Ancient origin of an urban underground mosquito

Yuki Haba^{1

2}; PipPop Consortium‡; Petra Korlević³, Erica McAlister⁴, Mara K N Lawniczak³, Molly Schumer⁵, Noah H Rose^{1

2}, Carolyn S McBride^{1

2}, Matthew L Aardema⁶, Maria O Afonso⁷, Natasha M Agramonte⁸, John Albright⁹, Ana Margarida Alho¹⁰, Antonio P G Almeida⁷, Haoues Alout¹¹, Bulent Alten¹², Mine Altinli^{13

14}, Raouf Amara Korba¹⁵, Stefanos S Andreadis¹⁶, Vincent Anghel¹⁷, Soukaina Arich^{13

18}, Arielle Arsenault-Benoit¹⁹, Célestine Atyame²⁰, Fabien Aubry²¹, Frank W Avila²², Diego Ayala^{23

24}, Rasha S Azrag²⁵, Lilit Babayan²⁶, Allon Bear²⁷, Norbert Becker^{28

29}, Anna G Bega^{30

31}, Sophia Bejarano³², Ira Ben-Avi³³, Joshua B Benoit³⁴, Saïd C Boubidi³⁵, William E Bradshaw³⁶, Daniel Bravo-Barriga^{37

38}, Rubén Bueno-Marí³⁹, Nataša Bušić⁴⁰, Viktoria Čabanová⁴¹, Brittany Cabeje³², Beniamino Caputo⁴², Maria V Cardo⁴³, Simon Carpenter⁴⁴, Elena Carreton⁴⁵, Mouhamadou S Chouaïbou⁴⁶, Michelle Christian³², Maureen Coetzee^{47

48}, William R Conner⁴⁹, Anton Cornel⁵⁰, C Lorna Culverwell^{51

4}, Aleksandra I Cupina⁵², Katrien De Wolf⁵³, Isra Deblauwe⁵³, Brittany Deegan⁵⁴, Sarah Delacour-Estrella⁵⁵, Alessandra Della Torre⁴², Debora Diaz³³, Serena E Dool⁵⁶, Vitor L Dos Anjos¹, Sisay Dugassa⁵⁷, Babak Ebrahimi⁵⁸, Samar Y M Eisa²⁵, Nohal Elissa⁵⁹, Sahar A B Fallatah⁶⁰, Ary Faraji⁶¹, Marina V Fedorova⁶², Emily Ferrill³², Dina M Fonseca⁶³, Kimberly A Foss⁶⁴, Cipriano Foxi⁶⁵, Caio M França⁶⁶, Stephen R Fricker^{67

68}, Megan L Fritz¹⁹, Eva Frontera³⁷, Hans-Peter Fuehrer⁶⁹, Kyoko Futami⁷⁰, Enas H S Ghallab⁷¹, Romain Girod⁷², Mikhail I Gordeev⁷³, David Greer¹⁷, Martin Gschwind^{74

75}, Milehna M Guarido^{76

77}, Teoh Guat Ney⁷⁸, Filiz Gunay¹², Eran Haklay⁷⁹, Alwia A E Hamad²⁵, Jun Hang⁸⁰, Christopher M Hardy⁸¹, Jacob W Hartle⁸², Jenny C Hesson^{83

84}, Yukiko Higa⁸⁵, Christina M Holzapfel³⁶, Ann-Christin Honnen^{74

75}, Angela M Ionica⁸⁶, Laura Jones⁴⁴, Përparim Kadriaj⁸⁷, Hany A Kamal⁸⁸, Colince Kamdem⁸⁹, Dmitry A Karagodin⁹⁰, Shinji Kasai⁸⁵, Mihaela Kavran⁵², Emad I M Khater⁷¹, Frederik Kiene⁹¹, Heung-Chul Kim⁹², Ilias Kioulos⁹³, Annette Klein⁹¹, Marko Klemenčić⁹⁴, Ana Klobučar⁹⁵, Erin Knutson⁹⁶, Constantianus J M Koenraadt⁹⁷, Linda Kothera⁹⁸, Pauline Kreienbühl²¹, Pierrick Labbé^{13

99}, Itay Lachmi¹⁰⁰, Louis Lambrechts²¹, Nediljko Landeka¹⁰¹, Christopher H Lee¹⁰², Bryan D Lessard¹⁰³, Ignacio Leycegui¹⁷, Jan O Lundström^{83

84}, Yoav Lustigman¹⁰⁰, Caitlin MacIntyre¹⁰⁴, Andrew J Mackay¹⁰⁵, Krisztian Magori¹⁰⁶, Carla Maia⁷, Colin A Malcolm¹⁰⁷, Ralph-Joncyn O Marquez³³, Dino Martins¹⁰⁸, Reem A Masri¹⁰⁹, Gillian McDivitt³², Rebekah J McMinn¹¹⁰, Johana Medina¹¹¹, Karen S Mellor¹¹², Jason Mendoza³², Enrih Merdić⁴⁰, Stacey Mesler³², Camille Mestre¹³, Homer Miranda³², Martina Miterpáková¹¹³, Fabrizio Montarsi¹¹⁴, Anton V Moskaev³⁰, Tong Mu¹, Tim W R Möhlmann⁹⁷, Alice Namias¹³, Ivy Ng'iru¹⁰⁸, Marc F Ngangué²⁴, Maria T Novo⁷, Laor Orshan³³, José A Oteo¹¹⁵, Yasushi Otsuka¹¹⁶, Rossella Panarese¹¹⁷, Claudia Paredes-Esquivel¹¹⁸, Lusine Paronyan²⁶, Steven T Peper¹¹⁹, Dušan V Petrić⁵², Kervin Pilapil³², Cristina Pou-Barreto¹²⁰, Sebastien J Puechmaille^{13

