Genetics of the pig tapeworm in Madagascar reveal a history of human dispersal and colonization

Authors: YANAGIDA, TETSUYA - Asahikawa Medical College; CAROD, JEAN-FRANCOIS - Pasteur Institute Of Madagascar; SAKO, YASUHIKO - Asahikawa Medical College; NAKAO, MINORU - Asahikawa Medical College; Hoberg, Eric; ITO, AKIRA - Asahikawa Medical College

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/19/2014
Publication Date: 10/18/2014
Publication URL: http://doi:10.1371/journal.pone.0109002
Citation: Yanagida, T., Carod, J., Sako, Y., Nakao, M., Hoberg, E.P., Ito, A. 2014. Genetics of the pig tapeworm in Madagascar reveal a history of human dispersal and colonization. PLoS One. 9(10):e109003.

Interpretive Summary: Tapeworms are ubiquitous parasites among vertebrates globally, and some including those in the genus Taenia are important for people and our food animals. Understanding the distribution of these parasite and the potential for disease depends on knowledge of the history of association between humans and these tapeworms. We contribute to a broadening understanding of these infections based on genetic studies of parasites in Madagascar. An intricate history of human dispersal and geographic colonization has strongly affected the distribution of obligate parasites circulating among people. Understanding history and patterns of distribution is a cornerstone in defining the potential for disease attributed to parasites. Among these parasites, the pig tapeworm Taenia solium occurs throughout the world as the causative agent of cysticercosis, one of the most serious neglected tropical diseases. Differences in the manifestation of disease are linked to distinct genetic lineages of T. solium in Asia and Africa/Latin America; but only in Madagascar are both lineages codistributed. Aside from defining the geography of disease parasites also reveal important insights about the history of human dispersal and occupation around the globe. Linguistic, archaeological and genetic evidence has indicated that the people in Madagascar have mixed ancestry from Island Southeast Asia and from East Africa. Hence, anthropogenic (human related) introduction of the tapeworm from Southeast Asia and Africa had been postulated. In the present study, we show that T. solium obtained in Madagascar is closely related to those from the Indian subcontinent. Parasitological evidence presented in this study and human genetics support the hypothesis of an Indian influence on Malagasy culture coinciding with periods of early human migration into Madagascar. Analyses on genetic and geographic populations of T. solium in Madagascar will shed light on rapid evolution of this organism driven by recent (<2000 yr) human migrations, following tens of thousands of years of geographic isolation. Our study is of significance globally to disease ecologists, parasitologists and epidemiologists in providing a deeper understanding of processes for geographic dispersal for this parasite which can contribute to ongoing programs for control.

Technical Abstract: An intricate history of human dispersal and geographic colonization has strongly affected the distribution of obligate parasites circulating among people. Among these parasites, 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 both lineages codistributed. Linguistic, archaeological and genetic evidence has indicated that the people in Madagascar have mixed ancestry from Island Southeast Asia and from East Africa. Hence, anthropogenic introduction of the tapeworm from Southeast Asia and Africa had been postulated. In the present study, we show that the major mitochondrial haplotype of T. solium obtained in Madagascar is closely related to those from the Indian subcontinent. Parasitological evidence presented in this study and human mitochondrial genetics previously reported support the hypothesis of an Indian influence on Malagasy culture coinciding with periods of early human migration into Madagascar. We also found evidence of single tapeworms showing nuclear-mitochondrial discordance indicating unexpected cross-fertilization between the two lineages of T. solium. Analyses on genetic and geographic populations of T. solium in Madagascar will shed light on rapid evolution of this organism driven by recent (<2000 yr) human migrations, following tens of thousands of years of geographic isolation.