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Ancient origin of an urban underground mosquito

Haba Y 1 , Aardema ML 2 , Afonso MO 3 , Agramonte NM 4 , Albright J 5 , Alho AM 6 Show all authors , Almeida APG 3 , Alout H 7 , Alten B 8 , Altinli M 9 , Amara Korba R 10 , Andreadis SS 11 , Anghel V 12 , Arich S 9 , Arsenault-Benoit A 13 , Atyame C 14 , Aubry F 15 , Avila FW 16 , Ayala D 17 , Azrag RS 18 , Babayan L 19 , Bear A 20 , Becker N 21 , Bega AG 22 , Bejarano S 23 , Ben-Avi I 24 , Benoit JB 25 , Boubidi SC 26 , Bradshaw WE 27 , Bravo-Barriga D 28 , Bueno-Marí R 29 , Bušić N 30 , Čabanová V 31 , Cabeje B 23 , Caputo B 32 , Cardo MV 33 , Carpenter S 34 , Carreton E 35 , Chouaïbou MS 36 , Christian M 23 , Coetzee M 37 , Conner WR 38 , Cornel A 39 , Culverwell CL 40 , Cupina AI 41 , De Wolf K 42 , Deblauwe I 42 , Deegan B 43 , Delacour-Estrella S 44 , Torre AD 32 , Diaz D 24 , Dool SE 45 , Dos Anjos VL 1 , Dugassa S 46 , Ebrahimi B 47 , Eisa SYM 18 , Elissa N 48 , Fallatah SAB 49 , Faraji A 50 , Fedorova MV 51 , Ferrill E 23 , Fonseca DM 52 , Foss KA 53 , Foxi C 54 , França CM 55 , Fricker SR 56 , Fritz ML 13 , Frontera E 28 , Fuehrer HP 57 , Futami K 58 , Ghallab EHS 59 , Girod R 60 , Gordeev MI 61 , Greer D 12 , Gschwind M 62 , Guarido MM 63 , Guat Ney T 64 , Gunay F 8 , Haklay E 65 , Hamad AAE 18 , Hang J 66 , Hardy CM 67 , Hartle JW 68 , Hesson JC 69 , Higa Y 70 , Holzapfel CM 27 , Honnen AC 62 , Ionica AM 71 , Jones L 34 , Kadriaj P 72 , Kamal HA 73 , Kamdem C 74 , Karagodin DA 75 , Kasai S 70 , Kavran M 41 , Khater EIM 59 , Kiene F 76 , Kim HC 77 , Kioulos I 78 , Klein A 76 , Klemenčić M 79 , Klobučar A 80 , Knutson E 81 , Koenraadt CJM 82 , Kothera L 83 , Kreienbühl P 15 , Labbé P 9 , Lachmi I 84 , Lambrechts L 15 , Landeka N 85 , Lee CH 86 , Lessard BD 87 , Leycegui I 12 , Lundström JO 69 , Lustigman Y 84 , MacIntyre C 88 , Mackay AJ 89 , Magori K 90 , Maia C 3 , Malcolm CA 91 , Marquez RO 23 , Martins D 92 , Masri RA 93 , McDivitt G 23 , McMinn RJ 94 , Medina J 95 , Mellor KS 96 , Mendoza J 23 , Merdić E 30 , Mesler S 23 , Mestre C 9 , Miranda H 23 , Miterpáková M 97 , Montarsi F 98 , Moskaev AV 22 , Mu T 1 , Möhlmann TWR 82 , Namias A 9 , Ng'iru I 92 , Ngangué MF 99 , Novo MT 3 , Orshan L 24 , Oteo JA 100 , Otsuka Y 101 , Panarese R 102 , Paredes-Esquivel C 103 , Paronyan L 19 , Peper ST 104 , Petrić DV 41 , Pilapil K 23 , Pou-Barreto C 105 , Puechmaille SJ 9 , Radespiel U 106 , Rahola N 17 , Raman VK 12 , Redouane H 107 , Reiskind MH 108 , Reissen NM 50 , Rice BL 1 , Robert V 17 , Ruiz-Arrondo I 100 , Salamat R 23 , Salamone A 81 , Sarih M 109 , Satta G 54 , Sawabe K 70 , Schaffner F 110 , Schultz KE 111 , Shaikevich EV 112 , Sharakhov IV 93 , Sharakhova MV 93 , Shatara N 113 , Sibataev AK 114 , Sicard M 9 , Smith E 25 , Smith RC 86 , Smitz N 115 , Soriano N 23 , Spanoudis CG 116 , Stone CM 89 , Studentsky L 24 , Sulesco T 117 , Tantely LM 118 , Thao K 119 , Tietze N 47 , Tokarz RE 120 , Tsai KH 121 , Tsuda Y 70 , Turić N 30 , Uhran MR 25 , Unlu I 95 , Van Bortel W 42 , Vardanyan H 19 , Vavassori L 62 , Velo E 72 , Venter M 63 , Vignjević G 30 , Vogels CBF 82 , Volkava T 122 , Vontas J 78 , Ward HM 104 , Ahmad NW 64 , Weill M 9 , West JD 68 , Wheeler SS 123 , White GS 50 , Wipf NC 62 , Wu TP 124 , Yu KD 125 , Zimmermann E 106 , Zittra C 126 , Korlević P 127 , McAlister E 128 , Lawniczak MKN 127 , Schumer M 129 , Rose NH 1 , McBride CS 1

Affiliations 

  • 1 Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA
  • 2 Department of Biology, Montclair State University, Montclair, NJ, USA
  • 3 Global Health and Tropical Medicine, GHTM, LA-REAL, Instituto de Higiene e Medicina Tropical, Universidade NOVA de Lisboa, Lisboa, Portugal
  • 4 DeKalb County Board of Health, Decatur, GA, USA
  • 5 Shasta Mosquito and Vector Control District, Anderson, CA 96007, USA
  • 6 Public Health Unit USP Francisco George, Primary Medical Healthcare Cluster Lisbon North, Largo Professor Arnaldo Sampaio, 1549-010 Lisboa, Portugal
  • 7 ASTRE, UMR 117, INRAE-CIRAD, Montpellier, France
  • 8 Hacettepe University, Faculty of Science, Department of Biology, VERG Laboratories, Beytepe, Ankara, Turkey
