Ancient Origin of an Urban Underground Mosquito

Understanding how life is adapting to urban environments represents an important challenge in evolutionary biology. Here we investigate a widely cited example of urban adaptation, form , also known as the London Underground Mosquito. Population genomic analysis of ~350 contemporary and historical samples counter the popular hypothesis that originated belowground in London less than 200 years ago. Instead, we show that first adapted to human environments aboveground in the Middle East over the course of >1000 years, likely in concert with the rise of agricultural civilizations. Our results highlight the role of early human society in priming taxa for contemporary urban evolution and have important implications for understanding arbovirus transmission.

References

Fritz M, Walker E, Miller J, Severson D, Dworkin I . Divergent host preferences of above- and below-ground Culex pipiens mosquitoes and their hybrid offspring. Med Vet Entomol. 2015; 29(2):115-23. DOI: 10.1111/mve.12096. View

Giesen C, Herrador Z, Fernandez-Martinez B, Figuerola J, Gangoso L, Vazquez A . A systematic review of environmental factors related to WNV circulation in European and Mediterranean countries. One Health. 2023; 16:100478. PMC: 10288031. DOI: 10.1016/j.onehlt.2022.100478. View

Rose N, Badolo A, Sylla M, Akorli J, Otoo S, Gloria-Soria A . Dating the origin and spread of specialization on human hosts in mosquitoes. Elife. 2023; 12. PMC: 10038657. DOI: 10.7554/eLife.83524. View

Duron O, Lagnel J, Raymond M, Bourtzis K, Fort P, Weill M . Transposable element polymorphism of Wolbachia in the mosquito Culex pipiens: evidence of genetic diversity, superinfection and recombination. Mol Ecol. 2005; 14(5):1561-73. DOI: 10.1111/j.1365-294X.2005.02495.x. View

Dumas E, Atyame C, Milesi P, Fonseca D, Shaikevich E, Unal S . Population structure of Wolbachia and cytoplasmic introgression in a complex of mosquito species. BMC Evol Biol. 2013; 13:181. PMC: 3846486. DOI: 10.1186/1471-2148-13-181. View

Martinez-de la Puente J, Ferraguti M, Ruiz S, Roiz D, Soriguer R, Figuerola J . Culex pipiens forms and urbanization: effects on blood feeding sources and transmission of avian Plasmodium. Malar J. 2016; 15(1):589. PMC: 5146868. DOI: 10.1186/s12936-016-1643-5. View

Ravinet M, Elgvin T, Trier C, Aliabadian M, Gavrilov A, Saetre G . Signatures of human-commensalism in the house sparrow genome. Proc Biol Sci. 2018; 285(1884). PMC: 6111181. DOI: 10.1098/rspb.2018.1246. View

Farajollahi A, Fonseca D, Kramer L, Kilpatrick A . "Bird biting" mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect Genet Evol. 2011; 11(7):1577-85. PMC: 3190018. DOI: 10.1016/j.meegid.2011.08.013. View

Weissbrod L, Marshall F, Valla F, Khalaily H, Bar-Oz G, Auffray J . Origins of house mice in ecological niches created by settled hunter-gatherers in the Levant 15,000 y ago. Proc Natl Acad Sci U S A. 2017; 114(16):4099-4104. PMC: 5402403. DOI: 10.1073/pnas.1619137114. View

10.

Hendry A, Gotanda K, Svensson E . Human influences on evolution, and the ecological and societal consequences. Philos Trans R Soc Lond B Biol Sci. 2016; 372(1712). PMC: 5182424. DOI: 10.1098/rstb.2016.0028. View

11.

Osorio H, Ze-Ze L, Amaro F, Nunes A, Alves M . Sympatric occurrence of Culex pipiens (Diptera, Culicidae) biotypes pipiens, molestus and their hybrids in Portugal, Western Europe: feeding patterns and habitat determinants. Med Vet Entomol. 2013; 28(1):103-9. DOI: 10.1111/mve.12020. View

12.

Harpak A, Garud N, Rosenberg N, Petrov D, Combs M, Pennings P . Genetic Adaptation in New York City Rats. Genome Biol Evol. 2020; 13(1). PMC: 7851592. DOI: 10.1093/gbe/evaa247. View

13.

Harbach R . Culex pipiens: species versus species complex taxonomic history and perspective. J Am Mosq Control Assoc. 2013; 28(4 Suppl):10-23. DOI: 10.2987/8756-971X-28.4.10. View

14.

Otto S . Adaptation, speciation and extinction in the Anthropocene. Proc Biol Sci. 2018; 285(1891). PMC: 6253383. DOI: 10.1098/rspb.2018.2047. View

15.

Naddaf M . Mosquito-borne diseases are surging in Europe - how worried are scientists?. Nature. 2024; 633(8031):749. DOI: 10.1038/d41586-024-03031-y. View

16.

Petersen L, Brault A, Nasci R . West Nile virus: review of the literature. JAMA. 2013; 310(3):308-15. PMC: 4563989. DOI: 10.1001/jama.2013.8042. View

17.

Byrne K, Nichols R . Culex pipiens in London Underground tunnels: differentiation between surface and subterranean populations. Heredity (Edinb). 1999; 82 ( Pt 1):7-15. DOI: 10.1038/sj.hdy.6884120. View

18.

Haba Y, McBride L . Origin and status of Culex pipiens mosquito ecotypes. Curr Biol. 2022; 32(5):R237-R246. PMC: 9108678. DOI: 10.1016/j.cub.2022.01.062. View

19.

Thompson K, Rieseberg L, Schluter D . Speciation and the City. Trends Ecol Evol. 2018; 33(11):815-826. DOI: 10.1016/j.tree.2018.08.007. View

20.

Winchell K, Losos J, Verrelli B . Urban evolutionary ecology brings exaptation back into focus. Trends Ecol Evol. 2023; 38(8):719-726. DOI: 10.1016/j.tree.2023.03.006. View