Isolation of Novel Trypanosomatid, Zelonia australiensis sp. nov. (Kinetoplastida: Trypanosomatidae) Provides Support for a Gondwanan Origin of Dixenous Parasitism in the Leishmaniinae

Abstract

The genus Leishmania includes approximately 53 species, 20 of which cause human leishmaniais; a significant albeit neglected tropical disease. Leishmaniasis has afflicted humans for millennia, but how ancient is Leishmania and where did it arise? These questions have been hotly debated for decades and several theories have been proposed. One theory suggests Leishmania originated in the Palearctic, and dispersed to the New World via the Bering land bridge. Others propose that Leishmania evolved in the Neotropics. The Multiple Origins theory suggests that separation of certain Old World and New World species occurred due to the opening of the Atlantic Ocean. Some suggest that the ancestor of the dixenous genera Leishmania, Endotrypanum and Porcisia evolved on Gondwana between 90 and 140 million years ago. In the present study a detailed molecular and morphological characterisation was performed on a novel Australian trypanosomatid following its isolation in Australia’s tropics from the native black fly, Simulium ( Morops) dycei Colbo, 1976. Phylogenetic analyses were conducted and confirmed this parasite as a sibling to Zelonia costaricensis, a close relative of Leishmania previously isolated from a reduviid bug in Costa Rica. Consequently, this parasite was assigned the name Zelonia australiensis sp. nov. Assuming Z. costaricensis and Z. australiensis diverged when Australia and South America became completely separated, their divergence occurred between 36 and 41 million years ago at least. Using this vicariance event as a calibration point for a phylogenetic time tree, the common ancestor of the dixenous genera Leishmania, Endotrypanum and Porcisia appeared in Gondwana approximately 91 million years ago. Ultimately, this study contributes to our understanding of trypanosomatid diversity, and of Leishmania origins by providing support for a Gondwanan origin of dixenous parasitism in the Leishmaniinae.

Author Summary

The genus Leishmania includes approximately 53 species, 20 of which cause human leishmaniais, a significant disease that has afflicted humans for millennia. But how ancient is Leishmania and where did it arise? Some suggest Leishmania originated in the Palearctic. Others suggest it appeared in the Neotropics. The Multiple Origins theory proposes that separation of certain Old World and Neotropical species occurred following the opening of the Atlantic. Others suggest that an ancestor to the Euleishmania and Paraleishmania appeared on Gondwana 90 to 140 million years ago (MYA). We performed a detailed molecular and morphological characterisation of a novel Australian trypanosomatid. This parasite is a sibling to the Neotropical Zelonia costaricensis, a close relative of Leishmania, and designated as Zelonia australiensis sp. nov. Assuming Z. costaricensis and Z. australiensis split when Australia and South America separated, their divergence occurred between 36 and 41 MYA. Using this event as a calibration point for a phylogenetic time tree, an ancestor of the dixenous Leishmaniinae appeared in Gondwana ~ 91 MYA. This study contributes to our understanding of trypanosomatid diversity by describing a unique Australian trypanosomatid and to our understanding of Leishmania evolution by inferring a Gondwanan origin for dixenous parasitism in the Leishmaniinae.