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Evolutionary modelling indicates that mosquito metabolism shapes the life-history strategies of Plasmodium parasites

Author

Listed:
  • Paola Carrillo-Bustamante

    (Max Planck Institute for Infection Biology)

  • Giulia Costa

    (Max Planck Institute for Infection Biology)

  • Lena Lampe

    (Max Planck Institute for Infection Biology
    The Francis Crick Institute)

  • Elena A. Levashina

    (Max Planck Institute for Infection Biology)

Abstract

Within-host survival and between-host transmission are key life-history traits of single-celled malaria parasites. Understanding the evolutionary forces that shape these traits is crucial to predict malaria epidemiology, drug resistance, and virulence. However, very little is known about how Plasmodium parasites adapt to their mosquito vectors. Here, we examine the evolution of the time Plasmodium parasites require to develop within the vector (extrinsic incubation period) with an individual-based model of malaria transmission that includes mosquito metabolism. Specifically, we model the metabolic cascade of resource allocation induced by blood-feeding, as well as the influence of multiple blood meals on parasite development. Our model predicts that successful vector-to-human transmission events are rare, and are caused by long-lived mosquitoes. Importantly, our results show that the life-history strategies of malaria parasites depend on the mosquito’s metabolic status. In our model, additional resources provided by multiple blood meals lead to selection for parasites with slow or intermediate developmental time. These results challenge the current assumption that evolution favors fast developing parasites to maximize their chances to complete their within-mosquito life cycle. We propose that the long sporogonic cycle observed for Plasmodium is not a constraint but rather an adaptation to increase transmission potential.

Suggested Citation

  • Paola Carrillo-Bustamante & Giulia Costa & Lena Lampe & Elena A. Levashina, 2023. "Evolutionary modelling indicates that mosquito metabolism shapes the life-history strategies of Plasmodium parasites," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43810-1
    DOI: 10.1038/s41467-023-43810-1
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    References listed on IDEAS

    as
    1. Sarah E. Reece & Damien R. Drew & Andy Gardner, 2008. "Sex ratio adjustment and kin discrimination in malaria parasites," Nature, Nature, vol. 453(7195), pages 609-614, May.
    2. Lena Lampe & Marius Jentzsch & Sylwia Kierszniowska & Elena A. Levashina, 2019. "Metabolic balancing by miR-276 shapes the mosquito reproductive cycle and Plasmodium falciparum development," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    3. Doreen J. Siria & Roger Sanou & Joshua Mitton & Emmanuel P. Mwanga & Abdoulaye Niang & Issiaka Sare & Paul C. D. Johnson & Geraldine M. Foster & Adrien M. G. Belem & Klaas Wynne & Roderick Murray-Smit, 2022. "Rapid age-grading and species identification of natural mosquitoes for malaria surveillance," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    4. G. Costa & M. Gildenhard & M. Eldering & R. L. Lindquist & A. E. Hauser & R. Sauerwein & C. Goosmann & V. Brinkmann & P. Carrillo-Bustamante & E. A. Levashina, 2018. "Non-competitive resource exploitation within mosquito shapes within-host malaria infectivity and virulence," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
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