99

121}, Ute Radespiel¹²², Nil Rahola²³, Vivek K Raman¹⁷, Hamadouche Redouane¹²³, Michael H Reiskind¹²⁴, Nadja M Reissen⁶¹, Benjamin L Rice^{1

125}, Vincent Robert²³, Ignacio Ruiz-Arrondo¹¹⁵, Ryan Salamat³², Amy Salamone⁹⁶, M'hammed Sarih¹⁸, Giuseppe Satta⁶⁵, Kyoko Sawabe⁸⁵, Francis Schaffner^{126

127}, Karen E Schultz¹²⁸, Elena V Shaikevich³¹, Igor V Sharakhov^{109

129}, Maria V Sharakhova^{109

130}, Nader Shatara¹³¹, Anuarbek K Sibataev^{132

133}, Mathieu Sicard¹³, Evan Smith³⁴, Ryan C Smith¹⁰², Nathalie Smitz¹³⁴, Nicolas Soriano³², Christos G Spanoudis¹³⁵, Christopher M Stone¹⁰⁵, Liora Studentsky³⁴, Tatiana Sulesco¹⁴, Luciano M Tantely¹³⁶, La K Thao¹³⁷, Noor Tietze⁵⁸, Ryan E Tokarz¹³⁸, Kun-Hsien Tsai¹³⁹, Yoshio Tsuda⁸⁵, Nataša Turić⁴⁰, Melissa R Uhran³⁴, Isik Unlu¹¹¹, Wim Van Bortel^{53

140}, Haykuhi Vardanyan²⁶, Laura Vavassori^{74

75}, Enkelejda Velo⁸⁷, Marietjie Venter^{76

141}, Goran Vignjević⁴⁰, Chantal B F Vogels^{97

142}, Tatsiana Volkava¹⁴³, John Vontas^{93

144}, Heather M Ward¹¹⁹, Nazni Wasi Ahmad⁷⁸, Mylène Weill¹³, Jennifer D West⁸², Sarah S Wheeler¹⁴⁵, Gregory S White⁶¹, Nadja C Wipf^{74