  • 9 Institut des Sciences de l'Évolution de Montpellier (UMR 5554, CNRS-UM-IRD-EPHE), Université de Montpellier, Montpellier, 34095, France
  • 10 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, 34030, Algeria
  • 11 Institute of Plant Breeding and Genetic Resources, Hellenic Agricultural Organization - DIMITRA, 57001 Thermi, Greece
  • 12 Southern Nevada Health District, Las Vegas, NV 89107, USA
  • 13 Department of Entomology, University of Maryland, College Park, MD 20742, USA
  • 14 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
  • 15 Institut Pasteur, Université Paris Cité, CNRS UMR2000, Insect-Virus Interactions Unit, 75015 Paris, France
  • 16 Max Planck Tandem Group in Mosquito Reproductive Biology, Universidad de Antioquia, Medellín, 050010, Colombia
  • 17 MIVEGEC, University of Montpellier, CNRS, IRD, 34394 Montpellier, France
  • 18 Department of Zoology, Faculty of Science, University of Khartoum, Khartoum, Sudan
  • 19 National Center of Disease Control and Prevention, Ministry of Health, Yerevan 0025, Republic of Armenia
  • 20 E7 Ministry of Environmental Protection, Ramla, Israel
  • 21 Center for Organismal Studies, University of Heidelberg, Heidelberg, Germany
  • 22 Laboratory of Experimental Biology and Biotechnology, Scientific and Educational Center in Chernogolovka, Federal State University of Education, Moscow 105005, Russia
  • 23 County of San Diego, Vector Control Program, San Diego, CA 92123, USA
  • 24 Ministry of Health, Jerusalem, Israel
  • 25 Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45211, USA
  • 26 Entomology Unit, Laboratory of Parasitology, Pasteur Institute of Algeria, Algiers, Algeria
  • 27 Institute of Ecology and Evolution, 5289 University of Oregon, Eugene, OR 97403-5289, USA
  • 28 Parasitología, Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad de Extremadura, Cáceres, Spain
  • 29 European Center of Excellence for Vector Control, Laboratorios Lokímica - Rentokil Initial, Valencia, Spain
  • 30 Department of Biology, Josip Juraj Strossmayer University of Osijek, Osijek, 31000, Croatia
  • 31 Department of Virus Ecology, Institute of Virology, Biomedical Research Center Slovak Academy of Sciences, Bratislava, 845 05, Slovakia
  • 32 Department of Public Health and Infectious Diseases, Sapienza University, Rome, 00185, Italy
  • 33 Ecología de Enfermedades Transmitidas por Vectores, Instituto de Investigación e Ingeniería Ambiental, UNSAM, CONICET, Buenos Aires, Argentina
  • 34 The Pirbright Institute, Ash Road, Woking, Surrey, GU24 0NF, UK
  • 35 Faculty of Veterinary Medicine, Research Institute of Biomedical and Health Sciences, University of Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Spain
  • 36 Centre Suisse de Recherches Scientifiques en Côte d'Ivoire, Abidjan 1301, Côte d'Ivoire
  • 37 Wits Research Institute for Malaria, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
  • 38 Department of Evolution and Ecology, University of California, Davis, CA 95616, USA
  • 39 Kearney Agricultural Research and Extension Center, Parlier, CA 93648, USA
  • 40 University of Helsinki, Medicum, Department of Virology, Helsinki 00014, Finland
  • 41 Faculty of Agriculture, Centre of Excellence One Health Vectors and Climate, Laboratory for Medical and Veterinary Entomology, University of Novi Sad, 21101 Novi Sad, Serbia
  • 42 Entomology Unit, Department of Biomedical Sciences, Institute of Tropical Medicine, 2000 Antwerp, Belgium
  • 43 Consolidated Mosquito Abatement District, Parlier, CA 93648, USA
  • 44 Department of Animal Pathology, Faculty of Veterinary Medicine at the University of Zaragoza, Zaragoza, Spain
  • 45 Zoological Institute and Museum, University of Greifswald, Greifswald, 17489, Germany
  • 46 Aklilu Lemma Institute of Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia
  • 47 Santa Clara County Vector Control District, San Jose, CA 95112, USA
  • 48 Département Faune et Actions de Salubrité, Service Parisien de Santé Environnementale, Direction de la Santé Publique, Ville de Paris, Paris 75019, France
  • 49 Biology Department, College of Science, Imam Abdulrahman bin Faisal University, Dammam 31113, Kingdom of Saudi Arabia
