Two novel, tightly linked, and rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought
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 ferti...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2023-02-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/80489 |
| _version_ | 1797851677696458752 |
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| author | Krithika Venkataraman Nadav Shai Priyanka Lakhiani Sarah Zylka Jieqing Zhao Margaret Herre Joshua Zeng Lauren A Neal Henrik Molina Li Zhao Leslie B Vosshall |
| author_facet | Krithika Venkataraman Nadav Shai Priyanka Lakhiani Sarah Zylka Jieqing Zhao Margaret Herre Joshua Zeng Lauren A Neal Henrik Molina Li Zhao Leslie B Vosshall |
| author_sort | Krithika Venkataraman |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-09T19:21:43Z |
| format | Article |
| id | doaj.art-df8d2a079d314c448888cfedafdfbf56 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-09T19:21:43Z |
| publishDate | 2023-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-df8d2a079d314c448888cfedafdfbf562023-04-05T13:37:37ZengeLife Sciences Publications LtdeLife2050-084X2023-02-011210.7554/eLife.80489Two novel, tightly linked, and rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during droughtKrithika Venkataraman0https://orcid.org/0000-0002-2067-2387Nadav Shai1https://orcid.org/0000-0002-2812-3884Priyanka Lakhiani2https://orcid.org/0000-0003-2797-8650Sarah Zylka3https://orcid.org/0000-0002-7311-2981Jieqing Zhao4https://orcid.org/0000-0002-0134-7538Margaret Herre5https://orcid.org/0000-0001-7868-3321Joshua Zeng6https://orcid.org/0000-0002-4694-3309Lauren A Neal7https://orcid.org/0000-0002-0092-2852Henrik Molina8https://orcid.org/0000-0001-8950-4990Li Zhao9https://orcid.org/0000-0001-6776-1996Leslie B Vosshall10https://orcid.org/0000-0002-6060-8099Laboratory of Neurogenetics and Behavior, Rockefeller University, New York, United StatesLaboratory of Neurogenetics and Behavior, Rockefeller University, New York, United States; Howard Hughes Medical Institute, New York, United StatesLaboratory of Neurogenetics and Behavior, Rockefeller University, New York, United States; Laboratory of Evolutionary Genetics and Genomics, Rockefeller University, New York, United StatesLaboratory of Neurogenetics and Behavior, Rockefeller University, New York, United StatesLaboratory of Neurogenetics and Behavior, Rockefeller University, New York, United StatesLaboratory of Neurogenetics and Behavior, Rockefeller University, New York, United States; Kavli Neural Systems Institute, New York, United StatesLaboratory of Neurogenetics and Behavior, Rockefeller University, New York, United StatesLaboratory of Neurogenetics and Behavior, Rockefeller University, New York, United StatesProteomics Resource Center, Rockefeller University, New York, United StatesLaboratory of Evolutionary Genetics and Genomics, Rockefeller University, New York, United StatesLaboratory of Neurogenetics and Behavior, Rockefeller University, New York, United States; Howard Hughes Medical Institute, New York, United States; Kavli Neural Systems Institute, New York, United StatesFemale 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.https://elifesciences.org/articles/80489Aedes aegyptimosquitoAedes albopictusAnopheles gambiaeCulex quinquefasciatustranscriptomics |
| spellingShingle | Krithika Venkataraman Nadav Shai Priyanka Lakhiani Sarah Zylka Jieqing Zhao Margaret Herre Joshua Zeng Lauren A Neal Henrik Molina Li Zhao Leslie B Vosshall Two novel, tightly linked, and rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought eLife Aedes aegypti mosquito Aedes albopictus Anopheles gambiae Culex quinquefasciatus transcriptomics |
| title | Two novel, tightly linked, and rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought |
| title_full | Two novel, tightly linked, and rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought |
| title_fullStr | Two novel, tightly linked, and rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought |
| title_full_unstemmed | Two novel, tightly linked, and rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought |
| title_short | Two novel, tightly linked, and rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought |
| title_sort | two novel tightly linked and rapidly evolving genes underlie aedes aegypti mosquito reproductive resilience during drought |
| topic | Aedes aegypti mosquito Aedes albopictus Anopheles gambiae Culex quinquefasciatus transcriptomics |
| url | https://elifesciences.org/articles/80489 |
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