Inference of Evolutionary History of Aedes aegypti Mosquito Populations in Saudi Arabia and Africa and Implications for Arbovirus Transmission

Abstract

The process of the evolution of host preference, which occurs frequently in nature, is an exciting opportunity to study ecological divergence as well as having important consequences for disease transmission. The mosquito Aedes aegypti presents an outstanding chance to investigate such an evolutionary process since its recent evolutionary history includes a host switch. The ancestral form of the mosquito, Aedes aegypti formosus, is sylvatic and has a zoophilic host preference whereas the domestic form, Aedes aegypti aegypti, is anthropophagic and breeds in and around human habitation. The domestic form of Aedes aegypti is the main vector for the diseases of dengue, yellow fever, chikungunya, and Zika which are a major public health concern worldwide. This species, which had its beginnings in African forests, successfully spread to other parts of the world by colonizing domestic habitats in towns and villages. A key part of the domestication process was the host switch to feeding on humans which results in part from newly evolved alleles of the odorant receptor gene AaegOr4 that result in a preference for feeding on humans. In Chapter 3, I sequenced a region of this gene from African and non-African mosquito populations that contains two new mutations only found in human-feeding allelic variants. I showed that the human feeding alleles were geographically widespread, had low genetic diversity and were at high frequency which is a strong genetic signal of a selective sweep. The selective advantage of human-feeding alleles is likely related to the ease of finding and feeding on abundant human hosts. In the populations studied here, only human feeding variants were found outside of Africa and animal-feeding alleles occurred only in Africa. However, the derived human feeding allele was also at high frequency in many African populations indicating that it is spreading in Africa. I hypothesise that this spread lies behind the increase in dengue in Africa in recent years and indicates a future heightened risk of dengue and other diseases such as chikungunya and Zika in Africa. Saudi Arabia is very close to Africa with a long history of sea trade along the East African coast. In Chapter 4 I therefore addressed the question of what the source was of Aedes aegypti mosquitoes in Saudi Arabia: had they invaded from Africa, from other pantropical populations, or both? Using sequence data from four putatively neutral nuclear loci I explored the genetic make-up and historical information of Aedes aegypti samples from Saudi Arabian, African and non-African populations. I showed that Saudi Arabia had the genetic characteristics of both African and non-African populations indicating that it has been colonised from both sources. This may have implications for high variation in habitat and host use by Aedes aegypti in Saudi Arabia that could influence disease risk and vector control. To improve our knowledge of how human activities influenced the recent evolutionary history and colonisation of Aedes aegypti, future research should test the hypotheses generated by this thesis.

Date of Award	1 Aug 2023
Original language	English
Awarding Institution	The University of Manchester
Supervisor	Catherine Walton (Supervisor) & Robert Gilman (Supervisor)