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

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.

Figure 1. Mitochondrial genotypes of T. solium in Madagascar.

(A) Pie charts illustrating the frequencies of the Asian and Afro-American mitochondrial genotypes of T. solium in each collection site. The numbers in the charts show the sample size for parasite isolates examined. Madagascar is divided into the 7 former provinces. (B) The haplotype network of concatenated mtDNA gene sequences. The size of the ellipses is roughly proportional to the haplotype frequency, and the actual numbers of haplotypes (>1) are enclosed in parentheses.