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

Abstract 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 op...

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Main Authors: Mijke J. van derZee, James R. Whiting, Josephine R. Paris, Ron D. Bassar, Joseph Travis, Detlef Weigel, David N. Reznick, Bonnie A. Fraser
Format: Article
Language:English
Published: Oxford University Press 2022-04-01
Series:Evolution Letters
Subjects:
Online Access:https://doi.org/10.1002/evl3.272
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author Mijke J. van derZee
James R. Whiting
Josephine R. Paris
Ron D. Bassar
Joseph Travis
Detlef Weigel
David N. Reznick
Bonnie A. Fraser
author_facet Mijke J. van derZee
James R. Whiting
Josephine R. Paris
Ron D. Bassar
Joseph Travis
Detlef Weigel
David N. Reznick
Bonnie A. Fraser
author_sort Mijke J. van derZee
collection DOAJ
description Abstract 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 doaj.art-75e0dd0f38cc471f8670b322d1fcc8bb2023-08-02T06:43:23ZengOxford University PressEvolution Letters2056-37442022-04-016214916110.1002/evl3.272Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)Mijke J. van derZee0James R. Whiting1Josephine R. Paris2Ron D. Bassar3Joseph Travis4Detlef Weigel5David N. Reznick6Bonnie A. Fraser7Biosciences University of Exeter Exeter EX4 4QD United KingdomBiosciences University of Exeter Exeter EX4 4QD United KingdomBiosciences University of Exeter Exeter EX4 4QD United KingdomDepartment of Biology Williams College Williamstown Massachusetts 01267Department of Biological Science Florida State University Tallahassee Florida 32306Department of Molecular Biology Max Planck Institute for Developmental Biology Tübingen 72076 GermanyDepartment of Biology University of California, Riverside Riverside California 92521Biosciences University of Exeter Exeter EX4 4QD United KingdomAbstract 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.https://doi.org/10.1002/evl3.272Convergent evolutionexperimental evolutionguppiesPoecilia reticulatapopulation genomicsrapid evolution
spellingShingle Mijke J. van derZee
James R. Whiting
Josephine R. Paris
Ron D. Bassar
Joseph Travis
Detlef Weigel
David N. Reznick
Bonnie A. Fraser
Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)
Evolution Letters
Convergent evolution
experimental evolution
guppies
Poecilia reticulata
population genomics
rapid evolution
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 Convergent evolution
experimental evolution
guppies
Poecilia reticulata
population genomics
rapid evolution
url https://doi.org/10.1002/evl3.272
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