Hybrid adaptation is hampered by Haldane’s sieve

Abstract Hybrids between species exhibit plastic genomic architectures that could foster or slow down their adaptation. When challenged to evolve in an environment containing a UV mimetic drug, yeast hybrids have reduced adaptation rates compared to parents. We find that hybrids and their parents co...

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Main Authors: Carla Bautista, Isabelle Gagnon-Arsenault, Mariia Utrobina, Anna Fijarczyk, Devin P. Bendixsen, Rike Stelkens, Christian R. Landry
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54105-4
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author Carla Bautista
Isabelle Gagnon-Arsenault
Mariia Utrobina
Anna Fijarczyk
Devin P. Bendixsen
Rike Stelkens
Christian R. Landry
author_facet Carla Bautista
Isabelle Gagnon-Arsenault
Mariia Utrobina
Anna Fijarczyk
Devin P. Bendixsen
Rike Stelkens
Christian R. Landry
author_sort Carla Bautista
collection DOAJ
description Abstract Hybrids between species exhibit plastic genomic architectures that could foster or slow down their adaptation. When challenged to evolve in an environment containing a UV mimetic drug, yeast hybrids have reduced adaptation rates compared to parents. We find that hybrids and their parents converge onto similar molecular mechanisms of adaptation by mutations in pleiotropic transcription factors, but at a different pace. After 100 generations, mutations in these genes tend to be homozygous in the parents but heterozygous in the hybrids. We hypothesize that a lower rate of loss of heterozygosity (LOH) in hybrids could limit fitness gain. Using genome editing, we first demonstrate that mutations display incomplete dominance, requiring homozygosity to show full impact and to entirely circumvent Haldane’s sieve, which favors the fixation of dominant mutations. Second, tracking mutations in earlier generations confirmed a different rate of LOH in hybrids. Together, these findings show that Haldane’s sieve slows down adaptation in hybrids, revealing an intrinsic constraint of hybrid genomic architecture that can limit the role of hybridization in adaptive evolution.
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issn 2041-1723
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spelling doaj-art-473340992c6f4f369da92ede7d70a2a92024-12-01T12:36:21ZengNature PortfolioNature Communications2041-17232024-11-0115111610.1038/s41467-024-54105-4Hybrid adaptation is hampered by Haldane’s sieveCarla Bautista0Isabelle Gagnon-Arsenault1Mariia Utrobina2Anna Fijarczyk3Devin P. Bendixsen4Rike Stelkens5Christian R. Landry6Institut de Biologie Intégrative et des Systèmes (IBIS), Université LavalInstitut de Biologie Intégrative et des Systèmes (IBIS), Université LavalInstitut de Biologie Intégrative et des Systèmes (IBIS), Université LavalInstitut de Biologie Intégrative et des Systèmes (IBIS), Université LavalDepartment of Zoology, Stockholm UniversityDepartment of Zoology, Stockholm UniversityInstitut de Biologie Intégrative et des Systèmes (IBIS), Université LavalAbstract Hybrids between species exhibit plastic genomic architectures that could foster or slow down their adaptation. When challenged to evolve in an environment containing a UV mimetic drug, yeast hybrids have reduced adaptation rates compared to parents. We find that hybrids and their parents converge onto similar molecular mechanisms of adaptation by mutations in pleiotropic transcription factors, but at a different pace. After 100 generations, mutations in these genes tend to be homozygous in the parents but heterozygous in the hybrids. We hypothesize that a lower rate of loss of heterozygosity (LOH) in hybrids could limit fitness gain. Using genome editing, we first demonstrate that mutations display incomplete dominance, requiring homozygosity to show full impact and to entirely circumvent Haldane’s sieve, which favors the fixation of dominant mutations. Second, tracking mutations in earlier generations confirmed a different rate of LOH in hybrids. Together, these findings show that Haldane’s sieve slows down adaptation in hybrids, revealing an intrinsic constraint of hybrid genomic architecture that can limit the role of hybridization in adaptive evolution.https://doi.org/10.1038/s41467-024-54105-4
spellingShingle Carla Bautista
Isabelle Gagnon-Arsenault
Mariia Utrobina
Anna Fijarczyk
Devin P. Bendixsen
Rike Stelkens
Christian R. Landry
Hybrid adaptation is hampered by Haldane’s sieve
Nature Communications
title Hybrid adaptation is hampered by Haldane’s sieve
title_full Hybrid adaptation is hampered by Haldane’s sieve
title_fullStr Hybrid adaptation is hampered by Haldane’s sieve
title_full_unstemmed Hybrid adaptation is hampered by Haldane’s sieve
title_short Hybrid adaptation is hampered by Haldane’s sieve
title_sort hybrid adaptation is hampered by haldane s sieve
url https://doi.org/10.1038/s41467-024-54105-4
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