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Genomes from historical Drosophila melanogaster specimens illuminate adaptive and demographic changes across more than 200 years of evolution

The ability to perform genomic sequencing on long-dead organisms is opening new frontiers in evolutionary research. These opportunities are especially notable in the case of museum collections, from which countless documented specimens may now be suitable for genomic analysis—if data of sufficient q...

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Autores principales: Shpak, Max, Ghanavi, Hamid R., Lange, Jeremy D., Pool, John E., Stensmyr, Marcus C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10569592/
https://www.ncbi.nlm.nih.gov/pubmed/37824452
http://dx.doi.org/10.1371/journal.pbio.3002333
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author Shpak, Max
Ghanavi, Hamid R.
Lange, Jeremy D.
Pool, John E.
Stensmyr, Marcus C.
author_facet Shpak, Max
Ghanavi, Hamid R.
Lange, Jeremy D.
Pool, John E.
Stensmyr, Marcus C.
author_sort Shpak, Max
collection PubMed
description The ability to perform genomic sequencing on long-dead organisms is opening new frontiers in evolutionary research. These opportunities are especially notable in the case of museum collections, from which countless documented specimens may now be suitable for genomic analysis—if data of sufficient quality can be obtained. Here, we report 25 newly sequenced genomes from museum specimens of the model organism Drosophila melanogaster, including the oldest extant specimens of this species. By comparing historical samples ranging from the early 1800s to 1933 against modern-day genomes, we document evolution across thousands of generations, including time periods that encompass the species’ initial occupation of northern Europe and an era of rapidly increasing human activity. We also find that the Lund, Sweden population underwent local genetic differentiation during the early 1800s to 1933 interval (potentially due to drift in a small population) but then became more similar to other European populations thereafter (potentially due to increased migration). Within each century-scale time period, our temporal sampling allows us to document compelling candidates for recent natural selection. In some cases, we gain insights regarding previously implicated selection candidates, such as ChKov1, for which our inferred timing of selection favors the hypothesis of antiviral resistance over insecticide resistance. Other candidates are novel, such as the circadian-related gene Ahcy, which yields a selection signal that rivals that of the DDT resistance gene Cyp6g1. These insights deepen our understanding of recent evolution in a model system, and highlight the potential of future museomic studies.
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spelling pubmed-105695922023-10-13 Genomes from historical Drosophila melanogaster specimens illuminate adaptive and demographic changes across more than 200 years of evolution Shpak, Max Ghanavi, Hamid R. Lange, Jeremy D. Pool, John E. Stensmyr, Marcus C. PLoS Biol Research Article The ability to perform genomic sequencing on long-dead organisms is opening new frontiers in evolutionary research. These opportunities are especially notable in the case of museum collections, from which countless documented specimens may now be suitable for genomic analysis—if data of sufficient quality can be obtained. Here, we report 25 newly sequenced genomes from museum specimens of the model organism Drosophila melanogaster, including the oldest extant specimens of this species. By comparing historical samples ranging from the early 1800s to 1933 against modern-day genomes, we document evolution across thousands of generations, including time periods that encompass the species’ initial occupation of northern Europe and an era of rapidly increasing human activity. We also find that the Lund, Sweden population underwent local genetic differentiation during the early 1800s to 1933 interval (potentially due to drift in a small population) but then became more similar to other European populations thereafter (potentially due to increased migration). Within each century-scale time period, our temporal sampling allows us to document compelling candidates for recent natural selection. In some cases, we gain insights regarding previously implicated selection candidates, such as ChKov1, for which our inferred timing of selection favors the hypothesis of antiviral resistance over insecticide resistance. Other candidates are novel, such as the circadian-related gene Ahcy, which yields a selection signal that rivals that of the DDT resistance gene Cyp6g1. These insights deepen our understanding of recent evolution in a model system, and highlight the potential of future museomic studies. Public Library of Science 2023-10-12 /pmc/articles/PMC10569592/ /pubmed/37824452 http://dx.doi.org/10.1371/journal.pbio.3002333 Text en © 2023 Shpak et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Shpak, Max
Ghanavi, Hamid R.
Lange, Jeremy D.
Pool, John E.
Stensmyr, Marcus C.
Genomes from historical Drosophila melanogaster specimens illuminate adaptive and demographic changes across more than 200 years of evolution
title Genomes from historical Drosophila melanogaster specimens illuminate adaptive and demographic changes across more than 200 years of evolution
title_full Genomes from historical Drosophila melanogaster specimens illuminate adaptive and demographic changes across more than 200 years of evolution
title_fullStr Genomes from historical Drosophila melanogaster specimens illuminate adaptive and demographic changes across more than 200 years of evolution
title_full_unstemmed Genomes from historical Drosophila melanogaster specimens illuminate adaptive and demographic changes across more than 200 years of evolution
title_short Genomes from historical Drosophila melanogaster specimens illuminate adaptive and demographic changes across more than 200 years of evolution
title_sort genomes from historical drosophila melanogaster specimens illuminate adaptive and demographic changes across more than 200 years of evolution
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10569592/
https://www.ncbi.nlm.nih.gov/pubmed/37824452
http://dx.doi.org/10.1371/journal.pbio.3002333
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