Fine-scale adaptive divergence of Aedes aegypti in heterogeneous landscapes and among climatic conditions in Metropolitan Manila, Philippines

The adaptive divergence of Aedes aegypti populations to heterogeneous environments may be a driving force behind the recent expansion of their habitat distribution and outbreaks of dengue disease in urbanized areas. In this study, we investigated the population genomics of Ae. aegypti at a regional scale in Metropolitan Manila, Philippines using double digestion restriction-site association DNA sequencing (ddRAD-Seq). Specifically, we used a Pool-Seq approach to generate a high number of single nucleotide polymorphisms (SNPs), which were used to determine local adaptation and population structure. We detected 65,473 SNPs in 217 Ae. aegypti individuals from 14 populations with 76 non-neutral SNP loci. Additionally, 57 of these non-neutral SNP loci were associated with 8 landscape variables (e.g., open space, forest, etc) and 4 climate variables (e.g., air temperature, humidity, etc). Furthermore, the percentage of the area of landscape variables, such as forest, parks and recreation, air temperature, man-made building, and open space per local population was frequently associated with non-neutral SNP loci. Most non-neutral SNP loci formed four clusters that were in linkage disequilibrium with each other in physical proximity on the chromosome and were associated with a common environmental variable. Male and female populations exhibited contrasting spatial divergence, i.e., males exhibited greater divergence, likely reflecting their different dispersal abilities. In comparative analysis of the same Ae. aegypti individuals, the pairwise FST values of 11 microsatellite markers were lower than those of neutral SNP loci, indicating that the neutral SNP loci generated via ddRAD-Seq were more sensitive in terms of detecting genetic differences between populations at fine-spatial scales. Overall, this study demonstrates the utility of ddRAD-Seq for examining genetic differences in Ae. aegypti populations, and our data on mosquito dispersal at a regional spatial scale could inform vector control programs. Author SummaryThe population expansion of dengue vector, Aedes aegypti mosquitoes is one of the factors that may promote the outbreak of the diseases. Understanding the population genomics of Ae.aegypti may contribute to better knowledge about mosquito expansion and how they can adapt to the change in environment. In this study, we used pool-based ddRAD-Seq (Double Digest Restriction site Association DNA Sequencing) to generate SNPs that occur between the Ae.aegypti populations in Metropolitan Manila, Philippines. We found that non-neutral SNP loci are frequently associated with landscape variables compared to climatic variables. Landscape variables such as forest, park and recreation, air temperature, man-made building and open space are more frequently associated with non-neutral SNPs loci. Those landscape variables may relate to the mosquitos fitness, therefore, induce the adaptive divergence within Ae.aegypti population. We also found male and female populations are exhibiting a contrast spatial divergence by using neutral SNP loci. In addition, neutral SNPs loci showed higher resolution in population structuring than microsatellite markers using the same individuals.