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Rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought

View ORCID ProfileKrithika Venkataraman, View ORCID ProfileNadav Shai, View ORCID ProfilePriyanka Lakhiani, View ORCID ProfileSarah Zylka, View ORCID ProfileJieqing Zhao, View ORCID ProfileMargaret Herre, View ORCID ProfileJoshua Zeng, View ORCID ProfileLauren A. Neal, View ORCID ProfileHenrik Molina, View ORCID ProfileLi Zhao, View ORCID ProfileLeslie B. Vosshall
doi: https://doi.org/10.1101/2022.03.01.482582
Krithika Venkataraman
1Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
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  • For correspondence: krithika.venkataraman@gmail.com leslie@rockefeller.edu
Nadav Shai
1Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
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Priyanka Lakhiani
1Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
2Laboratory of Evolutionary Genetics and Genomics, The Rockefeller University, New York, NY 10065 USA
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Sarah Zylka
1Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
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Jieqing Zhao
1Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
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Margaret Herre
1Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
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Joshua Zeng
1Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
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Lauren A. Neal
1Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
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Henrik Molina
3Proteomics Resource Center, The Rockefeller University, New York, NY 10065 USA
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Li Zhao
2Laboratory of Evolutionary Genetics and Genomics, The Rockefeller University, New York, NY 10065 USA
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Leslie B. Vosshall
1Laboratory of Neurogenetics and Behavior, The Rockefeller University, New York, NY 10065 USA
4Kavli Neural Systems Institute, New York, NY 10065 USA
5Howard Hughes Medical Institute, New York, NY 10065 USA
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  • For correspondence: krithika.venkataraman@gmail.com leslie@rockefeller.edu
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SUMMARY

Female Aedes aegypti mosquitoes impose a severe global public health burden as vectors of multiple viral pathogens. Under optimal environmental conditions, Aedes aegypti females have access to human hosts that provide blood proteins for egg development, conspecific males that provide sperm for fertilization, and freshwater that serves as an egg-laying substrate suitable for offspring survival. As global temperatures rise, Aedes aegypti females are faced with climate challenges like intense droughts and intermittent precipitation, which create unpredictable, suboptimal conditions for egg-laying. Here we show that under drought-like conditions simulated in the laboratory, females retain mature eggs in their ovaries for extended periods, while maintaining the viability of these eggs until they can be laid in freshwater. Using transcriptomic and proteomic profiling of Aedes aegypti ovaries, we identify two previously uncharacterized genes named tweedledee and tweedledum, each encoding a small, secreted protein that both show ovary-enriched, temporally-restricted expression during egg retention. These genes are mosquito-specific, linked within a syntenic locus, and rapidly evolving under positive selection, raising the possibility that they serve an adaptive function. CRISPR-Cas9 deletion of both tweedledee and tweedledum demonstrates that they are specifically required for extended retention of viable eggs. These results highlight an elegant example of taxon-restricted genes at the heart of an important adaptation that equips Aedes aegypti females with “insurance” to flexibly extend their reproductive schedule without losing reproductive capacity, thus allowing this species to exploit unpredictable habitats in a changing world.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://doi.org/10.5281/zenodo.5945525

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted March 02, 2022.
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Rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought
Krithika Venkataraman, Nadav Shai, Priyanka Lakhiani, Sarah Zylka, Jieqing Zhao, Margaret Herre, Joshua Zeng, Lauren A. Neal, Henrik Molina, Li Zhao, Leslie B. Vosshall
bioRxiv 2022.03.01.482582; doi: https://doi.org/10.1101/2022.03.01.482582
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Rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought
Krithika Venkataraman, Nadav Shai, Priyanka Lakhiani, Sarah Zylka, Jieqing Zhao, Margaret Herre, Joshua Zeng, Lauren A. Neal, Henrik Molina, Li Zhao, Leslie B. Vosshall
bioRxiv 2022.03.01.482582; doi: https://doi.org/10.1101/2022.03.01.482582

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