Population genomics reveals that an anthropophilic population of Aedes aegypti mosquitoes in West Africa recently gave rise to American and Asian populations of this major disease vector

Abstract

BackgroundThe mosquito Aedes aegypti is the main vector of dengue, Zika, chikungunya and yellow fever viruses. This major disease vector is thought to have arisen when the African subspecies Ae. aegypti formosus evolved from being zoophilic and living in forest habitats into a form that specialises on humans and resides near human population centres. The resulting domestic subspecies, Ae. aegypti aegypti, is found throughout the tropics and largely blood-feeds on humans.ResultsTo understand this transition, we have sequenced the exomes of mosquitoes collected from five populations from around the world. We found that Ae. aegypti specimens from an urban population in Senegal in West Africa were more closely related to populations in Mexico and Sri Lanka than they were to a nearby forest population. We estimate that the populations in Senegal and Mexico split just a few hundred years ago, and we found no evidence of Ae. aegypti aegypti mosquitoes migrating back to Africa from elsewhere in the tropics. The out-of-Africa migration was accompanied by a dramatic reduction in effective population size, resulting in a loss of genetic diversity and rare genetic variants.ConclusionsWe conclude that a domestic population of Ae. aegypti in Senegal and domestic populations on other continents are more closely related to each other than to other African populations. This suggests that an ancestral population of Ae. aegypti evolved to become a human specialist in Africa, giving rise to the subspecies Ae. aegypti aegypti. The descendants of this population are still found in West Africa today, and the rest of the world was colonised when mosquitoes from this population migrated out of Africa. This is the first report of an African population of Ae. aegypti aegypti mosquitoes that is closely related to Asian and American populations. As the two subspecies differ in their ability to vector disease, their existence side by side in West Africa may have important implications for disease transmission.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-017-0351-0) contains supplementary material, which is available to authorized users.

Population structure of a vector of human diseases: Aedes aegypti in its ancestral range, Africa

“…A recent study (Crawford et al., ) based on exome sequence data, suggested that Aaa may have arisen from populations of Aaf in West Africa, specifically from Senegal which was the only West African country sampled in that study. Our data indicate that, while Senegal has some genetic signal typical of Aaa outside Africa, the Angola sample displays an even stronger signal of genetic relatedness to Aaa outside Africa (Figure ).…”

“…However, there is a major difference between Bennett et al A recent study (Crawford et al, 2017) based on exome sequence data, suggested that Aaa may have arisen from populations of Aaf in West Africa, specifically from Senegal which was the only West…”

“…mascarensis was used as an outgroup, and Aaa samples from New World and Asia were used to test the distinctiveness of Aaf and Aaa lineages. Bootstraps are presented on the nodes; values <70 are not shown Using genetic data, the time of origin of Aaa in the New World has been estimated to be ~400-500 years ago (Crawford et al, 2017;Gloria-Soria et al, 2016;Kotsakiozi et al, 2018). Yellow fever was first reported in the New World in 1648 (McNeill, 1976) not long after the introduction of Ae.…”

Viral Emerging Pathogen Evolution

“…Recent evidence based on the sequencing of DNA and nucleotide polymorphisms (SNPs) of Aedes aegypti supports the evidence that shows that mosquito populations in the New World are derived directly from African populations. A. aegypti originated in Africa and then colonized the Americas, Oceania and the Asian tropics through trade during the 17thÀ19th centuries (Powell and Tabachnick, 2013;Brown et al, 2011;Brown et al, 2014;Bennett et al, 2016;Crawford et al, 2017). This redistribution of A. aegypti coincided with the appearance of yellow fever and dengue fever in the Americas and dengue fever in Asia (Gould et al, 2003;Tabachnick, 1991;Urdaneta-Marquez and Failloux, 2011).…”

Comparative phylogeography of Aedes mosquitoes and the role of past climatic change for evolution within Africa

“…aegypti have shown that the ancestral African populations are genetically distinct from a more domesticated pantropical form of Ae. aegypti that is widespread throughout the Tropics (Bennett et al., ; Brown, McBride, et al., , ; Crawford et al., ; Gloria‐Soria et al., ). Inference of the demographic history of Ae.…”