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The complex swarming dynamics of malaria mosquitoes emerge from simple minimally-interactive behavioral rules.

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Τίτλος: The complex swarming dynamics of malaria mosquitoes emerge from simple minimally-interactive behavioral rules.
Συγγραφείς: Cribellier A; Experimental Zoology Group, Wageningen University, Wageningen, The Netherlands., Poda BS; Experimental Zoology Group, Wageningen University, Wageningen, The Netherlands.; Institut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso, Burkina Faso., Dabiré RK; Institut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso, Burkina Faso., Diabaté A; Institut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso, Burkina Faso., Roux O; MIVEGEC, University of Montpellier, IRD, CNRS, Montpellier, France., Muijres FT; Experimental Zoology Group, Wageningen University, Wageningen, The Netherlands.
Πηγή: PLoS computational biology [PLoS Comput Biol] 2026 Aug 26; Vol. 22 (8), pp. e1014685. Date of Electronic Publication: 2026 Aug 26 (Print Publication: 2026).
Τύπος έκδοσης: Journal Article; Research Support, Non-U.S. Gov't
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Public Library of Science Country of Publication: United States NLM ID: 101238922 Publication Model: eCollection Cited Medium: Internet ISSN: 1553-7358 (Electronic) Linking ISSN: 1553734X NLM ISO Abbreviation: PLoS Comput Biol Subsets: MEDLINE
Imprint Name(s): Original Publication: San Francisco, CA : Public Library of Science, [2005]-
Ιατρικοί όροι (MeSH): Anopheles*/physiology , Malaria*/transmission , Behavior, Animal*/physiology , Mosquito Vectors*/physiology , Models, Biological*, Flight, Animal/physiology ; Sexual Behavior, Animal/physiology ; Animals ; Female ; Male ; Computational Biology ; Computer Simulation
Περίληψη: Swarming is a widespread collective behavior in animals, often thought to emerge from complex interactions among individuals. Here, we show that mating swarms of malaria mosquitoes can emerge from simple behavioral rules with minimal interaction between individuals. We analyzed two published experimental datasets with three-dimensional flight tracks of Anopheles coluzzii mosquitoes swarming in the lab under simulated sunset conditions and above a visual marker. We found that individuals alternate between straight flight and rapid turning maneuvers known as saccades. These saccades are triggered at the edge of the swarm, and their directions are biased along the sunset direction. This behavior was found consistent between both laboratory datasets, including swarming of solitary individuals; this indicates that inter‑individual interactions may play a limited role within the small-to-medium sized swarms that we studied. We developed a simple agent-based model incorporating three behavioral rules: attraction to the swarm center, alignment normal to the sunset horizon, both driven by environmental cues, and repulsion through short-range collision avoidance. This parsimonious model reproduced key features of the observed laboratory mosquito swarms, including looping flight paths, central density peaks, and directional alignment. Even in the absence of direct inter‑individual interactions, the model generated realistic emergent swarm dynamics, suggesting that social coordination is not required for swarm emergence. Although our lab-based findings remain to be confirmed across more naturalistic conditions, they suggest that the most parsimonious hypothesis behind male mosquito swarming is that it is primarily guided by environmental perception rather than social interaction. This minimal framework offers a new perspective on insect swarming and may apply broadly to the many other insect species that form mating swarms. Understanding the behavioral rules of mosquito swarming could inform strategies for vector control and improve the effectiveness of interventions targeting mosquito reproduction.
(Copyright: © 2026 Cribellier et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)
Competing Interests: The authors have declared that no competing interests exist.
