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

Roy N. Platt, Winka Le Clec'h, Frédéric D. Chevalier, Marina McDew-White, Philip T. LoVerde, Rafael Ramiro de Assis, Guilherme Oliveira, Safari Kinung'hi, Amadou Garba Djirmay, Michelle L. Steinauer, Anouk Gouvras, Muriel Rabone, Fiona Allan, Bonnie L. Webster, Joanne P. Webster, Aidan M. Emery, David Rollinson, Timothy J.C. Anderson

Research output: Contribution to journalArticlepeer-review

8 Scopus citations

Abstract

Schistosoma mansoni, a snail-borne, 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 South American Biomphalaria spp. snails would result in population bottlenecks and strong signatures of selection. We scored 475,081 single nucleotide variants 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? (iii) What were the source populations for colonizing parasites? We found a 2.4- to 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 populations from central African regions between Benin and Angola, with contributions from Niger, are probably 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 pre-adapted to the Americas and able to establish with relative ease.

Original languageEnglish (US)
Pages (from-to)2242-2263
Number of pages22
JournalMolecular Ecology
Volume31
Issue number8
DOIs
StatePublished - Apr 2022
Externally publishedYes

Keywords

  • Africa
  • Brazil
  • codispersal
  • exome
  • human parasite
  • migration

ASJC Scopus subject areas

  • Genetics
  • Ecology, Evolution, Behavior and Systematics

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