersed in bats within and between continents from ancient to unexpectedly recent times
Surveys by haemoculture and isolation in culture of trypanosomes from Pteronotus spp During the surveys of trypanosomes carried out from 2001 to 2009 in the state of Rondonia, 83 Pteronotus bats were captured, and the haemoculture (HE) analysis yielded a general prevalence of ~35 %, resulting in 29 cultures of trypanosomes obtained from P. parnellii (25), P. personatus (2) and P. gymnonotus (2) (Table 1)

Summary

Introduction

Bat trypanosomes are implicated in the evolution of the T. cruzi clade, which harbours most African, European and American trypanosomes from bats and other trypanosomes from African, Australian and American terrestrial mammals, including T. cruzi and T. rangeli, the agents of the American human trypanosomiasis. This clade was formed mainly by trypanosomes of bats, and some other mammalian hosts in the Americas, Africa and Australia It was proposed the bat-seeding hypothesis, in which a common ancestor bat trypanosome gave origin (speciation) to several trypanosomes that evolved linked to bats or have switched, by several independent events at different times, into a range of terrestrial mammals in the New and Old Worlds, originating several lineages (monophyletic assemblages) of bat trypanosomes [1,2,3,4,5]. The lineage of Australian trypanosomes from marsupials and rodents were basal to these lineages [1, 3, 4, 10]

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