Haba, Y.,  PipPop consortium including Smitz, N.,  Korlevic, P.,  Mcalister, E.,  Lawniczak, M.K.N,  Schumer, M.,  Rose, N.H. & Mcbride, C.S. 2025. ‘Ancient origin of an urban underground mosquito’. Corinne Simonti (ed), Science 390: 355. DOI: DOI: 10.1126/science.ady4515. URL: https://www.science.org/doi/10.1126/science.ady4515  I.F. 45,8.

Article in a scientific Journal / Article in a Journal

INTRODUCTION Urbanization is rapidly reshaping landscapes around the world, which poses questions about whether and how quickly animals and plants can adapt. Culex pipiens form molestus, more commonly known as the London Underground mosquito, has been held up as a benchmark for the potential speed and complexity of urban adaptation. This intraspecific lineage within Cx. pipiens s. s. is purported to have evolved human biting and a suite of other human-adaptive behaviors in the subways and cellars of northern Europe within the past 200 years. Form molestus features prominently in textbooks as well as scholarly reviews of urban adaptation. Yet, the hypothesis of in situ urban evolution has never been rigorously tested. RATIONALE In addition to spawning an enigmatic human-biting form, Cx. pipiens s. s. is one of the most important vectors of mosquito-borne disease in temperate regions across the world. The ancestral form of Cx. pipiens is bird biting and serves as a major vector of West Nile virus (WNV) within bird populations. Hybridization of this ancestral bird-biting form with human-biting molestus produces mosquitoes that are willing to bite both birds and humans and is hypothesized to have driven increasing spillover of WNV to humans in the US and southern Europe over the past two decades. Although this hypothesis has spurred intense efforts to characterize gene flow between forms, the results have been variable and confusing, with no clear consensus on where and to what degree gene flow occurs. RESULTS We sequenced the whole genomes of ~350 contemporary and historical Cx. pipiens mosquitoes from 77 populations scattered across Europe, North Africa, and western Asia and used population genomic analysis to infer the evolutionary history of molestus. Studies of population structure, derived allele sharing, phylogeny, and cross-coalescence show that molestus could not have evolved in urban belowground habitats over the past 200 years. Instead, it first adapted to human environments >1000 years ago in the Mediterranean or Middle East, most likely in ancient Egypt or another early agricultural society. Our genomic data also provide a major revision to our understanding of gene flow between bird- and mammal-biting forms. We found that genetic signatures that researchers previously ascribed to between-form hybridization instead reflect ancestral variation within bird-biting populations. After correcting for this variation, we can see that true hybridization is less common than previously believed and is associated with human population density—a proxy for urbanization. CONCLUSION Our work debunks one of the most widely cited examples of rapid urban adaptation—an example that has captured the attention of scientists and laypeople for 25 years. Rather than benchmarking the speed and complexity of urban evolution, this updated history highlights the role of early human society in priming taxa for colonization of modern urban environments. Our work also revises our fundamental understanding of gene flow in this important vector and opens the door to incisive investigation of the potential links between urbanization, hybridization, and arbovirus spillover to humans.