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Diet unmasks genetic variants that regulate lifespan in outbred Drosophila

View ORCID ProfileLuisa F. Pallares, View ORCID ProfileAmanda J. Lea, Clair Han, Elena V. Filippova, View ORCID ProfilePeter Andolfatto, Julien F. Ayroles
doi: https://doi.org/10.1101/2020.10.19.346312
Luisa F. Pallares
1Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton NJ, USA
2Ecology and Evolutionary Biology Department, Princeton University, Princeton NJ, USA
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  • ORCID record for Luisa F. Pallares
Amanda J. Lea
1Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton NJ, USA
2Ecology and Evolutionary Biology Department, Princeton University, Princeton NJ, USA
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Clair Han
1Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton NJ, USA
3Janelia Research Campus of the Howard Hughes Medical Institute, Ashburn VA, USA
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Elena V. Filippova
1Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton NJ, USA
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Peter Andolfatto
4Department of Biological Sciences, Columbia University, New York, NY, USA
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  • For correspondence: jayroles@princeton.edu pa2543@columbia.edu
Julien F. Ayroles
1Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton NJ, USA
2Ecology and Evolutionary Biology Department, Princeton University, Princeton NJ, USA
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  • For correspondence: jayroles@princeton.edu pa2543@columbia.edu
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Abstract

Evolutionary theory suggests that lifespan-associated alleles should be purged from the gene pool, and yet decades of GWAS and model organism studies have shown they persist. Here, we address one potential explanation, the idea that the alleles that regulate lifespan do so only in certain contexts. We exposed thousands of outbred Drosophila to a standard and a high sugar diet. We then sequenced over 10,000 individuals and track genome-wide allele frequency changes over time, as these populations aged. We mapped thousands of lifespan-altering alleles, some associated with early vs late life tradeoffs, late-onset effects, and genotype-by-environment interactions. We find that lifespan-reducing alleles are most likely to be recently derived, have stronger effects on a high-sugar diet, consistent with the hypothesis that historically neutral or beneficial alleles can become detrimental in novel conditions. We also show that the gene midway, a regulator of lipid storage and ortholog of the lifespan-associated gene DGAT1 in mice, also regulates lifespan in Drosophila. Our results provide insight into the highly polygenic and context-dependent genetic architecture of lifespan, as well as the evolutionary processes that shape this key trait.

Competing Interest Statement

The authors have declared no competing interest.

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-NC-ND 4.0 International license.
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Posted January 31, 2021.
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Diet unmasks genetic variants that regulate lifespan in outbred Drosophila
Luisa F. Pallares, Amanda J. Lea, Clair Han, Elena V. Filippova, Peter Andolfatto, Julien F. Ayroles
bioRxiv 2020.10.19.346312; doi: https://doi.org/10.1101/2020.10.19.346312
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Diet unmasks genetic variants that regulate lifespan in outbred Drosophila
Luisa F. Pallares, Amanda J. Lea, Clair Han, Elena V. Filippova, Peter Andolfatto, Julien F. Ayroles
bioRxiv 2020.10.19.346312; doi: https://doi.org/10.1101/2020.10.19.346312

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