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Proc Natl Acad Sci U S A. 2011 Nov 15;108(46):18726-31. (PMID: 22065759)
J Exp Biol. 2022 Mar 1;225(5):. (PMID: 35132997)
Vector Borne Zoonotic Dis. 2010 Apr;10(3):295-311. (PMID: 19725763)
Sci Rep. 2014 Sep 12;4:6318. (PMID: 25212874)
Science. 2020 May 8;368(6491):634-637. (PMID: 32381721)
Phys Rev E. 2022 Mar;105(3-1):034601. (PMID: 35428071)
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Science. 2006 Jun 2;312(5778):1402-6. (PMID: 16741126)
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J Med Entomol. 2013 May;50(3):552-9. (PMID: 23802449)
Philos Trans R Soc Lond B Biol Sci. 2023 Apr 10;378(1874):20220066. (PMID: 36802778)
iScience. 2024 Oct 11;27(11):111164. (PMID: 39524359)
Genetica. 2011 Jan;139(1):33-9. (PMID: 20821345)
Science. 2025 Feb 28;387(6737):995-1000. (PMID: 40014712)
J Med Entomol. 2022 Jan 12;59(1):56-66. (PMID: 34617121)
Interface Focus. 2012 Dec 6;2(6):726-37. (PMID: 24312726)
Trends Parasitol. 2003 Aug;19(8):349-55. (PMID: 12901936)
HFSP J. 2008 Aug;2(4):205-19. (PMID: 19404431)
Sci Rep. 2026 Jul 9;:. (PMID: 42426113)
Biol Lett. 2011 Oct 23;7(5):692-4. (PMID: 21525051)
J R Soc Interface. 2019 Jan 31;16(150):20180739. (PMID: 30958145)
Curr Biol. 2014 Sep 22;24(18):R828-R830. (PMID: 25247351)
Interface Focus. 2012 Dec 6;2(6):693-707. (PMID: 24312723)
J R Soc Interface. 2022 Aug;19(193):20220285. (PMID: 36000227)
Eur Phys J E Soft Matter. 2017 Apr;40(4):46. (PMID: 28417322)
J Exp Biol. 2011 Oct 15;214(Pt 20):3480-94. (PMID: 21957112)
J Med Entomol. 2009 Mar;46(2):227-35. (PMID: 19351073)
J R Soc Interface. 2022 Aug;19(193):20220258. (PMID: 36043287)
Trends Biotechnol. 2023 Feb;41(2):154-164. (PMID: 35868886)
J Med Entomol. 2023 Sep 12;60(5):857-864. (PMID: 37392071)
Sci Rep. 2013;3:1073. (PMID: 23323215)
PLoS Comput Biol. 2026 Aug 26;22(8):e1014685. (PMID: 42647567)
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J R Soc Interface. 2012 Oct 7;9(75):2624-38. (PMID: 22628212)
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Curr Biol. 2009 Mar 24;19(6):485-91. (PMID: 19269180)
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Grant Information: Human Frontier Science Program; Agence National de la Recherche; Netherlands NWO_ Dutch Research Council; Sectorplan Biology; Dutch Ministry of Education, Culture and Science (OCW); Institut de Recherche pour le Développement; Wageningen Graduate School of Wageningen University
Entry Date(s): Date Created: 20260826 Date Completed: 20260831 Latest Revision: 20260916
Update Code: 20260916
PubMed Central ID: PMC13529247
DOI: 10.1371/journal.pcbi.1014685
PMID: 42647567
Βάση Δεδομένων: MEDLINE
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  Data: The complex swarming dynamics of malaria mosquitoes emerge from simple minimally-interactive behavioral rules.
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  Data: <searchLink fieldCode="AU" term="%22Cribellier+A%22">Cribellier A</searchLink>; Experimental Zoology Group, Wageningen University, Wageningen, The Netherlands.<br /><searchLink fieldCode="AU" term="%22Poda+BS%22">Poda BS</searchLink>; Experimental Zoology Group, Wageningen University, Wageningen, The Netherlands.; Institut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso, Burkina Faso.<br /><searchLink fieldCode="AU" term="%22Dabiré+RK%22">Dabiré RK</searchLink>; Institut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso, Burkina Faso.<br /><searchLink fieldCode="AU" term="%22Diabaté+A%22">Diabaté A</searchLink>; Institut de Recherche en Sciences de la Santé (IRSS), Bobo-Dioulasso, Burkina Faso.<br /><searchLink fieldCode="AU" term="%22Roux+O%22">Roux O</searchLink>; MIVEGEC, University of Montpellier, IRD, CNRS, Montpellier, France.<br /><searchLink fieldCode="AU" term="%22Muijres+FT%22">Muijres FT</searchLink>; Experimental Zoology Group, Wageningen University, Wageningen, The Netherlands.
