Chromosome‐Level Genome Assembly and Whole‐Genome Resequencing Revealed Contrasting Population Genetic Differentiation of Black Bream (Megalobrama skolkovii) (Teleostei: Cyprinidae) Allopatric and Sympatric to Its Kin Species

ABSTRACT The black bream (Megalobrama skolkovii) is an economically important species widely distributed in China, with its geographic populations potentially having undergone differentiations and local adaptations. In this study, we presented a chromosome‐level genome assembly of this species and i...

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Main Authors: Ruijin Ding, Dan Yu, Ke Yang, Xinghua Wu, Huanzhang Liu
Format: Article
Language:English
Published: Wiley 2025-01-01
Series:Ecology and Evolution
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Online Access:https://doi.org/10.1002/ece3.70874
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author Ruijin Ding
Dan Yu
Ke Yang
Xinghua Wu
Huanzhang Liu
author_facet Ruijin Ding
Dan Yu
Ke Yang
Xinghua Wu
Huanzhang Liu
author_sort Ruijin Ding
collection DOAJ
description ABSTRACT The black bream (Megalobrama skolkovii) is an economically important species widely distributed in China, with its geographic populations potentially having undergone differentiations and local adaptations. In this study, we presented a chromosome‐level genome assembly of this species and investigated genetic differentiations of its populations that are allopatric (the northern one) and sympatric (the Poyang Lake) to its kin species, the blunt‐snout bream (M. amblycephala), using whole genome resequencing analysis. The results showed that the genome size of black bream was 1.13 Gb, very similar to its kin species but larger than its close relatives, the four Chinese major carps. By resequencing individuals from the northern and Poyang Lake populations, we found that the northern population showed lower genetic diversity, larger genetic differentiation, and two sharp historical declines in population size through demographic analysis, indicating the possible bottlenecks after the allopatric isolation. In contrast, the Poyang Lake population, with its higher genetic diversity, higher Tajima's D value, and lower levels of linkage disequilibrium, reflects the ancestral state of black bream. In addition, we also found that the northern population shared more alleles with its kin species, indicating it may retain more ancestral variations. This was further analyzed to be caused by incomplete lineage sorting and ancient introgression. Some key genes related to reproductive processes, body size development, and muscle metabolism were found under selection in the northern population, possibly responsible for its local adaptation. Our findings that the black bream allopatric population had a loss of genetic diversity but retained more ancestral variations can expand our knowledge on population genetic differentiation and give us hints for future genetic conservation.
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spelling doaj-art-5a21ffbe3f2e451cb90b3daee25403792025-01-29T05:08:42ZengWileyEcology and Evolution2045-77582025-01-01151n/an/a10.1002/ece3.70874Chromosome‐Level Genome Assembly and Whole‐Genome Resequencing Revealed Contrasting Population Genetic Differentiation of Black Bream (Megalobrama skolkovii) (Teleostei: Cyprinidae) Allopatric and Sympatric to Its Kin SpeciesRuijin Ding0Dan Yu1Ke Yang2Xinghua Wu3Huanzhang Liu4State Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology Chinese Academy of Sciences Wuhan ChinaState Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology Chinese Academy of Sciences Wuhan ChinaState Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology Chinese Academy of Sciences Wuhan ChinaResearch Center for Yangtze River Ecological and Environmental Engineering China Three Gorges Corporation Beijing ChinaState Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture, Institute of Hydrobiology Chinese Academy of Sciences Wuhan ChinaABSTRACT The black bream (Megalobrama skolkovii) is an economically important species widely distributed in China, with its geographic populations potentially having undergone differentiations and local adaptations. In this study, we presented a chromosome‐level genome assembly of this species and investigated genetic differentiations of its populations that are allopatric (the northern one) and sympatric (the Poyang Lake) to its kin species, the blunt‐snout bream (M. amblycephala), using whole genome resequencing analysis. The results showed that the genome size of black bream was 1.13 Gb, very similar to its kin species but larger than its close relatives, the four Chinese major carps. By resequencing individuals from the northern and Poyang Lake populations, we found that the northern population showed lower genetic diversity, larger genetic differentiation, and two sharp historical declines in population size through demographic analysis, indicating the possible bottlenecks after the allopatric isolation. In contrast, the Poyang Lake population, with its higher genetic diversity, higher Tajima's D value, and lower levels of linkage disequilibrium, reflects the ancestral state of black bream. In addition, we also found that the northern population shared more alleles with its kin species, indicating it may retain more ancestral variations. This was further analyzed to be caused by incomplete lineage sorting and ancient introgression. Some key genes related to reproductive processes, body size development, and muscle metabolism were found under selection in the northern population, possibly responsible for its local adaptation. Our findings that the black bream allopatric population had a loss of genetic diversity but retained more ancestral variations can expand our knowledge on population genetic differentiation and give us hints for future genetic conservation.https://doi.org/10.1002/ece3.70874ancestral polymorphismblack breamfounder effectspopulation bottleneckspopulation differentiationpopulation genomics
spellingShingle Ruijin Ding
Dan Yu
Ke Yang
Xinghua Wu
Huanzhang Liu
Chromosome‐Level Genome Assembly and Whole‐Genome Resequencing Revealed Contrasting Population Genetic Differentiation of Black Bream (Megalobrama skolkovii) (Teleostei: Cyprinidae) Allopatric and Sympatric to Its Kin Species
Ecology and Evolution
ancestral polymorphism
black bream
founder effects
population bottlenecks
population differentiation
population genomics
title Chromosome‐Level Genome Assembly and Whole‐Genome Resequencing Revealed Contrasting Population Genetic Differentiation of Black Bream (Megalobrama skolkovii) (Teleostei: Cyprinidae) Allopatric and Sympatric to Its Kin Species
title_full Chromosome‐Level Genome Assembly and Whole‐Genome Resequencing Revealed Contrasting Population Genetic Differentiation of Black Bream (Megalobrama skolkovii) (Teleostei: Cyprinidae) Allopatric and Sympatric to Its Kin Species
title_fullStr Chromosome‐Level Genome Assembly and Whole‐Genome Resequencing Revealed Contrasting Population Genetic Differentiation of Black Bream (Megalobrama skolkovii) (Teleostei: Cyprinidae) Allopatric and Sympatric to Its Kin Species
title_full_unstemmed Chromosome‐Level Genome Assembly and Whole‐Genome Resequencing Revealed Contrasting Population Genetic Differentiation of Black Bream (Megalobrama skolkovii) (Teleostei: Cyprinidae) Allopatric and Sympatric to Its Kin Species
title_short Chromosome‐Level Genome Assembly and Whole‐Genome Resequencing Revealed Contrasting Population Genetic Differentiation of Black Bream (Megalobrama skolkovii) (Teleostei: Cyprinidae) Allopatric and Sympatric to Its Kin Species
title_sort chromosome level genome assembly and whole genome resequencing revealed contrasting population genetic differentiation of black bream megalobrama skolkovii teleostei cyprinidae allopatric and sympatric to its kin species
topic ancestral polymorphism
black bream
founder effects
population bottlenecks
population differentiation
population genomics
url https://doi.org/10.1002/ece3.70874
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