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Mosquito microevolution drives Plasmodium falciparum dynamics

Nature Microbiology volume 4, pages 941–947 (2019)Cite this article

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Abstract

Malaria, a major cause of child mortality in Africa, is engendered by Plasmodium parasites that are transmitted by anopheline mosquitoes. Fitness of Plasmodium parasites is closely linked to the ecology and evolution of its anopheline vector. However, whether the genetic structure of vector populations impacts malaria transmission remains unknown. Here, we describe a partitioning of the African malaria vectors into generalists and specialists that evolve along ecological boundaries. We next identify the contribution of mosquito species to Plasmodium abundance using Granger causality tests for time-series data collected over two rainy seasons in Mali. We find that mosquito microevolution, defined by changes in the genetic structure of a population over short ecological timescales, drives Plasmodium dynamics in nature, whereas vector abundance, infection prevalence, temperature and rain have low predictive values. Our study demonstrates the power of time-series approaches in vector biology and highlights the importance of focusing local vector control strategies on mosquito species that drive malaria dynamics.

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Fig. 1: TEP1 diversity and classification.
Fig. 2: TEP1 population genetics.
Fig. 3: Genetic and ecotype structures of Anopheles gambiae s.l.
Fig. 4: Granger causality analysis.

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Data availability

The full-length TEP1 and TEP1–TED sequences are available at the NCBI GenBank under accession numbers MF098568 to MF098592 and MF035727 to MF035924, respectively. The data that support the findings of this study are available from the corresponding author upon request.

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Acknowledgements

We thank A. Telschow, F. Grziwotz and S. F. Traore for helpful suggestions; L. Spohr, S. Koppitz, D. Coulibaly, M. Coulibaly, C. Omogo, J. Shikaya, L. Abate, E. Onana, J. P. Agbor, J. Mwaura and A. Gildenhard for technical support; and M. Doumbia, B. Doumbia and C. Okech for their help with sample collections. This research was supported by funds from EC FP7 under grant agreements N°223601 (MALVECBLOK) and N°242095 (EVIMalar). E.K.R. was a DAAD fellow.

Author information

Author notes

  1. Priscila Bascunan

    Present address: Entomology Branch, CDC, Atlanta, GA, USA

  2. Paul Mireji

    Present address: Yale School of Public Health, New Heaven, CT, USA

  3. Sandrine E. Nsango

    Present address: Faculté de Médecine et des Sciences Pharmaceutiques, Université de Douala, Douala, Cameroon

  4. Julien Pompon

    Present address: Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore

  5. Martin K. Rono

    Present address: Pwani University Bioscience Research Centre, Pwani University, Kilifi, Kenya

  6. Martin K. Rono

    Present address: KEMRI-Wellcome Trust Research Programme, Kilifi, Kenya

  7. Flaminia Catteruccia

    Present address: Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Boston, MA, USA

  8. These authors contributed equally: Markus Gildenhard, Evans K. Rono.

  9. These authors jointly supervised this work: Flaminia Catteruccia, Isabelle Morlais, Mouctar Diallo, Djibril Sangare, Elena A. Levashina.

Authors and Affiliations

  1. Max Planck Institute for Infection Biology, Berlin, Germany

    Markus Gildenhard, Evans K. Rono, Paola Carrillo-Bustamante, Hanne Krüger, Yara Reis, Cynthia V. Yapto & Elena A. Levashina

  2. University of Sciences, Techniques and Technology, Bamako, Mali

    Assetou Diarra, Djeneba Camara, Modibo Mariko, Ramata Mariko, Alou Traorè, Mouctar Diallo & Djibril Sangare

  3. MIVEGEC, IRD, CNRS, Université Montpellier, Montpellier, France

    Anne Boissière, Julien Pompon & Isabelle Morlais

  4. Dipartimento di Medicina Sperimentale, Università degli Studi di Perugia, Perugia, Italy

    Priscila Bascunan & Flaminia Catteruccia

  5. International Centre of Insect Physiology and Ecology, Nairobi, Kenya

    Paul Mireji, Martin K. Rono, Pamela B. Seda & Daniel Masiga

  6. Malaria Research Laboratory, OCEAC, Yaounde, Cameroon

    Sandrine E. Nsango, Parfait Awono-Ambene & Isabelle Morlais

  7. UPR0922 CNRS, U963 Inserm, Université de Strasbourg, Strasbourg, France

    Julien Pompon & Elena A. Levashina

  8. Department of Life Sciences, Imperial College London, London, UK

    Janis Thailayil & Flaminia Catteruccia

  9. Institut de Recherche en Sciences de la Santé/Centre Muraz, Bobo-Dioulasso, Burkina Faso

    Roch K. Dabiré & Abdulaye Diabaté

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  1. Markus Gildenhard
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Contributions

F.C., D.M., M.D., I.M., D.S. and E.A.L. conceived and designed the study. D.S., M.D., A.Diabaté, R.K.D., P.A.-A., D.M. and I.M. designed and managed sample collections, genotyping and sequencing. E.K.R., A.B., I.M. and E.A.L. contributed molecular tools. J.T., J.P., P.A.-A., M.M., A.B., S.E.N., P.B.S., P.M., A.T., D.S., M.D., M.K.R., E.K.R., C.V.Y. and H.K. conducted sample collections, processing and genotyping. P.B., A.B., P.M., P.B.S. and E.K.R. performed sequencing. E.K.R., A.B., P.B., M.G., I.M., F.C. and E.A.L. analysed the data. M.G. and E.A.L. conceived and designed the time series. M.G., Y.R., M.D. and D.S. designed and managed time-series collections. D.C., R.M., H.K., M.G., D.S. and A.Diarra performed time-series collections and genotyping. E.A.L. and M.G. analysed time-series data. M.G. designed and carried out population genetic analyses and time-series modelling. P.C.-B. contributed to time-series analyses. M.G., E.K.R., P.C.B. and E.A.L. wrote the manuscript.

Corresponding author

Correspondence to Elena A. Levashina.

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Supplementary information

Supplementary Information

Supplementary Tables 1–3, Supplementary Tables 6–9, Supplementary Figures 1–6 and Supplementary References.

Reporting Summary

Supplementary Table 4

Sampling sites across Africa.

Supplementary Table 5

Vector autoregression models.

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Gildenhard, M., Rono, E.K., Diarra, A. et al. Mosquito microevolution drives Plasmodium falciparum dynamics. Nat Microbiol 4, 941–947 (2019). https://doi.org/10.1038/s41564-019-0414-9

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