Abstract

An intricate history of human dispersal and geographic colonization has strongly affected the distribution of human pathogens. The pig tapeworm Taenia solium occurs throughout the world as the causative agent of cysticercosis, one of the most serious neglected tropical diseases. Discrete genetic lineages of T. solium in Asia and Africa/Latin America are geographically disjunct; only in Madagascar are they sympatric. Linguistic, archaeological and genetic evidence has indicated that the people in Madagascar have mixed ancestry from Island Southeast Asia and East Africa. Hence, anthropogenic introduction of the tapeworm from Southeast Asia and Africa had been postulated. This study shows that the major mitochondrial haplotype of T. solium in Madagascar is closely related to those from the Indian Subcontinent. Parasitological evidence presented here, and human genetics previously reported, support the hypothesis of an Indian influence on Malagasy culture coinciding with periods of early human migration onto the island. We also found evidence of nuclear-mitochondrial discordance in single tapeworms, indicating unexpected cross-fertilization between the two lineages of T. solium. Analyses of genetic and geographic populations of T. solium in Madagascar will shed light on apparently rapid evolution of this organism driven by recent (<2,000 yr) human migrations, following tens of thousands of years of geographic isolation.

Highlights

  • The pig tapeworm Taenia solium (Cestoda: Taeniidae) is an etiologic agent of cysticercosis, an important zoonosis and neglected tropical disease, and recently ranked as the most important food-borne parasites on a global scale [1]

  • Cysticercosis refers to infection of various tissues of swine or humans with cysticerci larvae due to ingestion of eggs released from people harboring adult worms in the intestine

  • Cysticercosis of the central nervous system, warrants special attention because it is a major cause of seizures and epilepsy in endemic areas [2] and can be lethal especially in remote areas of developing countries [3]

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Summary

Introduction

The pig tapeworm Taenia solium (Cestoda: Taeniidae) is an etiologic agent of cysticercosis, an important zoonosis and neglected tropical disease, and recently ranked as the most important food-borne parasites on a global scale [1]. We previously reported that T. solium can be divided into two mitochondrial (mtDNA) genetic linages, Asian and Afro-American which differ in the clinical manifestations of human cysticercosis [4]. Their distributions are geographically disjunct in Asia or Africa and Latin America [4]. Phylogenetic studies have suggested that divergence of the two lineages occurred in the Pleistocene [4,6,8] Sympatry of both mitochondrial lineages was confirmed in Madagascar [6,8]

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