Invasion history and evolution of the Asian tiger mosquito Aedes albopictus (Skuse, 1894) and yellow fever mosquito Aedes aegypti (Linnaeus, 1762) in the Indo-Pacific

Abstract

Mosquitoes cause more human deaths than any other animal in the world. Diseases such as dengue, chikungunya and Zika are transmitted to humans by two chief mosquito vectors: the yellow fever mosquito Aedes aegypti (Linneaus, 1762) and the Asian tiger mosquito Aedes albopictus (Skuse, 1894). Both species are highly invasive due to their close association with humans and ecological plasticity. They originate from different parts of the world, and have discrete behaviours, evolution, and ecology, but share key similarities in their global invasions, making them ideal candidates for investigating population genetic processes in invasive species. My dissertation explores population genetic patterns and attempts to reconstruct the invasion histories of these two species using microsatellites, gene sequencing, and whole-genome sequencing, specifically focusing on Australasia and Southeast Asia.Within the last century, increases in human movement, globalisation, and trade have facilitated the establishment of several highly invasive mosquito species in new geographic locations causing major environmental, economic and health consequences. The Asian tiger mosquito, Ae. albopictus, has expanded globally in the last century, from its native range in Asia, chiefly due to increases of human movement. In Chapter II (https://doi.org/10.1371/journal.pntd.0005546), I used 13 nuclear microsatellite loci (911 individuals) and mitochondrial COI sequences to gain insight into the historical and contemporary movements of Ae. albopictus in the Indo-Pacific. Approximate Bayesian computation (ABC) was employed to test competing historical invasion routes within Southeast Asia and Australasia. I uncovered clear genetic clusters throughout the Indo-Pacific, but some geographically distant populations appear closely-related, likely due to human-associated movements. I also found that Ae. albopictus likely colonised New Guinea from mainland Southeast Asia, before spreading to the Solomon Islands via either Papua New Guinea (PNG) or Southeast Asia. In contrast, the recent (mid-2000s) incursion into northern Australia’s Torres Strait Islands likely stemmed from an Indonesian genetic source. These recently colonised populations displayed high spatio-temporal structure which could be due to genetic drift or represent a secondary invasion from an unknown source.For Chapter III, I used similar tools to elucidate the invasion history and population genetics of Ae. aegypti across several populations in Southeast Asia and Australasia. This African native spread globally several centuries (~500 years ago) prior to Ae. albopictus mediated by global shipping. I used 11 nuclear microsatellites (366 individuals) and COI sequences to explore Ae. aegypti’s population structure and invasion history using more detailed analyses and ABC simulations than previous investigations. My results highlight that Ae. aegypti established in the region via multiple, independent invasions between the late-1700s and early 1900s. My research also revealed further genetic divisions between populations that had not previously been found. These results help to resolve the invasive origins of Ae. aegypti and act as a starting place for future studies.In Chapter IV, I reanalysed some of the samples of Ae. albopictus used in Chapter II using a whole-genome sequencing approach. Until now, few studies have explored the genetics of this species using a genome-wide approach. To further investigate population structure and determine the sources of recently invaded regions, the genomes of 158 individuals from nine populations (one with temporal sampling) from Australasia and Southeast Asia were sequenced. Population patterns were mostly consistent with those obtained in Chapter II, but revealed less admixture between genetic clusters and clearer differentiation between populations than was shown with microsatellites. I found that certain genomic regions may be under selection in some native and introduced populations using sliding windows of FST across the genome. I estimated the demographic histories of populations using this genomic dataset to better understand how effective population size has varied over time to elucidate the biogeography of Ae. albopictus across Sundaland (exposed Southeast Asian landmass). I found strong support for post-glacial population isolation following the last glacial maximum (18-21 million years ago) when sea levels rose rapidly. Additionally, by analysing the mitochondrial genomes of my samples I was able to compare my dataset to a more global one, further detailing the relationships between various native and invasive populations of Ae. albopictus.Overall, this thesis represents the most comprehensive analysis of the population structure and invasion history of Ae. albopictus and Ae. aegypti in Australasia and Southeast Asia using genetic approaches to date. It also represents the first investigation of the biogeographic history of Ae. albopictus in an unstudied region of its native and introduced range using genomic techniques. This knowledge is crucial to understand the invasion histories and current genetic population structure of these two medically significant species. I have been able to compare and critique the different population genetic approaches used here to inform others. My dissertation results could be useful for the successful deployment of control strategies and for identifying invasion pathways for biosecurity as it enhances our understanding of mosquito movements, population relatedness and invasion history.