75

146}, Tai-Ping Wu¹⁴⁷, Kai-Di Yu¹⁴⁸, Elke Zimmermann¹²², Carina Zittra¹⁴⁹

Affiliations

¹ Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA.
² Princeton Neuroscience Institute, Princeton University, Princeton, NJ, USA.
³ Wellcome Sanger Institute, Hinxton, UK.
⁴ Department of Life Sciences, The Natural History Museum, London, UK.
⁵ Department of Biology and Howard Hughes Medical Institute, Stanford University, Stanford, CA, USA.
⁶ Department of Biology, Montclair State University, Montclair, NJ, USA.
⁷ Global Health and Tropical Medicine, GHTM, LA-REAL, Instituto de Higiene e Medicina Tropical, Universidade NOVA de Lisboa, Lisboa, Portugal.
⁸ DeKalb County Board of Health, Decatur, GA, USA.
⁹ Shasta Mosquito and Vector Control District, Anderson, CA, USA.
¹⁰ Public Health Unit USP Francisco George, Primary Medical Healthcare Cluster Lisbon North, Largo Professor Arnaldo Sampaio, Lisboa, Portugal.
¹¹ ASTRE, UMR 117, INRAE-CIRAD, Montpellier, France.
¹² Hacettepe University, Faculty of Science, Department of Biology, VERG Laboratories, Beytepe, Ankara, Turkey.
¹³ Institut des Sciences de l'Évolution de Montpellier (UMR 5554, CNRS-UM-IRD-EPHE), Université de Montpellier, Montpellier, France.
¹⁴ Bernhard-Nocht-Institute for Tropical Medicine, Bernhard Nocht Str. 74, Hamburg, Germany.
¹⁵ Laboratory of Health and Environment, Faculty of Life and Natural Sciences and of Earth and Universe Sciences, Mohamed El Bachir El Ibrahimi University, Bordj Bou Arreridj, Algeria.
¹⁶ Institute of Plant Breeding and Genetic Resources, Hellenic Agricultural Organization - DIMITRA, Thermi, Greece.
¹⁷ Southern Nevada Health District, Las Vegas, NV, USA.
¹⁸ Service de Parasitologie et des Maladies Vectorielles, Institut Pasteur du Maroc, Casablanca, Morocco.
¹⁹ Department of Entomology, University of Maryland, College Park, MD, USA.
²⁰ University of Reunion Island, UMR PIMIT (Processus Infectieux en Milieu Insulaire Tropical) CNRS 9192, INSERM 1187, IRD 249, University of Reunion Island, Reunion Island, France.
²¹ Institut Pasteur, Université Paris Cité, CNRS UMR2000, Insect-Virus Interactions Unit, Paris, France.
²² Max Planck Tandem Group in Mosquito Reproductive Biology, Universidad de Antioquia, Medellín, Colombia.
²³ MIVEGEC, University of Montpellier, CNRS, IRD, Montpellier, France.
²⁴ CIRMF, Franceville, Gabon.
²⁵ Department of Zoology, Faculty of Science, University of Khartoum, Khartoum, Sudan.
²⁶ National Center of Disease Control and Prevention, Ministry of Health, Yerevan, Republic of Armenia.
²⁷ E7 Ministry of Environmental Protection, Ramla, Israel.
²⁸ Center for Organismal Studies, University of Heidelberg, Heidelberg, Germany.
²⁹ German Mosquito Control Association, Speyer, Germany.
³⁰ Laboratory of Experimental Biology and Biotechnology, Scientific and Educational Center in Chernogolovka, Federal State University of Education, Moscow, Russia.
³¹ Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, Russia.
³² County of San Diego, Vector Control Program, San Diego, CA, USA.
³³ Ministry of Health, Jerusalem, Israel.
³⁴ Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, USA.
³⁵ Entomology Unit, Laboratory of Parasitology, Pasteur Institute of Algeria, Algiers, Algeria.
³⁶ Institute of Ecology and Evolution, 5289 University of Oregon, Eugene, OR, USA.
³⁷ Parasitología, Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad de Extremadura, Cáceres, Spain.
³⁸ Department of Animal Health Department (Parasitology and Parasitic Diseases), Faculty of Veterinary Medicine, University of Córdoba, Sanidad Animal Building, Rabanales Campus, Córdoba, Spain.
³⁹ European Center of Excellence for Vector Control, Laboratorios Lokímica - Rentokil Initial, Valencia, Spain.
⁴⁰ Department of Biology, Josip Juraj Strossmayer University of Osijek, Osijek, Croatia.
⁴¹ Department of Virus Ecology, Institute of Virology, Biomedical Research Center Slovak Academy of Sciences, Bratislava, Slovakia.
⁴² Department of Public Health and Infectious Diseases, Sapienza University, Rome, Italy.
⁴³ Ecología de Enfermedades Transmitidas por Vectores, Instituto de Investigación e Ingeniería Ambiental, UNSAM, CONICET, Buenos Aires, Argentina.
⁴⁴ The Pirbright Institute, Ash Road, Woking, Surrey, UK.
⁴⁵ Faculty of Veterinary Medicine, Research Institute of Biomedical and Health Sciences, University of Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Spain.
⁴⁶ Centre Suisse de Recherches Scientifiques en Côte d'Ivoire, Abidjan, Côte d'Ivoire.
⁴⁷ Wits Research Institute for Malaria, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
⁴⁸ Centre for Emerging Zoonotic and Parasitic Diseases, National Institute for Communicable Diseases, Johannesburg, South Africa.
⁴⁹ Department of Evolution and Ecology, University of California, Davis, CA, USA.
⁵⁰ Kearney Agricultural Research and Extension Center, Parlier, CA, USA.
⁵¹ University of Helsinki, Medicum, Department of Virology, Helsinki, Finland.
⁵² Faculty of Agriculture, Centre of Excellence One Health Vectors and Climate, Laboratory for Medical and Veterinary Entomology, University of Novi Sad, Novi Sad, Serbia.
⁵³ Entomology Unit, Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium.
⁵⁴ Consolidated Mosquito Abatement District, Parlier, CA, USA.
⁵⁵ Department of Animal Pathology, Faculty of Veterinary Medicine at the University of Zaragoza, Zaragoza, Spain.
⁵⁶ Zoological Institute and Museum, University of Greifswald, Greifswald, Germany.
⁵⁷ Aklilu Lemma Institute of Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia.
⁵⁸ Santa Clara County Vector Control District, San Jose, CA, USA.
⁵⁹ Département Faune et Actions de Salubrité, Service Parisien de Santé Environnementale, Direction de la Santé Publique, Ville de Paris, Paris, France.
⁶⁰ Biology Department, College of Science, Imam Abdulrahman bin Faisal University, Dammam, Kingdom of Saudi Arabia.
⁶¹ Salt Lake City Mosquito Abatement District, Salt Lake City, UT, USA.
⁶² Сentral Research Institute for Epidemiology, Moscow, Russia.
⁶³ Center for Vector Biology, Rutgers University, New Brunswick, NJ, USA.
⁶⁴ Northeast Massachusetts Mosquito Control District, Georgetown, MA, USA.
⁶⁵ Istituto Zooprofilattico Sperimentale della Sardegna, Sassari, Italy.
⁶⁶ Department of Biology, Southern Nazarene University, Bethany, OK, USA.
⁶⁷ STEM, University of South Australia, Adelaide, South Australia, Australia.
⁶⁸ Medical Entomology, Centre for Disease Control and Environmental Health, NT Health, NT, Australia.
⁶⁹ Institute of Parasitology, Department of Pathobiology, University of Veterinary Medicine, Vienna, Austria.
⁷⁰ Department of Vector Ecology and Environment, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan.
⁷¹ Department of Entomology, Faculty of Science, Ain Shams University, Abbassia, Cairo, Egypt.
⁷² Medical Entomology Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.
⁷³ Department of General Biology and Ecology, Federal State University of Education, Moscow, Russia.
⁷⁴ Swiss Tropical and Public Health Institute, Allschwil, Switzerland.
⁷⁵ University of Basel, Basel, Switzerland.