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  Data: <searchLink fieldCode="JN" term="%22101238922%22">PLoS computational biology</searchLink> [PLoS Comput Biol] 2026 Aug 26; Vol. 22 (8), pp. e1014685. <i>Date of Electronic Publication: </i>2026 Aug 26 (<i>Print Publication: </i>2026).
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  Data: <searchLink fieldCode="MM" term="%22Anopheles%22">Anopheles*</searchLink>/<searchLink fieldCode="MM" term="%22Anopheles+physiology%22">physiology</searchLink> <br /><searchLink fieldCode="MM" term="%22Malaria%22">Malaria*</searchLink>/<searchLink fieldCode="MM" term="%22Malaria+transmission%22">transmission</searchLink> <br /><searchLink fieldCode="MM" term="%22Behavior%2C+Animal%22">Behavior, Animal*</searchLink>/<searchLink fieldCode="MM" term="%22Behavior%2C+Animal+physiology%22">physiology</searchLink> <br /><searchLink fieldCode="MM" term="%22Mosquito+Vectors%22">Mosquito Vectors*</searchLink>/<searchLink fieldCode="MM" term="%22Mosquito+Vectors+physiology%22">physiology</searchLink> <br /><searchLink fieldCode="MM" term="%22Models%2C+Biological%22">Models, Biological*</searchLink><br /><searchLink fieldCode="MH" term="%22Flight%2C+Animal%22">Flight, Animal</searchLink>/<searchLink fieldCode="MH" term="%22Flight%2C+Animal+physiology%22">physiology</searchLink> ; <searchLink fieldCode="MH" term="%22Sexual+Behavior%2C+Animal%22">Sexual Behavior, Animal</searchLink>/<searchLink fieldCode="MH" term="%22Sexual+Behavior%2C+Animal+physiology%22">physiology</searchLink> ; <searchLink fieldCode="MH" term="%22Animals%22">Animals</searchLink> ; <searchLink fieldCode="MH" term="%22Female%22">Female</searchLink> ; <searchLink fieldCode="MH" term="%22Male%22">Male</searchLink> ; <searchLink fieldCode="MH" term="%22Computational+Biology%22">Computational Biology</searchLink> ; <searchLink fieldCode="MH" term="%22Computer+Simulation%22">Computer Simulation</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Swarming is a widespread collective behavior in animals, often thought to emerge from complex interactions among individuals. Here, we show that mating swarms of malaria mosquitoes can emerge from simple behavioral rules with minimal interaction between individuals. We analyzed two published experimental datasets with three-dimensional flight tracks of Anopheles coluzzii mosquitoes swarming in the lab under simulated sunset conditions and above a visual marker. We found that individuals alternate between straight flight and rapid turning maneuvers known as saccades. These saccades are triggered at the edge of the swarm, and their directions are biased along the sunset direction. This behavior was found consistent between both laboratory datasets, including swarming of solitary individuals; this indicates that inter‑individual interactions may play a limited role within the small-to-medium sized swarms that we studied. We developed a simple agent-based model incorporating three behavioral rules: attraction to the swarm center, alignment normal to the sunset horizon, both driven by environmental cues, and repulsion through short-range collision avoidance. This parsimonious model reproduced key features of the observed laboratory mosquito swarms, including looping flight paths, central density peaks, and directional alignment. Even in the absence of direct inter‑individual interactions, the model generated realistic emergent swarm dynamics, suggesting that social coordination is not required for swarm emergence. Although our lab-based findings remain to be confirmed across more naturalistic conditions, they suggest that the most parsimonious hypothesis behind male mosquito swarming is that it is primarily guided by environmental perception rather than social interaction. This minimal framework offers a new perspective on insect swarming and may apply broadly to the many other insect species that form mating swarms. Understanding the behavioral rules of mosquito swarming could inform strategies for vector control and improve the effectiveness of interventions targeting mosquito reproduction.<br /> (Copyright: © 2026 Cribellier et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: The authors have declared that no competing interests exist.
