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Vector bionomics and vectorial capacity as emergent properties of mosquito behaviors and ecology

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Listed:
  • Sean L Wu
  • Héctor M Sánchez C.
  • John M Henry
  • Daniel T Citron
  • Qian Zhang
  • Kelly Compton
  • Biyonka Liang
  • Amit Verma
  • Derek A T Cummings
  • Arnaud Le Menach
  • Thomas W Scott
  • Anne L Wilson
  • Steven W Lindsay
  • Catherine L Moyes
  • Penny A Hancock
  • Tanya L Russell
  • Thomas R Burkot
  • John M Marshall
  • Samson Kiware
  • Robert C Reiner Jr
  • David L Smith

Abstract

Mosquitoes are important vectors for pathogens that infect humans and other vertebrate animals. Some aspects of adult mosquito behavior and mosquito ecology play an important role in determining the capacity of vector populations to transmit pathogens. Here, we re-examine factors affecting the transmission of pathogens by mosquitoes using a new approach. Unlike most previous models, this framework considers the behavioral states and state transitions of adult mosquitoes through a sequence of activity bouts. We developed a new framework for individual-based simulation models called MBITES (Mosquito Bout-based and Individual-based Transmission Ecology Simulator). In MBITES, it is possible to build models that simulate the behavior and ecology of adult mosquitoes in exquisite detail on complex resource landscapes generated by spatial point processes. We also developed an ordinary differential equation model which is the Kolmogorov forward equations for models developed in MBITES under a specific set of simplifying assumptions. While mosquito infection and pathogen development are one possible part of a mosquito’s state, that is not our main focus. Using extensive simulation using some models developed in MBITES, we show that vectorial capacity can be understood as an emergent property of simple behavioral algorithms interacting with complex resource landscapes, and that relative density or sparsity of resources and the need to search can have profound consequences for mosquito populations’ capacity to transmit pathogens.Author summary: Mathematical modelling of pathogen transmission by mosquitoes began over a century ago with Ronald Ross and has produced a set of metrics that are the basis of measuring transmission. One crucial metric is vectorial capacity (VC), a simple equation describing the potential of mosquitoes to transmit pathogens. Despite its elegance, this formula lacks specificity to describe mosquitoes in a particular landscape. To study how these metrics arise in particular places, we built MBITES (Mosquito Bout-based and Individual-based Transmission Ecology Simulator), a complex stochastic individual-based model where mosquitoes fly from place to place to blood feed, sugar feed, lay eggs, mate, or rest. We also built a related model, MBDETES based on deterministic mathematics to show how the complex behaviors possible in MBITES can be summarized on average, and to provide a bridge to the simple equations describing VC. Through a series of computational experiments, we show a strong dependence VC and other metrics on fine details of the landscape mosquitoes inhabit which are not obvious from simple equations.

Suggested Citation

  • Sean L Wu & Héctor M Sánchez C. & John M Henry & Daniel T Citron & Qian Zhang & Kelly Compton & Biyonka Liang & Amit Verma & Derek A T Cummings & Arnaud Le Menach & Thomas W Scott & Anne L Wilson & St, 2020. "Vector bionomics and vectorial capacity as emergent properties of mosquito behaviors and ecology," PLOS Computational Biology, Public Library of Science, vol. 16(4), pages 1-32, April.
  • Handle: RePEc:plo:pcbi00:1007446
    DOI: 10.1371/journal.pcbi.1007446
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    References listed on IDEAS

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    1. Sachie Kanatani & Deborah Stiffler & Teun Bousema & Gayane Yenokyan & Photini Sinnis, 2024. "Revisiting the Plasmodium sporozoite inoculum and elucidating the efficiency with which malaria parasites progress through the mosquito," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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