⁷⁶ Centre for Emerging and Reemerging Arbo and Respiratory Virus Research (CEARV), Department Medical Virology, University of Pretoria, South Africa.
⁷⁷ Department of Production Animal Studies, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, South Africa.
⁷⁸ Medical Entomology Unit, Infectious Disease Research Centre, Institute For Medical Research, National Institutes of Health, Kuala Lumpur, Malaysia.
⁷⁹ Ministry of Environmental Protection, Jerusalem, Israel.
⁸⁰ Walter Reed Army Institute of Research, Silver Spring, MD, USA.
⁸¹ Environment, CSIRO, Canberra, Australia.
⁸² Placer Mosquito and Vector Control District, Roseville, CA, USA.
⁸³ Department of Medical Biochemistry and Microbiology/Zoonosis Science Center, Uppsala University, Uppsala, Sweden.
⁸⁴ Biologisk Myggkontroll, Nedre Dalälven Utvecklings AB, Uppsala, Sweden.
⁸⁵ Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan.
⁸⁶ Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Cluj-Napoca, Romania.
⁸⁷ Vector Control Unit, Department of Epidemiology and Control of Infectious Diseases, Institute of Public Health, Tirana, Albania.
⁸⁸ Department of Pest Control Projects, Dallah Company, Jeddah, Kingdom of Saudi Arabia.
⁸⁹ Department of Biological Sciences, The University of Texas at El Paso, El Paso, TX, USA.
⁹⁰ Institute of Cytology and Genetics, Novosibirsk, Russia.
⁹¹ Institute of Zoology and Institute of Parasitology, Centre for Infection Medicine, University of Veterinary Medicine Hannover, Hanover, Germany.
⁹² Force Health Protection and Preventive Medicine, Medical Department Activity-Korea/65th Medical Brigade, Unit 15281, APO AP 96271-5281, USA.
⁹³ Department of Crop Science, Agricultural University of Athens, Athens, Greece.
⁹⁴ Croatian Institute for Public Health of Međimurje County, Čakovec, Croatia.
⁹⁵ Department of Epidemiology, Andrija Stampar Teaching Institute of Public Health, Zagreb, Croatia.
⁹⁶ Washington State Department of Health, Olympia, WA, USA.
⁹⁷ Laboratory of Entomology, Wageningen University and Research, Wageningen, Netherlands.
⁹⁸ Centers for Disease Control and Prevention, Fort Collins, CO, USA.
⁹⁹ Institut Universitaire de France, Paris, France.
¹⁰⁰ Nature and Parks Authority, Jerusalem, Israel.
¹⁰¹ Institute of Public Health of the Istrian County, Pula, Croatia.
¹⁰² Department of Plant Pathology, Entomology and Microbiology Iowa State University, Ames, IA, USA.
¹⁰³ Australian National Insect Collection, National Research Collections Australia, CSIRO, Canberra, Australia.
¹⁰⁴ Zoonotic Arbo- and Respiratory Virus Program, Centre for Viral Zoonoses, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa.
¹⁰⁵ Illinois Natural History Survey, Prairie Research Institute, University of Illinois at Urbana-Champaign, Champaign, IL, USA.
¹⁰⁶ Department of Biology, Eastern Washington University, Cheney, WA, USA.
¹⁰⁷ School of Health, Medicine and Life Sciences, University of Hertfordshire, Hatfield, Hertfordshire, UK.
¹⁰⁸ Mpala Research Centre, Nanyuki, Kenya.
¹⁰⁹ Department of Entomology and Fralin Life Sciences Institute, Virginia Polytechnic and State University, Blacksburg, VA, USA.
¹¹⁰ Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO, USA.
¹¹¹ Miami-Dade County Mosquito Control, Miami, FL, USA.
¹¹² Antelope Valley Mosquito and Vector Control District, Lancaster, CA, USA.
¹¹³ Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovakia.
¹¹⁴ Laboratorio di Entomologia Sanitaria e Patogeni Trasmessi da Vettori, Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Italy.
¹¹⁵ Department of Infectious Diseases, Center of Rickettsiosis and Arthropod-Borne Diseases (CRETAV), San Pedro University Hospital-Center for Biomedical Research from La Rioja (CIBIR), Logroño, Spain.
¹¹⁶ Research Center for the Pacific Islands, Kagoshima University, Kagoshima, Japan.
¹¹⁷ Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Valenzano, Italy.
¹¹⁸ Parasitology and Mediterranean Ecoepidemiology Research Group, University of the Balearic Islands, Palma, Spain.
¹¹⁹ Anastasia Mosquito Control District of St. Johns County, Augustine, FL, USA.
¹²⁰ Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias. Universidad de La Laguna, Tenerife, Spain.
¹²¹ Applied Zoology and Nature Conservation, University of Greifswald, Greifswald, Germany.
¹²² Institute of Zoology, University of Veterinary Medicine Hannover, Hanover, Germany.
¹²³ Regional Health Observatories, Oran, Algeria.
¹²⁴ Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, USA.
¹²⁵ Madagascar Health and Environmental Research (MAHERY), Maroantsetra, Madagascar.
¹²⁶ Francis Schaffner Consultancy, Riehen, Switzerland.
¹²⁷ National Centre for Vector Entomology, Institute of Parasitology, Vetsuisse Faculty, University of Zürich, Zürich, Switzerland.
¹²⁸ Mosquito and Vector Management District of Santa Barbara County, Summerland, CA, USA.
¹²⁹ Department of Genetics and Cell Biology, Tomsk State University, Tomsk, Russia.
¹³⁰ Laboratory of Cell Differentiation Mechanisms, Institute of Cytology and Genetics, Novosibirsk, Russia.
¹³¹ San Francisco Department of Public Health, San Francisco, CA, USA.
¹³² Department of Biology, Plant Protection and Quarantine, S.Seifullin Kazakh Agrotechnical Research University, Astana, Kazakhstan.
¹³³ Department of General Biology and Genomics, Eurasian National University, Astana, Kazakhstan.
¹³⁴ Royal Museum for Central Africa, Tervuren, Belgium.
¹³⁵ Faculty of Agriculture, Forestry and Natural Environment, School of Agriculture, Laboratory of Applied Zoology and Parasitology, Aristotle University of Thessaloniki, Thessaloniki, Greece.
¹³⁶ Unité d'Entomologie Médicale, Institut Pasteur de Madagascar, Antananarivo, Madagascar.
¹³⁷ Kern Mosquito and Vector Control District, Bakersfield, CA, USA.
¹³⁸ Department of International and Global Studies, Mercer University, Macon, GA, USA.
¹³⁹ Department of Public Health, Institute of Environmental and Occupational Health Sciences, College of Public Health, National Taiwan University, Taipei, Taiwan.
¹⁴⁰ Outbreak Research Team, Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium.
¹⁴¹ Emerging Viral Threats, One Health Vaccines and Surveillance (EVITOH) Division, Infectious Disease and Oncology Research Institute (IDORI), University of the Witwatersrand, Johannesburg, South Africa.
¹⁴² Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA.
¹⁴³ Laboratory of Parasitology, The State Scientific and Production Amalgamation, The Scientific and Practical Center of the National Academy of Sciences of Belarus for Biological Resources, Belarus, Minsk.
¹⁴⁴ Institute Molecular Biology Biotechnology Foundation for Research and Technology, Heraklion, Crete, Greece.
¹⁴⁵ Sacramento-Yolo Mosquito and Vector Control District, Elk Grove, CA, USA.
¹⁴⁶ Vector Biology Department, Liverpool School of Tropical Medicine, Liverpool, UK.
¹⁴⁷ Wuhan Center for Disease Control and Prevention, Wuhan, China.
¹⁴⁸ Institute of Environmental and Occupational Health Sciences, College of Public Health, National Taiwan University, Taipei, Taiwan.
¹⁴⁹ Division Limnology, Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, Austria.