– Name: Ref
  Label: References
  Group: RefInfo
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(PMID: <searchLink fieldCode="PM" term="%2235007287%22">35007287)</searchLink><br />Curr Biol. 2024 Mar 25;34(6):1194-1205.e7. (PMID: <searchLink fieldCode="PM" term="%2238367617%22">38367617)</searchLink><br />Proc Natl Acad Sci U S A. 2011 Nov 15;108(46):18726-31. (PMID: <searchLink fieldCode="PM" term="%2222065759%22">22065759)</searchLink><br />J Exp Biol. 2022 Mar 1;225(5):. (PMID: <searchLink fieldCode="PM" term="%2235132997%22">35132997)</searchLink><br />Vector Borne Zoonotic Dis. 2010 Apr;10(3):295-311. (PMID: <searchLink fieldCode="PM" term="%2219725763%22">19725763)</searchLink><br />Sci Rep. 2014 Sep 12;4:6318. (PMID: <searchLink fieldCode="PM" term="%2225212874%22">25212874)</searchLink><br />Science. 2020 May 8;368(6491):634-637. (PMID: <searchLink fieldCode="PM" term="%2232381721%22">32381721)</searchLink><br />Phys Rev E. 2022 Mar;105(3-1):034601. (PMID: <searchLink fieldCode="PM" term="%2235428071%22">35428071)</searchLink><br />J Med Entomol. 2023 Nov 14;60(6):1278-1287. (PMID: <searchLink fieldCode="PM" term="%2237738317%22">37738317)</searchLink><br />Science. 2006 Jun 2;312(5778):1402-6. (PMID: <searchLink fieldCode="PM" term="%2216741126%22">16741126)</searchLink><br />Acta Trop. 2014 Apr;132 Suppl:S53-63. (PMID: <searchLink fieldCode="PM" term="%2224113221%22">24113221)</searchLink><br />J Med Entomol. 2013 May;50(3):552-9. (PMID: <searchLink fieldCode="PM" term="%2223802449%22">23802449)</searchLink><br />Philos Trans R Soc Lond B Biol Sci. 2023 Apr 10;378(1874):20220066. (PMID: <searchLink fieldCode="PM" term="%2236802778%22">36802778)</searchLink><br />iScience. 2024 Oct 11;27(11):111164. (PMID: <searchLink fieldCode="PM" term="%2239524359%22">39524359)</searchLink><br />Genetica. 2011 Jan;139(1):33-9. 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(PMID: <searchLink fieldCode="PM" term="%2230958145%22">30958145)</searchLink><br />Curr Biol. 2014 Sep 22;24(18):R828-R830. (PMID: <searchLink fieldCode="PM" term="%2225247351%22">25247351)</searchLink><br />Interface Focus. 2012 Dec 6;2(6):693-707. (PMID: <searchLink fieldCode="PM" term="%2224312723%22">24312723)</searchLink><br />J R Soc Interface. 2022 Aug;19(193):20220285. (PMID: <searchLink fieldCode="PM" term="%2236000227%22">36000227)</searchLink><br />Eur Phys J E Soft Matter. 2017 Apr;40(4):46. (PMID: <searchLink fieldCode="PM" term="%2228417322%22">28417322)</searchLink><br />J Exp Biol. 2011 Oct 15;214(Pt 20):3480-94. (PMID: <searchLink fieldCode="PM" term="%2221957112%22">21957112)</searchLink><br />J Med Entomol. 2009 Mar;46(2):227-35. (PMID: <searchLink fieldCode="PM" term="%2219351073%22">19351073)</searchLink><br />J R Soc Interface. 2022 Aug;19(193):20220258. (PMID: <searchLink fieldCode="PM" term="%2236043287%22">36043287)</searchLink><br />Trends Biotechnol. 2023 Feb;41(2):154-164. (PMID: <searchLink fieldCode="PM" term="%2235868886%22">35868886)</searchLink><br />J Med Entomol. 2023 Sep 12;60(5):857-864. (PMID: <searchLink fieldCode="PM" term="%2237392071%22">37392071)</searchLink><br />Sci Rep. 2013;3:1073. (PMID: <searchLink fieldCode="PM" term="%2223323215%22">23323215)</searchLink><br />PLoS Comput Biol. 2026 Aug 26;22(8):e1014685. (PMID: <searchLink fieldCode="PM" term="%2242647567%22">42647567)</searchLink><br />Philos Trans R Soc Lond B Biol Sci. 2018 May 19;373(1746):. (PMID: <searchLink fieldCode="PM" term="%2229581389%22">29581389)</searchLink><br />J R Soc Interface. 