Human migration and the spread of malaria parasites to the New World
Authors: Rodrigues Priscila T. , Valdivia Hugo O. , de Oliveira Thais C. , Alves João Marcelo P. , Duarte Ana Maria R. C. , Cerutti-Junior Crispim , Buery Julyana C. , Brito Cristiana F. A. , de Souza Júlio César , Hirano Zelinda Maria Braga , Malafronte Rosely S. , Ladeia-Andrade Simone , Mita Toshihiro , Santamaria Ana Maria , Calzada José E. , Kawamoto Fumihiko , Raijmakers Leonie R. J. , Mueller Ivo , Pacheco Maria A. , Escalante Ananias A. , Felger Ingrid , Ferreira Marcelo U. 
Published: May 2017

Background

The Americas were the last continent to be settled by modern humans, but how and when human malaria parasites arrived in the New World is uncertain. Here, we apply phylogenetic analysis and coalescent-based gene flow modeling to a global collection ofPlasmodium falciparumandP. vivaxmitogenomes to infer the demographic history and geographic origins of malaria parasites circulating in the Americas. Importantly, we examineP. vivaxmitogenomes from previously unsampled forest-covered sites along the Atlantic Coast of Brazil, including the vivax-like speciesP. simiumthat locally infects platyrrhini monkeys.

Results

The best-supported gene flow models are consistent with migration of both malaria parasites from Africa and South Asia to the New World, with no genetic signature of a population bottleneck upon parasite's arrival in the Americas. We found evidence of additional gene flow from Melanesia inP. vivax(but notP. falciparum)mitogenomes from the Americas and speculate that someP. vivaxlineages might have arrived with the Australasian peoples who contributed genes to Native Americans in pre-Columbian times. Mitochondrial haplotypes characterized inP. simiumfrom monkeys from the Atlantic Forest are shared by local humans. These vivax-like lineages have not spread to the Amazon Basin, are much less diverse thanP. vivaxcirculating elsewhere in Brazil, and show no close genetic relatedness withP. vivaxpopulations from other continents.

Conclusions

Enslaved peoples brought from a wide variety of African locations were major carriers ofP. falciparummitochondrial lineages into the Americas, but additional human migration waves are likely to have contributed to the extensive genetic diversity of present-day New World populations ofP. vivax. The reduced genetic diversity of vivax-like monkey parasites, compared with humanP. vivaxfrom across this country, argues for a recent human-to-monkey transfer of these lineages in the Atlantic Forest of Brazil.

Author summary

Malaria is currently endemic to the Americas, with over 400,000 laboratory-confirmed infections reported annually, but how and when human malaria parasites entered this continent remains largely unknown. To determine the geographic origins of malaria parasites currently circulating in the Americas, we examined a global collection ofPlasmodium falciparumandP. vivaxmitochondrial genomes, including those from understudied isolates ofP. vivaxandP. simium, a vivax-like species that infect platyrrhini monkeys, from the Atlantic Forest of Brazil. We found evidence of significant historical migration to the New World of malaria parasites from Africa and, to a lesser extent, South Asia, with further genetic contribution of Melanesian lineages to South AmericanP. vivaxpopulations. Importantly, mitochondrial haplotypes ofP. simiumare shared by monkeys and humans from the Atlantic Forest, most likely as a result of a recent human-to-monkey transfer. Interestingly, these potentially zoonotic lineages are not found in the Amazon Basin, the main malaria-endemic area in the Americas. We conclude that enslaved Africans were the main carriers ofP. falciparummitochondrial lineages into the Americas, whereas additional migration waves of Australasian peoples and parasites may have contributed to the genetic makeup of present-day New World populations ofP. vivax.