Population genomics of two invasive mosquitoes ( Aedes aegypti and Aedes albopictus) from the Indo-Pacific

Abstract

The arbovirus vectors Aedes aegypti (yellow fever mosquito) and Ae. albopictus (Asian tiger mosquito) are both common throughout the Indo-Pacific region, where 70% of global dengue transmission occurs. For Ae. aegypti all Indo-Pacific populations are invasive, having spread from an initial native range of Africa, while for Ae. albopictus the Indo-Pacific includes invasive populations and those from the native range: putatively, India to Japan to Southeast Asia. This study analyses the population genomics of 480 of these mosquitoes sampled from 27 locations in the Indo-Pacific. We investigated patterns of genome-wide genetic differentiation to compare pathways of invasion and ongoing gene flow in both species, and to compare invasive and native-range populations of Ae. albopictus. We also tested landscape genomic hypotheses that genetic differentiation would increase with geographical distance and be lower between locations with high connectivity to human transportation routes, the primary means of dispersal at these scales. We found that genetic distances were generally higher in Ae. aegypti, with Pacific populations the most highly differentiated. The most differentiated Ae. albopictus populations were in Vanuatu, Indonesia and Sri Lanka, the latter two representing potential native-range populations and potential cryptic subspeciation respectively. Genetic distances in Ae. aegypti increased with geographical distance, while in Ae. albopictus they decreased with higher connectivity to human transportation routes. Contrary to the situation in Ae. aegypti, we found evidence of long-distance Ae. albopictus colonisation events, including colonisation of Mauritius from East Asia and of Fiji from Southeast Asia. These direct genomic comparisons indicate likely differences in dispersal ecology in these species, despite their broadly sympatric distributions and similar use of human transport to disperse. Our findings will assist biosecurity operations to trace the source of invasive material and for biocontrol operations that benefit from matching genetic backgrounds of released and local populations.

Author summary

The mosquitoes Ae. aegypti and Ae. albopictus are highly invasive and transmit dengue and other arboviruses. This study investigates the genetics of these mosquitoes in the Indo-Pacific region, where 70% of global dengue transmission occurs and where both species have established widespread invasions by hitch-hiking on human transport vessels. We compared patterns of genetic differentiation to determine the pathways these species have taken while spreading through the Indo-Pacific, and to better understand how they disperse. We sequenced DNA from 480 mosquitoes sampled from 27 locations in the Indo-Pacific, and found many genetic differences between the two species. Populations of Ae. aegypti, which is not native to the region, tended to be genetically different from each other, and populations in the Pacific Ocean were particularly divergent. Aedes albopictus populations were generally more similar to each other, though genetically different populations in Sri Lanka and Indonesia point to these having a different history to other populations. Genetic differences between Ae. aegypti populations were larger when populations were geographically distant, while differences between Ae. albopictus populations were larger when populations likely had limited access to human transportation. These results will help improve strategies for controlling these species and stopping their spread around the world.