The origin and maintenance of supergenes contributing to ecological adaptation in Atlantic herring

Abstract Chromosomal inversions are associated with local adaptation in many species. However, questions regarding how they are formed, maintained and impact various other evolutionary processes remain elusive. Here, using a large genomic dataset of long-read and short-read sequencing, we ask these...

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Main Authors: Minal Jamsandekar, Mafalda S. Ferreira, Mats E. Pettersson, Edward D. Farrell, Brian W. Davis, Leif Andersson
Format: Article
Language:English
Published: Nature Portfolio 2024-10-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-53079-7
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author Minal Jamsandekar
Mafalda S. Ferreira
Mats E. Pettersson
Edward D. Farrell
Brian W. Davis
Leif Andersson
author_facet Minal Jamsandekar
Mafalda S. Ferreira
Mats E. Pettersson
Edward D. Farrell
Brian W. Davis
Leif Andersson
author_sort Minal Jamsandekar
collection DOAJ
description Abstract Chromosomal inversions are associated with local adaptation in many species. However, questions regarding how they are formed, maintained and impact various other evolutionary processes remain elusive. Here, using a large genomic dataset of long-read and short-read sequencing, we ask these questions in one of the most abundant vertebrates on Earth, the Atlantic herring. This species has four megabase-sized inversions associated with ecological adaptation that correlate with water temperature. The S and N inversion alleles at these four loci dominate in the southern and northern parts, respectively, of the species distribution in the North Atlantic Ocean. By determining breakpoint coordinates of the four inversions and the structural variations surrounding them, we hypothesize that these inversions are formed by ectopic recombination between duplicated sequences immediately outside of the inversions. We show that these are old inversions (>1 MY), albeit formed after the split between the Atlantic herring and its sister species, the Pacific herring. There is evidence for extensive gene flux between inversion alleles at all four loci. The large Ne of herring combined with the common occurrence of opposite homozygotes across the species distribution has allowed effective purifying selection to prevent the accumulation of genetic load and repeats within the inversions.
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spelling doaj-art-55bbfc9ad98d47a296383c18ff46dd212025-08-20T02:11:29ZengNature PortfolioNature Communications2041-17232024-10-0115111910.1038/s41467-024-53079-7The origin and maintenance of supergenes contributing to ecological adaptation in Atlantic herringMinal Jamsandekar0Mafalda S. Ferreira1Mats E. Pettersson2Edward D. Farrell3Brian W. Davis4Leif Andersson5Department of Veterinary Integrative Biosciences, Texas A&M UniversityDepartment of Medical Biochemistry and Microbiology, Uppsala UniversityDepartment of Medical Biochemistry and Microbiology, Uppsala UniversityKillybegs Fishermen’s OrganisationDepartment of Veterinary Integrative Biosciences, Texas A&M UniversityDepartment of Veterinary Integrative Biosciences, Texas A&M UniversityAbstract Chromosomal inversions are associated with local adaptation in many species. However, questions regarding how they are formed, maintained and impact various other evolutionary processes remain elusive. Here, using a large genomic dataset of long-read and short-read sequencing, we ask these questions in one of the most abundant vertebrates on Earth, the Atlantic herring. This species has four megabase-sized inversions associated with ecological adaptation that correlate with water temperature. The S and N inversion alleles at these four loci dominate in the southern and northern parts, respectively, of the species distribution in the North Atlantic Ocean. By determining breakpoint coordinates of the four inversions and the structural variations surrounding them, we hypothesize that these inversions are formed by ectopic recombination between duplicated sequences immediately outside of the inversions. We show that these are old inversions (>1 MY), albeit formed after the split between the Atlantic herring and its sister species, the Pacific herring. There is evidence for extensive gene flux between inversion alleles at all four loci. The large Ne of herring combined with the common occurrence of opposite homozygotes across the species distribution has allowed effective purifying selection to prevent the accumulation of genetic load and repeats within the inversions.https://doi.org/10.1038/s41467-024-53079-7
spellingShingle Minal Jamsandekar
Mafalda S. Ferreira
Mats E. Pettersson
Edward D. Farrell
Brian W. Davis
Leif Andersson
The origin and maintenance of supergenes contributing to ecological adaptation in Atlantic herring
Nature Communications
title The origin and maintenance of supergenes contributing to ecological adaptation in Atlantic herring
title_full The origin and maintenance of supergenes contributing to ecological adaptation in Atlantic herring
title_fullStr The origin and maintenance of supergenes contributing to ecological adaptation in Atlantic herring
title_full_unstemmed The origin and maintenance of supergenes contributing to ecological adaptation in Atlantic herring
title_short The origin and maintenance of supergenes contributing to ecological adaptation in Atlantic herring
title_sort origin and maintenance of supergenes contributing to ecological adaptation in atlantic herring
url https://doi.org/10.1038/s41467-024-53079-7
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