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. 2019 Sep 1;36(9):1931-1941.
doi: 10.1093/molbev/msz116.

Human Migration and the Spread of the Nematode Parasite Wuchereria bancrofti

Scott T Small  1   2 , Frédéric Labbé  1 , Yaya I Coulibaly  3 , Thomas B Nutman  4 , Christopher L King  5 , David Serre  6 , Peter A Zimmerman  5   7
Affiliations

Human Migration and the Spread of the Nematode Parasite Wuchereria bancrofti

Scott T Small et al. Mol Biol Evol. .

Abstract

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, Brugia timori, and Wuchereria bancrofti, but 90% of all cases of lymphatic filariasis are caused solely by W. bancrofti (Wb). Here we use population genomics to reconstruct the probable route and timing of migration of Wb strains that currently infect Africa, Haiti, and Papua New Guinea (PNG). We used selective whole genome amplification to sequence 42 whole genomes of single Wb worms from populations in Haiti, Mali, Kenya, and PNG. Our results are consistent with a hypothesis of an Island Southeast Asia or East Asian origin of Wb. Our demographic models support divergence times that correlate with the migration of human populations. We hypothesize that PNG was infected at two separate times, first by the Melanesians and later by the migrating Austronesians. The migrating Austronesians also likely introduced Wb to Madagascar where later migrations spread it to continental Africa. From Africa, Wb spread to the New World during the transatlantic slave trade. Genome scans identified 17 genes that were highly differentiated among Wb populations. Among these are genes associated with human immune suppression, insecticide sensitivity, and proposed drug targets. Identifying the distribution of genetic diversity in Wb populations and selection forces acting on the genome will build a foundation to test future hypotheses and help predict response to current eradication efforts.

Keywords: genomics; parasite; population genetics.

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Figures

<sc>Fig</sc>. 1.
Fig. 1.
Genetic structure and ancestry among Wuchereria bancrofti populations. (A) PCA of 10,000 SNPs across the genome after removing sites in high LD. Principal component (PC) 1 separates Haiti (green), Mali (orange), Kenya (red) from the population of Papua New Guinea (blue). PC 2 separates Kenya, Mali, and Haiti. Percent variation explained by each component is summarized in the bar plot (inset). (B) Coancestry matrix (a summary of nearest neighbor haplotype relationships in the data set) of Wb populations using fineSTRUCTURE. Dendrograms relating individuals to the coancestry matrix are along the vertical axis with populations denoted by colors corresponding to PCA. Cooler colors represent higher coancestry. Fused boxes of similar color denote worms sampled from the same host infection. A plot with individual sample labels on the vertical axis is available in supplementary figure S3 (Supplementary Material online). (C) Whole genome SNP phylogeny using SNPhylo highlights that individuals from the same population are monophyletic. Support is shown for bootstrap values greater than 70.
<sc>Fig</sc>. 2.
Fig. 2.
Demographic history of Wuchereria bancrofti. (A) Map representing potential routes of Wb dispersal highlighting sampled populations and shared ancestry: Haiti (green), Mali (orange), Kenya (red), Papua New Guinea (blue). Pink colors represent unsampled and thus inferred population ancestry connecting Wb populations (color figure available online). (B) Reconstruction of change in effective population size for each Wb population using MSMC2 and PopSizeABC. Thinner shaped lines of same shape represent 95% confidence intervals for the effective population sizes.
<sc>Fig</sc>. 3.
Fig. 3.
Manhattan plot of local adaptation in Wuchereria bancrofti. Results of selection scan using hapFLK. Scaffolds are listed along the horizontal axis alternating between black and gray for contrast. The horizontal line represents an FDR of 10%. Outlier regions above the line were annotated and examined for gene function and presented in table 2.
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