Affiliations: 1) Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ; 2) Department of Biology, Stanford University, Stanford, CA
Keywords: Population history
The Northern House Mosquito Culex pipiens sensu stricto is the most important disease vector mosquito in temperate zones across the northern hemisphere, responsible for the emergence of West Nile Virus and filarial worms over the last few decades. There are two ecologically distinct yet morphologically indistinguishable forms. An aboveground form pipiens diapauses in winter and primarily targets birds, while a belowground form molestus thrives year round in belowground habitats such as subways or basements, and prefers mammals over birds. Despite their abundance and importance, we know surprisingly little about the genetic and evolutionary history of these two Cx. pipiens ecotypes. The origin of the belowground molestus is particularly contentious, with iconic populations from the London Underground metro system being held up by evolutionary biologists as a proof-of-principle example of rapid, in situ, urban adaptation and speciation. Furthermore, the two forms hybridize in some zones of contact, which further complicates inferences of evolutionary history and public health efforts. To better understand the genomic status and evolutionary history of the ecotypes, we launched the Culex pipiens Population Genomics Project (PipPop). Here, by sequencing the genomes of 800+ individual mosquitoes collected across the entire global distribution of the species, we provide the first clear picture of genomic variation in this group and infer the timing and geography of divergence within the species. We find that aboveground populations form a latitudinal hybrid gradient stretching from what are known to be traditional pipiens populations in northern Europe down to molestus-like aboveground populations in the Middle East. We also find that belowground molestus from all over the world are genetically most similar to Middle Eastern populations. Together, our data reject the popular in situ evolution hypothesis and instead suggest that underground populations represent recent migrants from the Middle Eastern populations that evolved the anthropophilic ecology over the course of millennia rather than centuries. We test alternative demographic models using the genomic data. Lastly, using the worldwide panel of genomes, we build an eco-geographic model to understand the current and future distributions of the cosmopolitan mosquito.