Schistosoma mansoni, a snail-vectored, blood fluke that infects humans, was introduced into the Americas from Africa during the Trans-Atlantic slave trade. As this parasite shows strong specificity to the snail intermediate host, we expected that adaptation to S. American Biomphalaria spp. snails would result in population bottlenecks and strong signatures of selection. We scored 475,081 single nucleotide variants (SNVs) in 143 S. mansoni from the Americas (Brazil, Guadeloupe, and Puerto Rico) and Africa (Cameroon, Niger, Senegal, Tanzania, and Uganda), and used these data to ask: (i) Was there a population bottleneck during colonization? (ii) Can we identify signatures of selection associated with colonization? And (iii) what were the source populations for colonizing parasites? We found a 2.4-2.9-fold reduction in diversity and much slower decay in linkage disequilibrium (LD) in parasites from East to West Africa. However, we observed similar nuclear diversity and LD in West Africa and Brazil, suggesting no strong bottlenecks and limited barriers to colonization. We identified five genome regions showing selection in the Americas, compared with three in West Africa and none in East Africa, which we speculate may reflect adaptation during colonization. Finally, we infer that unsampled African populations from central African regions between Benin and Angola, with contributions from Niger, are likely the major source(s) for Brazilian S. mansoni. The absence of a bottleneck suggests that this is a rare case of a serendipitous invasion, where S. mansoni parasites were preadapted to the Americas and were able to establish with relative ease.

We examined published exomic and genomic data from 178 individual Schistosoma samples/isolates, from multiple geographical locations, available from three studies (Berriman et al., 2009; Chevalier et al., 2019; Crellen et al., 2016). All exome data is from Chevalier et al. (2016) and Chevalier et al. (2019). These data were generated from individual larval miracidia hatched from S. mansoni eggs and preserved on FTA cards. Exome libraries were generated via whole genome amplification followed by targeted capture of the exome (Le Clec'h et al., 2018). This method specifically targets 95% (14.81 Mb) of the exome with 2x tiled probes. The whole genome sequence data came from adult worms cultured through laboratory rodents and snails for two or more generations before whole genome library prep and sequencing (Berriman et al., 2009; Crellen et al., 2016; International Helminth Genomes Consortium, 2019).