The remarkable journey of adaptation of the Plasmodium falciparum malaria parasite to New World anopheline mosquitoes

Abstract

Plasmodium falciparum originated in Africa, dispersed around the world as a result of human migration and had to adapt to several different indigenous anopheline mosquitoes. Anophelines from the New World are evolutionary distant form African ones and this probably resulted in a more stringent selection of Plasmodium as it adapted to these vectors. It is thought that Plasmodium has been genetically selected by some anopheline species through unknown mechanisms. The mosquito immune system can greatly limit infection and P. falciparum evolved a strategy to evade these responses, at least in part mediated by Pfs47, a highly polymorphic gene. We propose that adaptation of P. falciparum to new vectors may require evasion of their immune system. Parasites with a Pfs47 haplotype compatible with the indigenous mosquito vector would be able to survive and be transmitted. The mosquito antiplasmodial response could be an important determinant of P. falciparum population structure and could affect malaria transmission in the Americas.

Mosquito Vectors and the Globalization of Plasmodium falciparum Malaria

“…The parasite genetic diversity in South America is far less than would be expected in light of the more than 7 million African slaves imported (22,112), which suggests that many of the parasite lineages that arrived in the Americas failed to persist. For example, selection of parasites with a compatible Pfs47 haplotype by New World vectors could have decreased the genetic diversity of P. falciparum in the Americas (53). This hypothesis is supported by the strong geographic differentiation of Pfs47 haplotypes between the Americas and the African (F ST = 0.754) and Asian (F ST = 0.876) continents.…”

Plasmodium P47 : a key gene for malaria transmission by mosquito vectors

“…Plasmodium falciparum and Plasmodium vivax are the most prevalent agents of human malaria and are transmitted by anopheline mosquitoes. While Plasmodium parasites have a rather restricted vertebrate host range, they have adapted to at least 70 different mosquito species [2], many of them evolutionarily distant from vectors in Africa, where human malarias originated [3,4]. …”

Plasmodium evasion of mosquito immunity and global malaria transmission: The lock-and-key theory

“…For example, anophelines of the subgenus Nyssorhynchus (malaria vectors in Central and South America, such as Anopheles albimanus) diverged from the subgenus Cellia (malaria vectors in Africa, India, and South Asia) about 100 Mya (4). P. falciparum parasites are transmitted by more than 70 different anopheline species worldwide (3), but compatibilities differ between specific vector-parasite combinations (5). For example, P. falciparum NF54 (Pf NF54), of putative African origin, effectively infects Anopheles gambiae, the main malaria vector in sub-Saharan Africa; but A. albimanus is highly refractory to this strain (6)(7)(8); whereas Asian P. falciparum isolates infect Anopheles stephensi (Nijmegen strain), a major vector in India, more effectively than A. gambiae (9).…”