PMID: 41129649
DOI: 10.1126/science.ady4515

Ancient origin of an urban underground mosquito

Yuki Haba et al. Science. 2025.

. 2025 Oct 23;390(6771):eady4515.

doi: 10.1126/science.ady4515. Epub 2025 Oct 23.

Authors

Affiliations

¹ Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA.
² Princeton Neuroscience Institute, Princeton University, Princeton, NJ, USA.
³ Wellcome Sanger Institute, Hinxton, UK.
⁴ Department of Life Sciences, The Natural History Museum, London, UK.
⁵ Department of Biology and Howard Hughes Medical Institute, Stanford University, Stanford, CA, USA.
⁶ Department of Biology, Montclair State University, Montclair, NJ, USA.
⁷ Global Health and Tropical Medicine, GHTM, LA-REAL, Instituto de Higiene e Medicina Tropical, Universidade NOVA de Lisboa, Lisboa, Portugal.
⁸ DeKalb County Board of Health, Decatur, GA, USA.
⁹ Shasta Mosquito and Vector Control District, Anderson, CA, USA.
¹⁰ Public Health Unit USP Francisco George, Primary Medical Healthcare Cluster Lisbon North, Largo Professor Arnaldo Sampaio, Lisboa, Portugal.
¹¹ ASTRE, UMR 117, INRAE-CIRAD, Montpellier, France.
¹² Hacettepe University, Faculty of Science, Department of Biology, VERG Laboratories, Beytepe, Ankara, Turkey.
¹³ Institut des Sciences de l'Évolution de Montpellier (UMR 5554, CNRS-UM-IRD-EPHE), Université de Montpellier, Montpellier, France.
¹⁴ Bernhard-Nocht-Institute for Tropical Medicine, Bernhard Nocht Str. 74, Hamburg, Germany.
¹⁵ Laboratory of Health and Environment, Faculty of Life and Natural Sciences and of Earth and Universe Sciences, Mohamed El Bachir El Ibrahimi University, Bordj Bou Arreridj, Algeria.
¹⁶ Institute of Plant Breeding and Genetic Resources, Hellenic Agricultural Organization - DIMITRA, Thermi, Greece.
¹⁷ Southern Nevada Health District, Las Vegas, NV, USA.
¹⁸ Service de Parasitologie et des Maladies Vectorielles, Institut Pasteur du Maroc, Casablanca, Morocco.
¹⁹ Department of Entomology, University of Maryland, College Park, MD, USA.
²⁰ University of Reunion Island, UMR PIMIT (Processus Infectieux en Milieu Insulaire Tropical) CNRS 9192, INSERM 1187, IRD 249, University of Reunion Island, Reunion Island, France.
²¹ Institut Pasteur, Université Paris Cité, CNRS UMR2000, Insect-Virus Interactions Unit, Paris, France.
²² Max Planck Tandem Group in Mosquito Reproductive Biology, Universidad de Antioquia, Medellín, Colombia.
²³ MIVEGEC, University of Montpellier, CNRS, IRD, Montpellier, France.
²⁴ CIRMF, Franceville, Gabon.
²⁵ Department of Zoology, Faculty of Science, University of Khartoum, Khartoum, Sudan.
²⁶ National Center of Disease Control and Prevention, Ministry of Health, Yerevan, Republic of Armenia.
²⁷ E7 Ministry of Environmental Protection, Ramla, Israel.
²⁸ Center for Organismal Studies, University of Heidelberg, Heidelberg, Germany.
²⁹ German Mosquito Control Association, Speyer, Germany.
³⁰ Laboratory of Experimental Biology and Biotechnology, Scientific and Educational Center in Chernogolovka, Federal State University of Education, Moscow, Russia.
³¹ Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, Russia.
³² County of San Diego, Vector Control Program, San Diego, CA, USA.
³³ Ministry of Health, Jerusalem, Israel.
³⁴ Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, USA.
³⁵ Entomology Unit, Laboratory of Parasitology, Pasteur Institute of Algeria, Algiers, Algeria.
³⁶ Institute of Ecology and Evolution, 5289 University of Oregon, Eugene, OR, USA.
³⁷ Parasitología, Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad de Extremadura, Cáceres, Spain.
³⁸ Department of Animal Health Department (Parasitology and Parasitic Diseases), Faculty of Veterinary Medicine, University of Córdoba, Sanidad Animal Building, Rabanales Campus, Córdoba, Spain.
³⁹ European Center of Excellence for Vector Control, Laboratorios Lokímica - Rentokil Initial, Valencia, Spain.
⁴⁰ Department of Biology, Josip Juraj Strossmayer University of Osijek, Osijek, Croatia.
⁴¹ Department of Virus Ecology, Institute of Virology, Biomedical Research Center Slovak Academy of Sciences, Bratislava, Slovakia.
⁴² Department of Public Health and Infectious Diseases, Sapienza University, Rome, Italy.
⁴³ Ecología de Enfermedades Transmitidas por Vectores, Instituto de Investigación e Ingeniería Ambiental, UNSAM, CONICET, Buenos Aires, Argentina.
⁴⁴ The Pirbright Institute, Ash Road, Woking, Surrey, UK.
⁴⁵ Faculty of Veterinary Medicine, Research Institute of Biomedical and Health Sciences, University of Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Spain.
⁴⁶ Centre Suisse de Recherches Scientifiques en Côte d'Ivoire, Abidjan, Côte d'Ivoire.
⁴⁷ Wits Research Institute for Malaria, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
