Complete Genomic Landscape Reveals Hidden Evolutionary History and Selection Signature in Asian Water Buffaloes (Bubalus bubalis)

Abstract To identify the genetic determinants of domestication and productivity of Asian water buffaloes (Bubalus bubalis), 470 genomes of domesticated river and swamp buffaloes along with their putative ancestors, the wild water buffaloes (Bubalus arnee) are sequenced and integrated. The swamp buff...

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Main Authors: Jingfang Si, Dongmei Dai, Neena Amatya Gorkhali, Mingshan Wang, Sheng Wang, Saroj Sapkota, Ram Chandra Kadel, Amir Sadaula, Aashish Dhakal, Md Omar Faruque, Abdullah Ibne Omar, Eka Meutia Sari, Hidayat Ashari, Muhammad Ihsan Andi Dagong, Marnoch Yindee, Hossam E. Rushdi, Hussein Elregalaty, Ahmed Amin, Mohamed A. Radwan, Lan Doan Pham, W. M. M. P. Hulugalla, G. L. L. Pradeepa Silva, Wei Zheng, Shahid Mansoor, Muhammad Basil Ali, Farhad Vahidi, Sahar Ahmed Al‐Bayatti, Alfredo Pauciullo, Johannes A. Lenstra, J. Stuart F. Barker, Lingzhao Fang, Dong‐Dong Wu, Jianlin Han, Yi Zhang
Format: Article
Language:English
Published: Wiley 2025-01-01
Series:Advanced Science
Subjects:
Online Access:https://doi.org/10.1002/advs.202407615
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author Jingfang Si
Dongmei Dai
Neena Amatya Gorkhali
Mingshan Wang
Sheng Wang
Saroj Sapkota
Ram Chandra Kadel
Amir Sadaula
Aashish Dhakal
Md Omar Faruque
Abdullah Ibne Omar
Eka Meutia Sari
Hidayat Ashari
Muhammad Ihsan Andi Dagong
Marnoch Yindee
Hossam E. Rushdi
Hussein Elregalaty
Ahmed Amin
Mohamed A. Radwan
Lan Doan Pham
W. M. M. P. Hulugalla
G. L. L. Pradeepa Silva
Wei Zheng
Shahid Mansoor
Muhammad Basil Ali
Farhad Vahidi
Sahar Ahmed Al‐Bayatti
Alfredo Pauciullo
Johannes A. Lenstra
J. Stuart F. Barker
Lingzhao Fang
Dong‐Dong Wu
Jianlin Han
Yi Zhang
author_facet Jingfang Si
Dongmei Dai
Neena Amatya Gorkhali
Mingshan Wang
Sheng Wang
Saroj Sapkota
Ram Chandra Kadel
Amir Sadaula
Aashish Dhakal
Md Omar Faruque
Abdullah Ibne Omar
Eka Meutia Sari
Hidayat Ashari
Muhammad Ihsan Andi Dagong
Marnoch Yindee
Hossam E. Rushdi
Hussein Elregalaty
Ahmed Amin
Mohamed A. Radwan
Lan Doan Pham
W. M. M. P. Hulugalla
G. L. L. Pradeepa Silva
Wei Zheng
Shahid Mansoor
Muhammad Basil Ali
Farhad Vahidi
Sahar Ahmed Al‐Bayatti
Alfredo Pauciullo
Johannes A. Lenstra
J. Stuart F. Barker
Lingzhao Fang
Dong‐Dong Wu
Jianlin Han
Yi Zhang
author_sort Jingfang Si
collection DOAJ
description Abstract To identify the genetic determinants of domestication and productivity of Asian water buffaloes (Bubalus bubalis), 470 genomes of domesticated river and swamp buffaloes along with their putative ancestors, the wild water buffaloes (Bubalus arnee) are sequenced and integrated. The swamp buffaloes inherit the morphology of the wild buffaloes. In contrast, most river buffaloes are unique in their morphology, but their genomes cluster with the wild buffaloes. The levels of genomic diversity in Italian river and Indonesian swamp buffaloes decrease at opposite extremes of their distribution range. Purifying selection prevented the accumulation of harmful loss‐of‐function variants in the Indonesian buffaloes. Genes that evolved rapidly (e.g., GKAP1) following differential selections in the river and swamp buffaloes are involved in their reproduction. Genes related to milk production (e.g., CSN2) and coat color (e.g., MC1R) underwent strong selections in the dairy river buffaloes via soft and hard selective sweeps, respectively. The selective sweeps and single‐cell RNA‐seq data revealed the luminal cells as the key cell type in response to artificial selection for milk production of the dairy buffaloes. These findings show how artificial selection has been driving the evolutionary divergence and genetic differentiation in morphology and productivity of Asian water buffaloes.
