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Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)

Although rapid phenotypic evolution has been documented often, the genomic basis of rapid adaptation to natural environments is largely unknown in multicellular organisms. Population genomic studies of experimental populations of Trinidadian guppies (Poecilia reticulata) provide a unique opportunity...

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Autores principales: van der Zee, Mijke J., Whiting, James R., Paris, Josephine R., Bassar, Ron D., Travis, Joseph, Weigel, Detlef, Reznick, David N., Fraser, Bonnie A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8966473/
https://www.ncbi.nlm.nih.gov/pubmed/35386829
http://dx.doi.org/10.1002/evl3.272
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author van der Zee, Mijke J.
Whiting, James R.
Paris, Josephine R.
Bassar, Ron D.
Travis, Joseph
Weigel, Detlef
Reznick, David N.
Fraser, Bonnie A.
author_facet van der Zee, Mijke J.
Whiting, James R.
Paris, Josephine R.
Bassar, Ron D.
Travis, Joseph
Weigel, Detlef
Reznick, David N.
Fraser, Bonnie A.
author_sort van der Zee, Mijke J.
collection PubMed
description Although rapid phenotypic evolution has been documented often, the genomic basis of rapid adaptation to natural environments is largely unknown in multicellular organisms. Population genomic studies of experimental populations of Trinidadian guppies (Poecilia reticulata) provide a unique opportunity to study this phenomenon. Guppy populations that were transplanted from high‐predation (HP) to low‐predation (LP) environments have been shown to evolve toward the phenotypes of naturally colonized LP populations in as few as eight generations. These changes persist in common garden experiments, indicating that they have a genetic basis. Here, we report results of whole genome variation in four experimental populations colonizing LP sites along with the corresponding HP source population. We examined genome‐wide patterns of genetic variation to estimate past demography and used a combination of genome scans, forward simulations, and a novel analysis of allele frequency change vectors to uncover the signature of selection. We detected clear signals of population growth and bottlenecks at the genome‐wide level that matched the known history of population numbers. We found a region on chromosome 15 under strong selection in three of the four populations and with our multivariate approach revealing subtle parallel changes in allele frequency in all four populations across this region. Investigating patterns of genome‐wide selection in this uniquely replicated experiment offers remarkable insight into the mechanisms underlying rapid adaptation, providing a basis for comparison with other species and populations experiencing rapidly changing environments.
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spelling pubmed-89664732022-04-05 Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata) van der Zee, Mijke J. Whiting, James R. Paris, Josephine R. Bassar, Ron D. Travis, Joseph Weigel, Detlef Reznick, David N. Fraser, Bonnie A. Evol Lett Letters Although rapid phenotypic evolution has been documented often, the genomic basis of rapid adaptation to natural environments is largely unknown in multicellular organisms. Population genomic studies of experimental populations of Trinidadian guppies (Poecilia reticulata) provide a unique opportunity to study this phenomenon. Guppy populations that were transplanted from high‐predation (HP) to low‐predation (LP) environments have been shown to evolve toward the phenotypes of naturally colonized LP populations in as few as eight generations. These changes persist in common garden experiments, indicating that they have a genetic basis. Here, we report results of whole genome variation in four experimental populations colonizing LP sites along with the corresponding HP source population. We examined genome‐wide patterns of genetic variation to estimate past demography and used a combination of genome scans, forward simulations, and a novel analysis of allele frequency change vectors to uncover the signature of selection. We detected clear signals of population growth and bottlenecks at the genome‐wide level that matched the known history of population numbers. We found a region on chromosome 15 under strong selection in three of the four populations and with our multivariate approach revealing subtle parallel changes in allele frequency in all four populations across this region. Investigating patterns of genome‐wide selection in this uniquely replicated experiment offers remarkable insight into the mechanisms underlying rapid adaptation, providing a basis for comparison with other species and populations experiencing rapidly changing environments. John Wiley and Sons Inc. 2022-01-18 /pmc/articles/PMC8966473/ /pubmed/35386829 http://dx.doi.org/10.1002/evl3.272 Text en © 2022 The Authors. Evolution Letters published by Wiley Periodicals LLC on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB). https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Letters
van der Zee, Mijke J.
Whiting, James R.
Paris, Josephine R.
Bassar, Ron D.
Travis, Joseph
Weigel, Detlef
Reznick, David N.
Fraser, Bonnie A.
Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)
title Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)
title_full Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)
title_fullStr Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)
title_full_unstemmed Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)
title_short Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)
title_sort rapid genomic convergent evolution in experimental populations of trinidadian guppies (poecilia reticulata)
topic Letters
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8966473/
https://www.ncbi.nlm.nih.gov/pubmed/35386829
http://dx.doi.org/10.1002/evl3.272
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