⁴⁸ Centre for Emerging Zoonotic and Parasitic Diseases, National Institute for Communicable Diseases, Johannesburg, South Africa.
⁴⁹ Department of Evolution and Ecology, University of California, Davis, CA, USA.
⁵⁰ Kearney Agricultural Research and Extension Center, Parlier, CA, USA.
⁵¹ University of Helsinki, Medicum, Department of Virology, Helsinki, Finland.
⁵² Faculty of Agriculture, Centre of Excellence One Health Vectors and Climate, Laboratory for Medical and Veterinary Entomology, University of Novi Sad, Novi Sad, Serbia.
⁵³ Entomology Unit, Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium.
⁵⁴ Consolidated Mosquito Abatement District, Parlier, CA, USA.
⁵⁵ Department of Animal Pathology, Faculty of Veterinary Medicine at the University of Zaragoza, Zaragoza, Spain.
⁵⁶ Zoological Institute and Museum, University of Greifswald, Greifswald, Germany.
⁵⁷ Aklilu Lemma Institute of Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia.
⁵⁸ Santa Clara County Vector Control District, San Jose, CA, USA.
⁵⁹ Département Faune et Actions de Salubrité, Service Parisien de Santé Environnementale, Direction de la Santé Publique, Ville de Paris, Paris, France.
⁶⁰ Biology Department, College of Science, Imam Abdulrahman bin Faisal University, Dammam, Kingdom of Saudi Arabia.
⁶¹ Salt Lake City Mosquito Abatement District, Salt Lake City, UT, USA.
⁶² Сentral Research Institute for Epidemiology, Moscow, Russia.
⁶³ Center for Vector Biology, Rutgers University, New Brunswick, NJ, USA.
⁶⁴ Northeast Massachusetts Mosquito Control District, Georgetown, MA, USA.
⁶⁵ Istituto Zooprofilattico Sperimentale della Sardegna, Sassari, Italy.
⁶⁶ Department of Biology, Southern Nazarene University, Bethany, OK, USA.
⁶⁷ STEM, University of South Australia, Adelaide, South Australia, Australia.
⁶⁸ Medical Entomology, Centre for Disease Control and Environmental Health, NT Health, NT, Australia.
⁶⁹ Institute of Parasitology, Department of Pathobiology, University of Veterinary Medicine, Vienna, Austria.
⁷⁰ Department of Vector Ecology and Environment, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan.
⁷¹ Department of Entomology, Faculty of Science, Ain Shams University, Abbassia, Cairo, Egypt.
⁷² Medical Entomology Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.
⁷³ Department of General Biology and Ecology, Federal State University of Education, Moscow, Russia.
⁷⁴ Swiss Tropical and Public Health Institute, Allschwil, Switzerland.
⁷⁵ University of Basel, Basel, Switzerland.
⁷⁶ Centre for Emerging and Reemerging Arbo and Respiratory Virus Research (CEARV), Department Medical Virology, University of Pretoria, South Africa.
⁷⁷ Department of Production Animal Studies, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, South Africa.
⁷⁸ Medical Entomology Unit, Infectious Disease Research Centre, Institute For Medical Research, National Institutes of Health, Kuala Lumpur, Malaysia.
⁷⁹ Ministry of Environmental Protection, Jerusalem, Israel.
⁸⁰ Walter Reed Army Institute of Research, Silver Spring, MD, USA.
⁸¹ Environment, CSIRO, Canberra, Australia.
⁸² Placer Mosquito and Vector Control District, Roseville, CA, USA.
⁸³ Department of Medical Biochemistry and Microbiology/Zoonosis Science Center, Uppsala University, Uppsala, Sweden.
⁸⁴ Biologisk Myggkontroll, Nedre Dalälven Utvecklings AB, Uppsala, Sweden.
⁸⁵ Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan.
⁸⁶ Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Cluj-Napoca, Romania.
⁸⁷ Vector Control Unit, Department of Epidemiology and Control of Infectious Diseases, Institute of Public Health, Tirana, Albania.
⁸⁸ Department of Pest Control Projects, Dallah Company, Jeddah, Kingdom of Saudi Arabia.
⁸⁹ Department of Biological Sciences, The University of Texas at El Paso, El Paso, TX, USA.
⁹⁰ Institute of Cytology and Genetics, Novosibirsk, Russia.
⁹¹ Institute of Zoology and Institute of Parasitology, Centre for Infection Medicine, University of Veterinary Medicine Hannover, Hanover, Germany.
⁹² Force Health Protection and Preventive Medicine, Medical Department Activity-Korea/65th Medical Brigade, Unit 15281, APO AP 96271-5281, USA.
⁹³ Department of Crop Science, Agricultural University of Athens, Athens, Greece.
⁹⁴ Croatian Institute for Public Health of Međimurje County, Čakovec, Croatia.
⁹⁵ Department of Epidemiology, Andrija Stampar Teaching Institute of Public Health, Zagreb, Croatia.
⁹⁶ Washington State Department of Health, Olympia, WA, USA.
⁹⁷ Laboratory of Entomology, Wageningen University and Research, Wageningen, Netherlands.
⁹⁸ Centers for Disease Control and Prevention, Fort Collins, CO, USA.
⁹⁹ Institut Universitaire de France, Paris, France.
¹⁰⁰ Nature and Parks Authority, Jerusalem, Israel.
¹⁰¹ Institute of Public Health of the Istrian County, Pula, Croatia.