2012 Oct 7;9(75):2624-38. (PMID: <searchLink fieldCode="PM" term="%2222628212%22">22628212)</searchLink><br />J Exp Biol. 2015 Mar;218(Pt 6):864-75. (PMID: <searchLink fieldCode="PM" term="%2225657212%22">25657212)</searchLink><br />Proc Natl Acad Sci U S A. 2011 Nov 15;108(46):18720-5. (PMID: <searchLink fieldCode="PM" term="%2221795604%22">21795604)</searchLink><br />PLoS Comput Biol. 2014 Jul 24;10(7):e1003697. (PMID: <searchLink fieldCode="PM" term="%2225057853%22">25057853)</searchLink><br />Curr Biol. 2014 Feb 3;24(3):274-86. (PMID: <searchLink fieldCode="PM" term="%2224440395%22">24440395)</searchLink><br />Curr Biol. 2024 Sep 23;34(18):4091-4103.e4. (PMID: <searchLink fieldCode="PM" term="%2239216484%22">39216484)</searchLink><br />Parasit Vectors. 2025 Nov 27;18(1):512. (PMID: <searchLink fieldCode="PM" term="%2241310880%22">41310880)</searchLink><br />Curr Opin Insect Sci. 2020 Jun;39:77-83. (PMID: <searchLink fieldCode="PM" term="%2232339930%22">32339930)</searchLink><br />Philos Trans R Soc Lond B Biol Sci. 2006 Jan 29;361(1465):5-22. 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  Data: Human Frontier Science Program; Agence National de la Recherche; Netherlands NWO_ Dutch Research Council; Sectorplan Biology; Dutch Ministry of Education, Culture and Science (OCW); Institut de Recherche pour le Développement; Wageningen Graduate School of Wageningen University
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        Type: general
      – SubjectFull: Sexual Behavior, Animal physiology
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      – SubjectFull: Computational Biology
        Type: general
      – SubjectFull: Computer Simulation
        Type: general
      – SubjectFull: Anopheles physiology
        Type: general
      – SubjectFull: Malaria transmission
        Type: general
      – SubjectFull: Behavior, Animal physiology
        Type: general
      – SubjectFull: Mosquito Vectors physiology
        Type: general
      – SubjectFull: Models, Biological
        Type: general
    Titles:
      – TitleFull: The complex swarming dynamics of malaria mosquitoes emerge from simple minimally-interactive behavioral rules.
        Type: main
  BibRelationships:
    HasContributorRelationships:
      – PersonEntity:
          Name:
            NameFull: Cribellier A
      – PersonEntity:
          Name:
            NameFull: Poda BS
      – PersonEntity:
          Name:
            NameFull: Dabiré RK
      – PersonEntity:
          Name:
            NameFull: Diabaté A
      – PersonEntity:
          Name:
            NameFull: Roux O
      – PersonEntity:
          Name:
            NameFull: Muijres FT
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      – BibEntity:
          Dates:
            – D: 26
              M: 08
              Text: 2026 Aug 26
              Type: published
              Y: 2026
          Identifiers:
            – Type: issn-electronic
              Value: 1553-7358
          Numbering:
            – Type: volume
              Value: 22
            – Type: issue
              Value: 8
          Titles:
            – TitleFull: PLoS computational biology
              Type: main
ResultId 1