Genomic evidence for human-mediated introgressive hybridization and selection in the developed breed

Abstract Background The pig (Sus Scrofa) is one of the oldest domesticated livestock species that has undergone extensive improvement through modern breeding. European breeds have advantages in lean meat development and highly-productive body type, whereas Asian breeds possess extraordinary fat depo...

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Main Authors: Heng Du, Zhen Liu, Shi-Yu Lu, Li Jiang, Lei Zhou, Jian-Feng Liu
Format: Article
Language:English
Published: BMC 2024-04-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-024-10259-5
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author Heng Du
Zhen Liu
Shi-Yu Lu
Li Jiang
Lei Zhou
Jian-Feng Liu
author_facet Heng Du
Zhen Liu
Shi-Yu Lu
Li Jiang
Lei Zhou
Jian-Feng Liu
author_sort Heng Du
collection DOAJ
description Abstract Background The pig (Sus Scrofa) is one of the oldest domesticated livestock species that has undergone extensive improvement through modern breeding. European breeds have advantages in lean meat development and highly-productive body type, whereas Asian breeds possess extraordinary fat deposition and reproductive performance. Consequently, Eurasian breeds have been extensively used to develop modern commercial breeds for fast-growing and high prolificacy. However, limited by the sequencing technology, the genome architecture of some nascent developed breeds and the human-mediated impact on their genomes are still unknown. Results Through whole-genome analysis of 178 individuals from an Asian locally developed pig breed, Beijing Black pig, and its two ancestors from two different continents, we found the pervasive inconsistent gene trees and species trees across the genome of Beijing Black pig, which suggests its introgressive hybrid origin. Interestingly, we discovered that this developed breed has more genetic relationships with European pigs and an unexpected introgression from Asian pigs to this breed, which indicated that human-mediated introgression could form the porcine genome architecture in a completely different type compared to native introgression. We identified 554 genomic regions occupied 63.30 Mb with signals of introgression from the Asian ancestry to Beijing Black pig, and the genes in these regions enriched in pathways associated with meat quality, fertility, and disease-resistant. Additionally, a proportion of 7.77% of genomic regions were recognized as regions that have been under selection. Moreover, combined with the results of a genome-wide association study for meat quality traits in the 1537 Beijing Black pig population, two important candidate genes related to meat quality traits were identified. DNAJC6 is related to intramuscular fat content and fat deposition, and RUFY4 is related to meat pH and tenderness. Conclusions Our research provides insight for analyzing the origins of nascent developed breeds and genome-wide selection remaining in the developed breeds mediated by humans during modern breeding.
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spelling doaj.art-8e471bc9ffa240e8b874a67dd52cfd792024-04-07T11:09:20ZengBMCBMC Genomics1471-21642024-04-0125111410.1186/s12864-024-10259-5Genomic evidence for human-mediated introgressive hybridization and selection in the developed breedHeng Du0Zhen Liu1Shi-Yu Lu2Li Jiang3Lei Zhou4Jian-Feng Liu5State Key Laboratory of Animal Biotech Breeding, Key Laboratory of Animal Genetics and Breeding, Ministry of Agriculture, College of Animal Science and Technology, China Agricultural University (West District)State Key Laboratory of Animal Biotech Breeding, Key Laboratory of Animal Genetics and Breeding, Ministry of Agriculture, College of Animal Science and Technology, China Agricultural University (West District)State Key Laboratory of Animal Biotech Breeding, Key Laboratory of Animal Genetics and Breeding, Ministry of Agriculture, College of Animal Science and Technology, China Agricultural University (West District)State Key Laboratory of Animal Biotech Breeding, Key Laboratory of Animal Genetics and Breeding, Ministry of Agriculture, College of Animal Science and Technology, China Agricultural University (West District)State Key Laboratory of Animal Biotech Breeding, Key Laboratory of Animal Genetics and Breeding, Ministry of Agriculture, College of Animal Science and Technology, China Agricultural University (West District)State Key Laboratory of Animal Biotech Breeding, Key Laboratory of Animal Genetics and Breeding, Ministry of Agriculture, College of Animal Science and Technology, China Agricultural University (West District)Abstract Background The pig (Sus Scrofa) is one of the oldest domesticated livestock species that has undergone extensive improvement through modern breeding. European breeds have advantages in lean meat development and highly-productive body type, whereas Asian breeds possess extraordinary fat deposition and reproductive performance. Consequently, Eurasian breeds have been extensively used to develop modern commercial breeds for fast-growing and high prolificacy. However, limited by the sequencing technology, the genome architecture of some nascent developed breeds and the human-mediated impact on their genomes are still unknown. Results Through whole-genome analysis of 178 individuals from an Asian locally developed pig breed, Beijing Black pig, and its two ancestors from two different continents, we found the pervasive inconsistent gene trees and species trees across the genome of Beijing Black pig, which suggests its introgressive hybrid origin. Interestingly, we discovered that this developed breed has more genetic relationships with European pigs and an unexpected introgression from Asian pigs to this breed, which indicated that human-mediated introgression could form the porcine genome architecture in a completely different type compared to native introgression. We identified 554 genomic regions occupied 63.30 Mb with signals of introgression from the Asian ancestry to Beijing Black pig, and the genes in these regions enriched in pathways associated with meat quality, fertility, and disease-resistant. Additionally, a proportion of 7.77% of genomic regions were recognized as regions that have been under selection. Moreover, combined with the results of a genome-wide association study for meat quality traits in the 1537 Beijing Black pig population, two important candidate genes related to meat quality traits were identified. DNAJC6 is related to intramuscular fat content and fat deposition, and RUFY4 is related to meat pH and tenderness. Conclusions Our research provides insight for analyzing the origins of nascent developed breeds and genome-wide selection remaining in the developed breeds mediated by humans during modern breeding.https://doi.org/10.1186/s12864-024-10259-5PigDeveloped breedGenetic structureIntrogressionSelectionModern breeding
spellingShingle Heng Du
Zhen Liu
Shi-Yu Lu
Li Jiang
Lei Zhou
Jian-Feng Liu
Genomic evidence for human-mediated introgressive hybridization and selection in the developed breed
BMC Genomics
Pig
Developed breed
Genetic structure
Introgression
Selection
Modern breeding
title Genomic evidence for human-mediated introgressive hybridization and selection in the developed breed
title_full Genomic evidence for human-mediated introgressive hybridization and selection in the developed breed
title_fullStr Genomic evidence for human-mediated introgressive hybridization and selection in the developed breed
title_full_unstemmed Genomic evidence for human-mediated introgressive hybridization and selection in the developed breed
title_short Genomic evidence for human-mediated introgressive hybridization and selection in the developed breed
title_sort genomic evidence for human mediated introgressive hybridization and selection in the developed breed
topic Pig
Developed breed
Genetic structure
Introgression
Selection
Modern breeding
url https://doi.org/10.1186/s12864-024-10259-5
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