¹⁰² Department of Plant Pathology, Entomology and Microbiology Iowa State University, Ames, IA, USA.
¹⁰³ Australian National Insect Collection, National Research Collections Australia, CSIRO, Canberra, Australia.
¹⁰⁴ Zoonotic Arbo- and Respiratory Virus Program, Centre for Viral Zoonoses, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa.
¹⁰⁵ Illinois Natural History Survey, Prairie Research Institute, University of Illinois at Urbana-Champaign, Champaign, IL, USA.
¹⁰⁶ Department of Biology, Eastern Washington University, Cheney, WA, USA.
¹⁰⁷ School of Health, Medicine and Life Sciences, University of Hertfordshire, Hatfield, Hertfordshire, UK.
¹⁰⁸ Mpala Research Centre, Nanyuki, Kenya.
¹⁰⁹ Department of Entomology and Fralin Life Sciences Institute, Virginia Polytechnic and State University, Blacksburg, VA, USA.
¹¹⁰ Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO, USA.
¹¹¹ Miami-Dade County Mosquito Control, Miami, FL, USA.
¹¹² Antelope Valley Mosquito and Vector Control District, Lancaster, CA, USA.
¹¹³ Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovakia.
¹¹⁴ Laboratorio di Entomologia Sanitaria e Patogeni Trasmessi da Vettori, Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Italy.
¹¹⁵ Department of Infectious Diseases, Center of Rickettsiosis and Arthropod-Borne Diseases (CRETAV), San Pedro University Hospital-Center for Biomedical Research from La Rioja (CIBIR), Logroño, Spain.
¹¹⁶ Research Center for the Pacific Islands, Kagoshima University, Kagoshima, Japan.
¹¹⁷ Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Valenzano, Italy.
¹¹⁸ Parasitology and Mediterranean Ecoepidemiology Research Group, University of the Balearic Islands, Palma, Spain.
¹¹⁹ Anastasia Mosquito Control District of St. Johns County, Augustine, FL, USA.
¹²⁰ Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias. Universidad de La Laguna, Tenerife, Spain.
¹²¹ Applied Zoology and Nature Conservation, University of Greifswald, Greifswald, Germany.
¹²² Institute of Zoology, University of Veterinary Medicine Hannover, Hanover, Germany.
¹²³ Regional Health Observatories, Oran, Algeria.
¹²⁴ Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, USA.
¹²⁵ Madagascar Health and Environmental Research (MAHERY), Maroantsetra, Madagascar.
¹²⁶ Francis Schaffner Consultancy, Riehen, Switzerland.
¹²⁷ National Centre for Vector Entomology, Institute of Parasitology, Vetsuisse Faculty, University of Zürich, Zürich, Switzerland.
¹²⁸ Mosquito and Vector Management District of Santa Barbara County, Summerland, CA, USA.
¹²⁹ Department of Genetics and Cell Biology, Tomsk State University, Tomsk, Russia.
¹³⁰ Laboratory of Cell Differentiation Mechanisms, Institute of Cytology and Genetics, Novosibirsk, Russia.
¹³¹ San Francisco Department of Public Health, San Francisco, CA, USA.
¹³² Department of Biology, Plant Protection and Quarantine, S.Seifullin Kazakh Agrotechnical Research University, Astana, Kazakhstan.
¹³³ Department of General Biology and Genomics, Eurasian National University, Astana, Kazakhstan.
¹³⁴ Royal Museum for Central Africa, Tervuren, Belgium.
¹³⁵ Faculty of Agriculture, Forestry and Natural Environment, School of Agriculture, Laboratory of Applied Zoology and Parasitology, Aristotle University of Thessaloniki, Thessaloniki, Greece.
¹³⁶ Unité d'Entomologie Médicale, Institut Pasteur de Madagascar, Antananarivo, Madagascar.
¹³⁷ Kern Mosquito and Vector Control District, Bakersfield, CA, USA.
¹³⁸ Department of International and Global Studies, Mercer University, Macon, GA, USA.
¹³⁹ Department of Public Health, Institute of Environmental and Occupational Health Sciences, College of Public Health, National Taiwan University, Taipei, Taiwan.
¹⁴⁰ Outbreak Research Team, Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium.
¹⁴¹ Emerging Viral Threats, One Health Vaccines and Surveillance (EVITOH) Division, Infectious Disease and Oncology Research Institute (IDORI), University of the Witwatersrand, Johannesburg, South Africa.
¹⁴² Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA.
¹⁴³ Laboratory of Parasitology, The State Scientific and Production Amalgamation, The Scientific and Practical Center of the National Academy of Sciences of Belarus for Biological Resources, Belarus, Minsk.
¹⁴⁴ Institute Molecular Biology Biotechnology Foundation for Research and Technology, Heraklion, Crete, Greece.
¹⁴⁵ Sacramento-Yolo Mosquito and Vector Control District, Elk Grove, CA, USA.
¹⁴⁶ Vector Biology Department, Liverpool School of Tropical Medicine, Liverpool, UK.
¹⁴⁷ Wuhan Center for Disease Control and Prevention, Wuhan, China.
¹⁴⁸ Institute of Environmental and Occupational Health Sciences, College of Public Health, National Taiwan University, Taipei, Taiwan.
¹⁴⁹ Division Limnology, Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, Austria.

