Phylogenetic characterization of the pork tapeworm Taenia solium in Japan: implications for the enigmatic evolutionary history

Abstract

Taenia solium is a tapeworm of the family Taeniidae that causes neurocysticercosis, a serious zoonotic disease in humans. Its life cycle involves pigs and wild boars as intermediate hosts and humans as the sole definitive host. Since poor sanitation and free-roaming pigs contribute to maintaining its life cycle, cysticercosis is endemic in developing countries across Asia, Africa, and Latin America, while local transmission is generally absent in developed countries. However, we unexpectedly identified three cases of cysticercosis in wild boars in Japan between 2014 and 2023. Genetic analyses were performed on six cysticerci collected from two wild boars independently captured in 2023. Phylogenetic analysis using three nuclear DNA markers confirmed that the cysticerci were indeed T. solium. Mitogenome sequencing from these cysticerci yielded six complete mitogenomes, each 13,712 bp in length and identical to each other. Haplotype network analysis using mitochondrial cox1 and cob sequences revealed that the cysticerci in Japan possess a haplotype distinct from haplogroups in other endemic regions, i.e., haplogroups in Asia, Africa/America, and Bhutan, indicating that the T. solium population is divided into at least four haplogroups. Subsequent phylogenetic inference from the mitochondrial 12 protein-coding genes demonstrated that the Japanese haplotype diverged from both the Asian and African/American haplogroups before the divergence of these two major haplogroups in the Early to Middle Pleistocene. Our findings indicate that the T. solium life cycle can be maintained in regions generally considered non-endemic, highlighting an overlooked risk of local transmission in developed countries. Furthermore, the genetic diversity and phylogenetic relationships revealed in this study may provide evidence for revisiting the “Out of Africa” hypothesis for T. solium. Comprehensive mitogenomic analyses based on additional specimens would hold the key to unraveling the evolutionary history of this tapeworm, which currently uses humans as its sole definitive host.