  • 50 Salt Lake City Mosquito Abatement District, Salt Lake City, UT 84116, USA
  • 51 Сentral Research Institute for Epidemiology, Moscow, 111123, Russia
  • 52 Center for Vector Biology, Rutgers University, New Brunswick, NJ, USA
  • 53 Northeast Massachusetts Mosquito Control District, 118 Tenney Street, Georgetown, MA 01833, USA
  • 54 Istituto Zooprofilattico Sperimentale della Sardegna, 07100, Sassari, Italy
  • 55 Department of Biology, Southern Nazarene University, Bethany, OK, USA
  • 56 STEM, University of South Australia, Adelaide, South Australia, 5000, Australia
  • 57 Institute of Parasitology, Department of Pathobiology, University of Veterinary Medicine, 1210 Vienna, Austria
  • 58 Department of Vector Ecology and Environment, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan
  • 59 Department of Entomology, Faculty of Science, Ain Shams University, Abbassia, Cairo 11566, Egypt
  • 60 Medical Entomology Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar
  • 61 Department of General Biology and Ecology, Federal State University of Education, 105005 Moscow, Russia
  • 62 Swiss Tropical and Public Health Institute, Allschwil, Switzerland
  • 63 Centre for Emerging and Reemerging Arbo and Respiratory Virus Research (CEARV), Department Medical Virology, University of Pretoria, South Africa
  • 64 Medical Entomology Unit, Infectious Disease Research Centre, Institute For Medical Research, National Institutes of Health, Jalan Pahang 50588, Kuala Lumpur, Malaysia
  • 65 Ministry of Environmental Protection, Jerusalem, Israel
  • 66 Walter Reed Army Institute of Research, Silver Spring, MD 20910, USA
  • 67 Environment, CSIRO, Canberra, Australia
  • 68 Placer Mosquito & Vector Control District, Roseville, CA 95678, USA
  • 69 Department of Medical Biochemistry and Microbiology/Zoonosis Science Center, Uppsala University, Uppsala, SE-75123, Sweden
  • 70 Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo 162-8640, Japan
  • 71 Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, 400372, Cluj-Napoca, Romania
  • 72 Vector Control Unit, Department of Epidemiology and Control of Infectious Diseases, Institute of Public Health, Tirana, Albania
  • 73 Department of Pest Control Projects, Dallah Company, Jeddah, Kingdom of Saudi Arabia
  • 74 Department of Biological Sciences, The University of Texas at El Paso, 500 W. University Ave., El Paso, TX 79968, USA
  • 75 Institute of Cytology and Genetics, Novosibirsk, Russia
  • 76 Institute of Zoology and Institute of Parasitology, Centre for Infection Medicine, University of Veterinary Medicine Hannover, 30559 Hanover, Germany
  • 77 Force Health Protection and Preventive Medicine, Medical Department Activity-Korea/65th Medical Brigade, Unit 15281, APO AP 96271-5281, USA
  • 78 Department of Crop Science, Agricultural University of Athens, 11855, Athens, Greece
  • 79 Croatian Institute for Public Health of Međimurje County, 40000 Čakovec, Croatia
  • 80 Department of Epidemiology, Andrija Stampar Teaching Institute of Public Health, Zagreb, 10000, Croatia
  • 81 Washington State Department of Health, Olympia, WA 98504, USA
  • 82 Laboratory of Entomology, Wageningen University & Research, Wageningen, The Netherlands
  • 83 Centers for Disease Control and Prevention, Fort Collins, CO, USA
  • 84 Nature and Parks Authority, Jerusalem, Israel
  • 85 Institute of Public Health of the Istrian County, 52100 Pula, Croatia
  • 86 Department of Plant Pathology, Entomology and Microbiology Iowa State University, Ames, IA 50011, USA
  • 87 Australian National Insect Collection, National Research Collections Australia, CSIRO, Canberra, Australia
  • 88 Zoonotic Arbo- and Respiratory Virus Program, Centre for Viral Zoonoses, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa
  • 89 Illinois Natural History Survey, Prairie Research Institute, University of Illinois at Urbana-Champaign, Champaign, IL 61820, USA
  • 90 Department of Biology, Eastern Washington University, Cheney, WA 99004, USA
  • 91 School of Health, Medicine and Life Sciences, University of Hertfordshire, Hatfield, Hertfordshire, AL10 9AB, United Kingdom
