Yali Hou1,2, Furong Qi3,4,5, Xue Bai3,4, Tong Ren3, Xu Shen3, Qin Chu6, Xiquan Zhang7, Xuemei Lu8,9,10. 1. Key Laboratory of Genomic and Precision Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, People's Republic of China. houyl@big.ac.cn. 2. China National Center for Bioinformation, Beijing, People's Republic of China. houyl@big.ac.cn. 3. Key Laboratory of Genomic and Precision Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, People's Republic of China. 4. China National Center for Bioinformation, Beijing, People's Republic of China. 5. University of Chinese Academy of Sciences, Beijing, People's Republic of China. 6. Institute of Animal Husbandry and Veterinary Medicine, Beijing Academy of Agriculture and Forestry Sciences, Beijing, People's Republic of China. 7. Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, and Key Lab of Chicken Genetics, Breeding and Reproduction, Ministry of Agriculture, South China Agricultural University, Guangzhou, People's Republic of China. xqzhang@scau.edu.cn. 8. Key Laboratory of Genomic and Precision Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, People's Republic of China. xuemeilu@mail.kiz.ac.cn. 9. University of Chinese Academy of Sciences, Beijing, People's Republic of China. xuemeilu@mail.kiz.ac.cn. 10. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, People's Republic of China. xuemeilu@mail.kiz.ac.cn.
Abstract
BACKGROUND: In response to ecological niche of domestication, domesticated mammals and birds developed adaptively phenotypic homoplasy in behavior modifications like fearlessness, altered sociability, exploration and cognition, which partly or indirectly result in consequences for economic productivity. Such independent adaptations provide an excellent model to investigate molecular mechanisms and patterns of evolutionary convergence driven by artificial selection. RESULTS: First performing population genomic and brain transcriptional comparisons in 68 wild and domesticated chickens, we revealed evolutionary trajectories, genetic architectures and physiologic bases of adaptively behavioral alterations. To extensively decipher molecular convergence on behavioral changes thanks to domestication, we investigated selection signatures in hundreds of genomes and brain transcriptomes across chicken and 6 other domesticated mammals. Although no shared substitution was detected, a common enrichment of the adaptive mutations in regulatory sequences was observed, presenting significance to drive adaptations. Strong convergent pattern emerged at levels of gene, gene family, pathway and network. Genes implicated in neurotransmission, semaphorin, tectonic protein and modules regulating neuroplasticity were central focus of selection, supporting molecular repeatability of homoplastic behavior reshapes. Genes at nodal positions in trans-regulatory networks were preferably targeted. Consistent down-regulation of majority brain genes may be correlated with reduced brain size during domestication. Up-regulation of splicesome genes in chicken rather mammals highlights splicing as an efficient way to evolve since avian-specific genomic contraction of introns and intergenics. Genetic burden of domestication elicits a general hallmark. The commonly selected genes were relatively evolutionary conserved and associated with analogous neuropsychiatric disorders in human, revealing trade-off between adaption to life with human at the cost of neural changes affecting fitness in wild. CONCLUSIONS: After a comprehensive investigation on genomic diversity and evolutionary trajectories in chickens, we revealed basis, pattern and evolutionary significance of molecular convergence in domesticated bird and mammals, highlighted the genetic basis of a compromise on utmost adaptation to the lives with human at the cost of high risk of neurophysiological changes affecting animals' fitness in wild.
BACKGROUND: In response to ecological niche of domestication, domesticated mammals and birds developed adaptively phenotypic homoplasy in behavior modifications like fearlessness, altered sociability, exploration and cognition, which partly or indirectly result in consequences for economic productivity. Such independent adaptations provide an excellent model to investigate molecular mechanisms and patterns of evolutionary convergence driven by artificial selection. RESULTS: First performing population genomic and brain transcriptional comparisons in 68 wild and domesticated chickens, we revealed evolutionary trajectories, genetic architectures and physiologic bases of adaptively behavioral alterations. To extensively decipher molecular convergence on behavioral changes thanks to domestication, we investigated selection signatures in hundreds of genomes and brain transcriptomes across chicken and 6 other domesticated mammals. Although no shared substitution was detected, a common enrichment of the adaptive mutations in regulatory sequences was observed, presenting significance to drive adaptations. Strong convergent pattern emerged at levels of gene, gene family, pathway and network. Genes implicated in neurotransmission, semaphorin, tectonic protein and modules regulating neuroplasticity were central focus of selection, supporting molecular repeatability of homoplastic behavior reshapes. Genes at nodal positions in trans-regulatory networks were preferably targeted. Consistent down-regulation of majority brain genes may be correlated with reduced brain size during domestication. Up-regulation of splicesome genes in chicken rather mammals highlights splicing as an efficient way to evolve since avian-specific genomic contraction of introns and intergenics. Genetic burden of domestication elicits a general hallmark. The commonly selected genes were relatively evolutionary conserved and associated with analogous neuropsychiatric disorders in human, revealing trade-off between adaption to life with human at the cost of neural changes affecting fitness in wild. CONCLUSIONS: After a comprehensive investigation on genomic diversity and evolutionary trajectories in chickens, we revealed basis, pattern and evolutionary significance of molecular convergence in domesticated bird and mammals, highlighted the genetic basis of a compromise on utmost adaptation to the lives with human at the cost of high risk of neurophysiological changes affecting animals' fitness in wild.
Entities:
Keywords:
Artificial selection; Behavioral modification; Convergent evolution; Domestication and adaptation