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spelling doaj-art-82e84e609da44990a24f395850ac94e02025-01-29T09:50:19ZengWileyAdvanced Science2198-38442025-01-01124n/an/a10.1002/advs.202407615Complete Genomic Landscape Reveals Hidden Evolutionary History and Selection Signature in Asian Water Buffaloes (Bubalus bubalis)Jingfang Si0Dongmei Dai1Neena Amatya Gorkhali2Mingshan Wang3Sheng Wang4Saroj Sapkota5Ram Chandra Kadel6Amir Sadaula7Aashish Dhakal8Md Omar Faruque9Abdullah Ibne Omar10Eka Meutia Sari11Hidayat Ashari12Muhammad Ihsan Andi Dagong13Marnoch Yindee14Hossam E. Rushdi15Hussein Elregalaty16Ahmed Amin17Mohamed A. Radwan18Lan Doan Pham19W. M. M. P. Hulugalla20G. L. L. Pradeepa Silva21Wei Zheng22Shahid Mansoor23Muhammad Basil Ali24Farhad Vahidi25Sahar Ahmed Al‐Bayatti26Alfredo Pauciullo27Johannes A. Lenstra28J. Stuart F. Barker29Lingzhao Fang30Dong‐Dong Wu31Jianlin Han32Yi Zhang33State Key Laboratory of Animal Biotech Breeding, National Engineering Laboratory for Animal Breeding Key Laboratory of Animal Genetics Breeding and Reproduction of Ministry of Agriculture and Rural Affairs College of Animal Science and Technology China Agricultural University Beijing 100193 ChinaState Key Laboratory of Animal Biotech Breeding, National Engineering Laboratory for Animal Breeding Key Laboratory of Animal Genetics Breeding and Reproduction of Ministry of Agriculture and Rural Affairs College of Animal Science and Technology China Agricultural University Beijing 100193 ChinaNational Animal Breeding and Genetics Research Centre National Animal Science Research Institute Nepal Agriculture Research Council Khumaltar Lalitpur NepalState Key Laboratory of Genetic Resources and Evolution Yunnan Laboratory of Molecular Biology of Domestic Animals Kunming Institute of Zoology Chinese Academy of Sciences Kunming 650023 ChinaState Key Laboratory of Genetic Resources and Evolution Yunnan Laboratory of Molecular Biology of Domestic Animals Kunming Institute of Zoology Chinese Academy of Sciences Kunming 650023 ChinaNational Animal Breeding and Genetics Research Centre National Animal Science Research Institute Nepal Agriculture Research Council Khumaltar Lalitpur NepalMinistry of Industry, Tourism, Forests and Environment Government of Gandaki Province Pokhara NepalNational Trust for Nature Conservation‐ Biodiversity Conservation Center Sauraha Chitwan NepalState Key Laboratory of Animal Biotech Breeding, National Engineering Laboratory for Animal Breeding Key Laboratory of Animal Genetics Breeding and Reproduction of Ministry of Agriculture and Rural Affairs College of Animal Science and Technology China Agricultural University Beijing 100193 ChinaDepartment of Animal Breeding and Genetics Bangladesh Agricultural University Mymensingh 2202 BangladeshState Key Laboratory of Animal Biotech Breeding, National Engineering Laboratory for Animal Breeding Key Laboratory of Animal Genetics Breeding and Reproduction of Ministry of Agriculture and Rural Affairs College of Animal Science and Technology China Agricultural University Beijing 100193 ChinaDepartment of Animal Science Faculty of Agriculture Syiah Kuala University Darussalam‐Banda Aceh 23111 IndonesiaDepartment of Animal Science Faculty of Agriculture Syiah Kuala University Darussalam‐Banda Aceh 23111 IndonesiaAnimal Science Faculty Hasanuddin University Makassar IndonesiaAkkhraratchakumari Veterinary College Walailak University Thaiburi 222 ThailandDepartment of Animal Production Faculty of Agriculture Cairo University Algammaa Street Giza 12613 EgyptAnimal Production Research Institute Agricultural Research Center Dokki Giza EgyptDepartment of Animal Production Faculty of Agriculture Cairo University Algammaa Street Giza 12613 EgyptDepartment of Animal Production Faculty of Agriculture Cairo University Algammaa Street Giza 12613 EgyptKey Laboratory of Animal Cell Technology National Institute of Animal Sciences Tu Liem Hanoi 100000 VietnamDepartment of Animal Science Faculty of Agriculture University of Peradeniya Sri LankaDepartment of Animal Science Faculty of Agriculture University of Peradeniya Sri LankaGuangxi Key Laboratory of Buffalo Genetics, Reproduction and Breeding Guangxi Buffalo Research Institute Chinese Academy of Agricultural Sciences Nanning 530001 ChinaNational Institute for Biotechnology and Genetic Engineering (NIBGE) Faisalabad PakistanNational Institute for Biotechnology and Genetic Engineering (NIBGE) Faisalabad