Signatures of aestivation and migration in Sahelian malaria mosquito populations

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Abstract

During the long Sahelian dry season, mosquito vectors of malaria are expected to perish when no larval sites are available; yet, days after the first rains, mosquitoes reappear in large numbers. How these vectors persist over the 3–6-month long dry season has not been resolved, despite extensive research for over a century1,2,3. Hypotheses for vector persistence include dry-season diapause (aestivation) and long-distance migration (LDM); both are facets of vector biology that have been highly controversial owing to lack of concrete evidence. Here we show that certain species persist by a form of aestivation, while others engage in LDM. Using time-series analyses, the seasonal cycles of Anopheles coluzzii, Anopheles gambiae sensu stricto (s.s.), and Anopheles arabiensis were estimated, and their effects were found to be significant, stable and highly species-specific. Contrary to all expectations, the most complex dynamics occurred during the dry season, when the density of A. coluzzii fluctuated markedly, peaking when migration would seem highly unlikely, whereas A. gambiae s.s. was undetected. The population growth of A. coluzzii followed the first rains closely, consistent with aestivation, whereas the growth phase of both A. gambiae s.s. and A. arabiensis lagged by two months. Such a delay is incompatible with local persistence, but fits LDM. Surviving the long dry season in situ allows A. coluzzii to predominate and form the primary force of malaria transmission. Our results reveal profound ecological divergence between A. coluzzii and A. gambiae s.s., whose standing as distinct species has been challenged, and suggest that climate is one of the selective pressures that led to their speciation. Incorporating vector dormancy and LDM is key to predicting shifts in the range of malaria due to global climate change4, and to the elimination of malaria from Africa.

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Figure 1: Species-specific population dynamics of the members of Anopheles gambiae s.l.
Figure 2: Seasonal population dynamics of the members of Anopheles gambiae s.l.

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Acknowledgements

We thank the residents of Thierola for their hospitality and assistance with mosquito collections; J. Ribeiro, T. Wellems, P. McQueen, R. Faiman and G. Wasserberg for their comments on previous versions of this manuscript; and C. Traoré, R. Sakai, R. Gwadz and T. Wellems for logistical support. This study was supported by the Tamaki Foundation and by the Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health.

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Contributions

T.L. conceived the study and together with A.D. and A.S.Y. designed it. A.D., A.S.Y., M.D., S.T., D.L.H., Y.K., A.I.T., Z.L.S. and D.S. performed the research, both in the field and the laboratory. All authors have discussed and interpreted the results as well as made decisions on various field and laboratory operations. A.D. led the field operations and data management; T.L. analysed the data and wrote the paper, with extensive input from A.D. and D.L.H.

Corresponding author

Correspondence to T. Lehmann.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Sex-ratio, density and composition of Anopheles gambiae s.l.

ac, Overall monthly means of the proportion of A. gambiae s.l. females (a), house density (b), and species composition (c). Nm, Nd, and Ng denote sample size of A. gambiae s.l., the number of collection days, and the number genotyped to species, respectively (Methods). Whiskers in box-whisker plots extend to the extreme values up to 1.5 the distance between the twenty-fifth and seventy-fifth percentiles. In a, blue triangles represent means that are significantly lower than the red triangles (based on the sequential Bonferroni test; see Extended Data Table 1) and the horizontal line represents 1:1 sex ratio.

Extended Data Figure 2 Population dynamics of Anopheles gambiae s.l.

House density over time in linear (top) and natural logarithm (bottom) scale to evaluate systematic change over time. Circles denote observed daily mean density and the black lines show the interpolated series of mean house density over 5-day intervals. Grey lines depict interpolation during the longest time without field samples (December 2008 to April 2009). First rain events are shown by green lines (dates listed above). Sample sizes of mosquitoes and collection days are the same as in Extended Data Fig. 1b.

Extended Data Figure 3 Population dynamics of Anopheles gambiae s.l. across years.

Observed daily mean density (circles) is shown against 5-day means (line) on linear and log scales from July to June of every year to assess similarity among years. Green arrows mark the first rain and the tan background denotes the dry season. Shading during 2008 indicates a gap in sampling (December–March) when imputed values were used (Methods). Sample sizes (Nm and Nd) are explained in Fig. 1.

Extended Data Figure 4 Level-adjusted seasonal component of the density of A. coluzzii, A. gambiae s.s. and A. arabiensis.

The level, seasonals, and their 95% CI (bands) were estimated using unobserved component time series models (Table 1; Methods). Arrows denote the start of the population growth (text and Fig. 2). Time is shown starting from May to maximize the comparability between the species. In the colour ruler on the x axis, yellow and green denote dry and wet seasons, respectively, and orange and light-green denote transition periods. Sample sizes are given in Extended Data Fig. 1.

Extended Data Table 1 Annual and monthly variation in the indoor sex ratio (proportion of females)
Extended Data Table 2 Putative elements of the seasonal cycles of the members of A. gambiae s.l.

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Dao, A., Yaro, A., Diallo, M. et al. Signatures of aestivation and migration in Sahelian malaria mosquito populations. Nature 516, 387–390 (2014). https://doi.org/10.1038/nature13987

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