PMID: 41129649
DOI: 10.1126/science.ady4515

Abstract

Understanding how life is adapting to urban environments represents an important challenge in evolutionary biology. In this work, we investigate a widely cited example of urban adaptation, Culex pipiens form molestus, also known as the London Underground mosquito. Population genomic analysis of ~350 contemporary and historical samples counters the popular hypothesis that molestus originated belowground in London <200 years ago. Instead, we show that molestus first adapted to human environments aboveground in the Mediterranean or Middle East over the course of more than 1000 years, possibly in association with ancient agricultural civilizations of the Middle East. Our results highlight the role of early human society in priming taxa for contemporary urban evolution. They also provide insight into whether and how molestus contributes to West Nile virus transmission in modern cities.

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Update of

Ancient origin of an urban underground mosquito.
Haba Y, Aardema ML, Afonso MO, Agramonte NM, Albright J, Alho AM, Almeida APG, Alout H, Alten B, Altinli M, Amara Korba R, Andreadis SS, Anghel V, Arich S, Arsenault-Benoit A, Atyame C, Aubry F, Avila FW, Ayala D, Azrag RS, Babayan L, Bear A, Becker N, Bega AG, Bejarano S, Ben-Avi I, Benoit JB, Boubidi SC, Bradshaw WE, Bravo-Barriga D, Bueno-Marí R, Bušić N, Čabanová V, Cabeje B, Caputo B, Cardo MV, Carpenter S, Carreton E, Chouaïbou MS, Christian M, Coetzee M, Conner WR, Cornel A, Culverwell CL, Cupina AI, De Wolf K, Deblauwe I, Deegan B, Delacour-Estrella S, Torre AD, Diaz D, Dool SE, Dos Anjos VL, Dugassa S, Ebrahimi B, Eisa SYM, Elissa N, Fallatah SAB, Faraji A, Fedorova MV, Ferrill E, Fonseca DM, Foss KA, Foxi C, França CM, Fricker SR, Fritz ML, Frontera E, Fuehrer HP, Futami K, Ghallab EHS, Girod R, Gordeev MI, Greer D, Gschwind M, Guarido MM, Guat Ney T, Gunay F, Haklay E, Hamad AAE, Hang J, Hardy CM, Hartle JW, Hesson JC, Higa Y, Holzapfel CM, Honnen AC, Ionica AM, Jones L, Kadriaj P, Kamal HA, Kamdem C, Karagodin DA, Kasai S, Kavran M, Khater EIM, Kiene F, Kim HC, Kioulos I, Klein A, Klemenčić M, Klobučar A, Knutson E, Koenraadt CJM, Kothera L, Kreienbühl P, Labbé P, Lach… See abstract for full author list ➔ Haba Y, et al. bioRxiv [Preprint]. 2025 Feb 5:2025.01.26.634793. doi: 10.1101/2025.01.26.634793. bioRxiv. 2025. Update in: Science. 2025 Oct 23;390(6771):eady4515. doi: 10.1126/science.ady4515. PMID: 39975080 Free PMC article. Updated. Preprint.

Comment in

Urban pests traveled with ancient humans.
Munshi-South J, Evankow A. Munshi-South J, et al. Science. 2025 Oct 23;390(6771):335-336. doi: 10.1126/science.aec1986. Epub 2025 Oct 23. Science. 2025. PMID: 41129657

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Ancient origin of an urban underground mosquito

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Ancient origin of an urban underground mosquito

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