PakistanDepartment of Genomics Agricultural Biotechnology Research Institute of Iran‐North Branch (ABRII) Rasht IranMedical Laboratory Techniques Department Al‐Farabi University College Ministry of Higher Education and Scientific Research Baghdad IraqDepartment of Agricultural, Forest and Food Sciences University of Turin Grugliasco (TO) 10095 ItalyFaculty of Veterinary Medicine Utrecht University Yalelaan 104 Utrecht CM 3584 The NetherlandsSchool of Environmental and Rural Science University of New England Armidale NSW 2351 AustraliaThe Center for Quantitative Genetics and Genomics (QGG) Aarhus University Aarhus 8000 DenmarkState Key Laboratory of Genetic Resources and Evolution Yunnan Laboratory of Molecular Biology of Domestic Animals Kunming Institute of Zoology Chinese Academy of Sciences Kunming 650023 ChinaYazhouwan National Laboratory Sanya 572024 ChinaState Key Laboratory of Animal Biotech Breeding, National Engineering Laboratory for Animal Breeding Key Laboratory of Animal Genetics Breeding and Reproduction of Ministry of Agriculture and Rural Affairs College of Animal Science and Technology China Agricultural University Beijing 100193 ChinaAbstract To identify the genetic determinants of domestication and productivity of Asian water buffaloes (Bubalus bubalis), 470 genomes of domesticated river and swamp buffaloes along with their putative ancestors, the wild water buffaloes (Bubalus arnee) are sequenced and integrated. The swamp buffaloes inherit the morphology of the wild buffaloes. In contrast, most river buffaloes are unique in their morphology, but their genomes cluster with the wild buffaloes. The levels of genomic diversity in Italian river and Indonesian swamp buffaloes decrease at opposite extremes of their distribution range. Purifying selection prevented the accumulation of harmful loss‐of‐function variants in the Indonesian buffaloes. Genes that evolved rapidly (e.g., GKAP1) following differential selections in the river and swamp buffaloes are involved in their reproduction. Genes related to milk production (e.g., CSN2) and coat color (e.g., MC1R) underwent strong selections in the dairy river buffaloes via soft and hard selective sweeps, respectively. The selective sweeps and single‐cell RNA‐seq data revealed the luminal cells as the key cell type in response to artificial selection for milk production of the dairy buffaloes. These findings show how artificial selection has been driving the evolutionary divergence and genetic differentiation in morphology and productivity of Asian water buffaloes.https://doi.org/10.1002/advs.202407615buffaloCSN2MC1Rpopulation genomicsselectionsingle‐cell RNA‐seq
spellingShingle Jingfang Si
Dongmei Dai
Neena Amatya Gorkhali
Mingshan Wang
Sheng Wang
Saroj Sapkota
Ram Chandra Kadel
Amir Sadaula
Aashish Dhakal
Md Omar Faruque
Abdullah Ibne Omar
Eka Meutia Sari
Hidayat Ashari
Muhammad Ihsan Andi Dagong
Marnoch Yindee
Hossam E. Rushdi
Hussein Elregalaty
Ahmed Amin
Mohamed A. Radwan
Lan Doan Pham
W. M. M. P. Hulugalla
G. L. L. Pradeepa Silva
Wei Zheng
Shahid Mansoor
Muhammad Basil Ali
Farhad Vahidi
Sahar Ahmed Al‐Bayatti
Alfredo Pauciullo
Johannes A. Lenstra
J. Stuart F. Barker
Lingzhao Fang
Dong‐Dong Wu
Jianlin Han
Yi Zhang
Complete Genomic Landscape Reveals Hidden Evolutionary History and Selection Signature in Asian Water Buffaloes (Bubalus bubalis)
Advanced Science
buffalo
CSN2
MC1R
population genomics
selection
single‐cell RNA‐seq
title Complete Genomic Landscape Reveals Hidden Evolutionary History and Selection Signature in Asian Water Buffaloes (Bubalus bubalis)
title_full Complete Genomic Landscape Reveals Hidden Evolutionary History and Selection Signature in Asian Water Buffaloes (Bubalus bubalis)
title_fullStr Complete Genomic Landscape Reveals Hidden Evolutionary History and Selection Signature in Asian Water Buffaloes (Bubalus bubalis)
title_full_unstemmed Complete Genomic Landscape Reveals Hidden Evolutionary History and Selection Signature in Asian Water Buffaloes (Bubalus bubalis)
title_short Complete Genomic Landscape Reveals Hidden Evolutionary History and Selection Signature in Asian Water Buffaloes (Bubalus bubalis)
title_sort complete genomic landscape reveals hidden evolutionary history and selection signature in asian water buffaloes bubalus bubalis
topic buffalo
CSN2
MC1R
population genomics
selection
single‐cell RNA‐seq
url https://doi.org/10.1002/advs.202407615
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