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Isotopic evidence that aestivation allows malaria mosquitoes to persist through the dry season in the Sahel

Nature Ecology & Evolution volume 6, pages 1687–1699 (2022)Cite this article

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Abstract

Data suggest that the malaria vector mosquito Anopheles coluzzii persists during the dry season in the Sahel through a dormancy mechanism known as aestivation; however, the contribution of aestivation compared with alternative strategies such as migration is unknown. Here we marked larval Anopheles mosquitoes in two Sahelian villages in Mali using deuterium (2H) to assess the contribution of aestivation to persistence of mosquitoes through the seven-month dry season. After an initial enrichment period, 33% of An. coluzzii mosquitoes were strongly marked. Seven months following enrichment, multiple analysis methods supported the ongoing presence of marked mosquitoes, compatible with the prediction that the fraction of marked mosquitoes should remain stable throughout the dry season if local aestivation is occurring. The results suggest that aestivation is a major persistence mechanism of An. coluzzii in the Sahel, contributing at least 20% of the adults at the onset of rains. This persistence strategy could influence mosquito control and malaria elimination campaigns.

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Fig. 1: Mark–release–recapture experiment timeline.
Fig. 2: Species composition and variation in marked adults and enrichment values in release villages.
Fig. 3: Evaluation of the proportion of marked mosquitoes during the dry season by different methods.
Fig. 4: Evaluation of the proportion of marked mosquitoes during the onset of rains, seven to eight months after end of enrichment.
Fig. 5: Spatial and seasonal natural variation in 2H and evaluating the possibility that mass migration from Niono accounts for the elevated 2H values in post-enrichment Thierola.
Fig. 6: Change in the proportion of marked An. coluzzii over the course of the experiment.

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Data availability

The dataset used in our analyses can be found at https://doi.org/10.6084/m9.figshare.20387328.v1.

Code availability

SAS code associated with these analyses will be made available by T.L. upon request (tlehmann@niaid.nih.gov).

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Acknowledgements

We thank C. Barillas-Mury, J. Ribeiro, K. A. Hobson, L. I. Wassenaar, G. Hamer, and D. X. Soto for ideation and critical reading of earlier versions of this manuscript. Special thanks is extended to C. A. M. France from The Smithsonian Museum Support Center and J. Matthews of U.C. Davis for help with IRMS work. We thank Dr. T. Wellems for his continuing support of our work. We thank F. Bathily, L. Juompan, M. Sullivan, A. Laughinghouse, K. Lee and S. Moretz for logistic support. We thank the residents of the villages of Thierola and M’Piabougou for their cooperation and hospitality. A special thanks goes to our spouses and families for their endurance, dedication and unwavering support throughout this endeavour. This study was supported by the Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD.

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Author notes

  1. These authors contributed equally: Roy Faiman, Alpha S. Yaro.

  2. These authors jointly supervised this work: Adama Dao, Tovi Lehmann.

Authors and Affiliations

  1. Laboratory of Malaria and Vector Research, NIAID, NIH, Rockville, MD, USA

    Roy Faiman, Laura M. Veru, Leland C. Graber, Abigail R. Conte, Cedric Kouam, Benjamin J. Krajacich & Tovi Lehmann

  2. Malaria Research and Training Center (MRTC)/Faculty of Medicine, Pharmacy and Odonto-stomatology, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali

    Alpha S. Yaro, Adama Dao, Zana L. Sanogo, Moussa Diallo, Djibril Samake & Ousmane Yossi

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Contributions

Conception and study design were by R.F., A.S.Y., A.D. and T.L. Fieldwork and sample collection were done by A.D., A.S.Y., M.D., D.S., Z.L.S. and O.Y. Mosquito identification and sample preparation were handled by R.F., L.M.V., L.C.G., A.R.C. and C.K. Data acquisition (IRMS) was by R.F., A.S.Y., A.D. and T.L. Data interpretation and analysis were done by R.F., A.S.Y., A.D., B.J.K. and T.L. Manuscript drafting was by R.F., A.S.Y. and T.L. Manuscript revision was by R.F., L.M.V., L.C.G., A.R.C., C.K., B.J.K., A.D., A.S.Y., M.D., D.S., Z.L.S., O.Y. and T.L.

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Correspondence to Roy Faiman.

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Extended data

Extended Data Fig. 1 Map of study area.

Map of study area including its location (black rectangle) on a map of Mali (inset). Location of the focal villages (red) surrounded by nearby villages (green) and distant villages (blue) is shown. Maps plotted using SAS 9.4 which is licensed to include maps from Gfk GeoMarketing GmbH (inset) and Open Street map.

Extended Data Fig. 2 Thierola and M’Piabougou satellite images.

Thierola (top) and M’Piabougou (bottom) satellite images; houses (black empty circles) and larval sites (Navy-blue dots). Image data from Google (©2022), Maxar Technologies and CNES/Airbus.

Extended Data Fig. 3 Residual marking.

Differences between pre-enrichment mosquitoes from Thierola collected indoors (September 2017: PreEnrContInd), experimentally marked mosquitoes collected as pupae and stage-4 instar larvae from enriched larval sites during enrichment (LV1Enrich and LV5Enrich), and naturally occurring pupae and stage-4 instar larvae collected after the first rain the following year (July 2018: LV1PostEnrich and LV5PostEnrich). Sample size is shown in blue, and green reference lines show the range of natural 2H levels as in Fig. 2.

Extended Data Fig. 4 Natural temporal variation within and between population in median 2H.

Natural temporal variation within and between population in median 2H (Y axis), spread of 2H as measured by the inter-quartile range (bubble size), and skewness measured by the non-parametric skewness (values inside bubbles; blue denotes negative skewness and yellow and red denote weaker and stronger positive skewness, respectively as seen in scale bar). Sampling years (August to July) are shown on each line and the letters T and M denote samples for Thierola and M’Piabougou.

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Faiman, R., Yaro, A.S., Dao, A. et al. Isotopic evidence that aestivation allows malaria mosquitoes to persist through the dry season in the Sahel. Nat Ecol Evol 6, 1687–1699 (2022). https://doi.org/10.1038/s41559-022-01886-w

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