Abstract
We examined the mitogenomes of a large global collection of human malaria parasites to explore how and when Plasmodium falciparum and P. vivax entered the Americas. We found evidence of a significant contribution of African and South Asian lineages to present-day New World malaria parasites with additional P. vivax lineages appearing to originate from Melanesia that were putatively carried by the Australasian peoples who contributed genes to Native Americans. Importantly, mitochondrial lineages of the P. vivax-like species P. simium are shared by platyrrhine monkeys and humans in the Atlantic Forest ecosystem, but not across the Amazon, which most likely resulted from one or a few recent human-to-monkey transfers. While enslaved Africans were likely the main carriers of P. falciparum mitochondrial lineages into the Americas after the conquest, additional parasites carried by Australasian peoples in pre-Columbian times may have contributed to the extensive diversity of extant local populations of P. vivax.
Highlights
The Americas were the last continent to be settled by modern humans
We identified 330 single-nucleotide polymorphisms (SNPs) and 325 unique haplotypes in 1,795 mitogenomes from six regional P. falciparum populations, namely, populations in Africa (AFR), South America (SAM), Central America (CAM), South Asia (SOA), Southeast Asia (SEA), and Melanesia (MEL)
The relative genetic proximity between SAM and AFR mitochondrial lineages compared with those from other regions suggests that AFR is a major source of extant South American populations of P. falciparum
Summary
The Americas were the last continent to be settled by modern humans. Approximately 15,000 years ago, the first Americans crossed the land bridge that connected Siberia to Alaska in the late Pleistocene. The precise date of the earliest arrival, number of founding events, and precise geographic source of peoples who migrated to the New World remain uncertain[1] These early migrants are unlikely to have carried malaria parasites through the cold and arid route to Alaska[2,3]. How and when the less deadly species P. vivax arrived in the New World remains controversial This parasite was endemic to southern Europe until the mid-1900s9,10, but it was rare in West and Central Africa, the origin of most enslaved peoples displaced to the Americas. We search for signatures of ancestral source populations in isolates of P. falciparum and P. vivax currently circulating in the Americas and of a P. vivax-like species, P. simium, which infects platyrrhine monkeys of the Atlantic Forest of South and Southeast Brazil. Because of the low diversity of P. simium lineages circulating in monkeys and humans in the Atlantic Forest ecosystem compared with P. vivax strains from across the country, we argue for a recent human-to-monkey transfer of these P. vivax-like parasites
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