Genomic analysis of a parasite invasion: colonization of the Americas by the blood fluke, Schistosoma mansoni

Roy N. Platt II*¹, Winka Le Clec'h*¹, Frédéric D. Chevalier*¹, Marina McDew-White¹, Philip T. LoVerde², Rafael R. de Assis³, Guilherme Oliveira^3,4, Safari Kinunghi⁵, Amadou Garba Djirmay⁶, Michelle L. Steinauer⁷, Anouk Gouvras⁸, Muriel Rabone⁸, Fiona Allan^9,10, Bonnie L. Webster^8,10, Joanne P. Webster⁹, Aidan Emery^8,10, David Rollinson^8,10, Timothy J. C. Anderson¹

¹Texas Biomedical Research Institute, San Antonio, San Antonio, TX, United States

²University of Texas Health Science Center, San Antonio, San Antonio, TX, United States

³Centro de Pesquisas René Rachou - Fiocruz/MG, Belo Horizonte, Brazil

⁴Instituto Tecnológico Vale, Belém, Brazil

⁵National Institute for Medical Research, Mwanza, Tanzania

⁶Réseau International Schistosomiases Environnemental Aménagement et Lutte (RISEAL), Niamey, Niger

⁷Western University of Heath Sciences, Corvallis, OR, United States

⁸Natural History Museum, London, United Kingdom

⁹Imperial College, London, United Kingdom

¹⁰London Centre for Neglected Tropical Disease Research (LCNTDR)

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.