Human Migration and the Spread of the Nematode Parasite Wuchereria bancrofti

The human disease lymphatic filariasis causes the debilitating effects of elephantiasis and hydrocele. Lymphatic filariasis currently affects the lives of 90 million people in 52 countries. There are three nematodes that cause lymphatic filariasis, Brugia malayi, B. timori, and Wuchereria bancrofti, but 90% of all cases of lymphatic filariasis are caused solely by W. bancrofti. Here we use population genomics to identify the geographic origin of W. bancrofti and reconstruct its spread. Previous genomic sequencing efforts have suffered from difficulties in obtaining Wb DNA. We used selective whole genome amplification to enrich W. bancrofti DNA from infected blood samples and were able to analyze 47 whole genomes of W. bancrofti from endemic locations in Haiti, Mali, Kenya, and Papua New Guinea. Our results are consistent with a Southeast Asia or East Asia origin for W. bancrofti spread around the globe by infecting migrating populations of humans. Austronesians probably introduced W. bancrofti to Madagascar where later migrations moved it to continental Africa. From Africa, W. bancrofti spread to the New World during the transatlantic slave trade. The greater genetic diversity of W. bancrofti populations from Haiti are also consistent with genetic admixture from multiple source populations. Genome scans for locally adapted haplotypes identified genes associated with human immune suppression and insecticide sensitivity. Locally adapted haplotypes may provide a foundation to understand the distribution of W. bancrofti compared to that of other filarial nematodes and how populations may differ in response to eradication efforts.