  • 92 Mpala Research Centre, 555-10400, Nanyuki, Kenya
  • 93 Department of Entomology and Fralin Life Sciences Institute, Virginia Polytechnic and State University, Blacksburg, VA 24061, USA
  • 94 Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO, USA
  • 95 Miami-Dade County Mosquito Control, Miami, FL 33178, USA
  • 96 Antelope Valley Mosquito & Vector Control District, Lancaster, CA 93535, USA
  • 97 Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovakia
  • 98 Laboratorio di Entomologia Sanitaria e Patogeni Trasmessi da Vettori, Istituto Zooprofilattico Sperimentale delle Venezie, 35020, Legnaro, Italy
  • 99 CIRMF, Franceville, Gabon
  • 100 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, 26006, Spain
  • 101 Research Center for the Pacific Islands, Kagoshima University, Kagoshima, Japan
  • 102 Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, 70010, Valenzano, Italy
  • 103 Parasitology and Mediterranean Ecoepidemiology Research Group, University of the Balearic Islands, 07122 Palma, Spain
  • 104 Anastasia Mosquito Control District of St. Johns County, Augustine, FL 32092, USA
  • 105 Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias. Universidad de La Laguna, Tenerife, 38206, Spain
  • 106 Institute of Zoology, University of Veterinary Medicine Hannover, 30559 Hanover, Germany
  • 107 Regional Health Observatories, Oran, Algeria
  • 108 Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27695 USA
  • 109 Service de Parasitologie et des Maladies Vectorielles, Institut Pasteur du Maroc, Casablanca 20360, Morocco
  • 110 Francis Schaffner Consultancy, Riehen, Switzerland
  • 111 Mosquito and Vector Management District of Santa Barbara County, Summerland, CA 93067, USA
  • 112 Vavilov Institute of General Genetics, Russian Academy of Sciences, 119991 Moscow, Russia
  • 113 San Francisco Department of Public Health, San Francisco, CA, USA
  • 114 Department of Biology, Plant Protection and Quarantine, S.Seifullin Kazakh Agrotechnical Research University, Astana, Kazakhstan
  • 115 Royal Museum for Central Africa, Leuvensesteenweg 13, 3080, Tervuren, Belgium
  • 116 Faculty of Agriculture, Forestry and Natural Environment, School of Agriculture, Laboratory of Applied Zoology and Parasitology, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
  • 117 Bernhard-Nocht-Institute for Tropical Medicine, Bernhard Nocht Str. 74, 20359, Hamburg, Germany
  • 118 Unité d'Entomologie Médicale, Institut Pasteur de Madagascar, Antananarivo 101, Madagascar
  • 119 Kern Mosquito & Vector Control District, Bakersfield, CA 93314, USA
  • 120 Department of International and Global Studies, Mercer University, Macon, GA 31207, USA
  • 121 Department of Public Health, Institute of Environmental and Occupational Health Sciences, College of Public Health, National Taiwan University, No. 17, Xu-Zhou Road, Taipei 100025, Taiwan
  • 122 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
  • 123 Sacramento-Yolo Mosquito & Vector Control District, Elk Grove, CA, 95624, USA
  • 124 Wuhan Center for Disease Control and Prevention, Wuhan, China
  • 125 Institute of Environmental and Occupational Health Sciences, College of Public Health, National Taiwan University, Taipei 100, Taiwan
  • 126 Division Limnology, Department of Functional and Evolutionary Ecology, University of Vienna, 1030 Vienna, Austria
  • 127 Wellcome Sanger Institute, Hinxton CB10 1SA, United Kingdom
  • 128 Department of Life Sciences, The Natural History Museum, London, SW7 5BD, UK
  • 129 Department of Biology and Howard Hughes Medical Institute, Stanford University, Stanford, CA, USA
bioRxiv, 2025 Feb 05.
PMID: 39975080 DOI: 10.1101/2025.01.26.634793

Abstract

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, Culex pipiens form molestus, also known as the London Underground Mosquito. Population genomic analysis of ~350 contemporary and historical samples counter the popular hypothesis that molestus originated belowground in London less than 200 years ago. Instead, we show that molestus 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.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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