Integration of Genomes and Transcriptomes Traces Evolutionary Trajectories Underlying Remould of Ingenious Red Jungle Fowls into Today's Diversified Dynamos

Domestication has been served as a fascinating model to posit evolutionary theory. Taking chicken as an important model organism, which has been subjected to intensive human remould hence remarkable diversity in behavior, morphology and physiology, we systematically provided detailed glimpses into the genetic legacy of domestication and centuries of breeding practices. Based on the whole-genome genetic variations, we scrutinized the comprehensive population characteristics underlying selective and non-selective forces among contemporary chickens, revealing intensive introgressions including feralization that violate the canonical assumption of reproductive isolation and warrant future studies. We provided the first molecular evidence of chicken domestication time. We disclosed a deleterious genetic load of domestication in terms of accumulation of deleterious mutants attributing to the Hill-Robertson effect or relaxed selection. Putative selective sweep analysis revealed that domesticated chickens have dominated remarkable alterations in nervous system, leading to distinguished behavior modifications of reduced fear response, shrunk explorative tendency and activity, degraded circadian rhythm, as well as impaired learning and memory capability. Additionally, we also identified the genetic basis of degenerated vision prowess, accelerated growth, enlarged body size, increased lipid deposit and fertility, highlighting a comprehensive mechanism by which genetic variations shape phenotypic diversity. We carefully scrutinized the complicated propagation of selective genes to transcriptional alterations, elucidating a tight affinity in a regulatory network pattern and a specific regulation of alternative splicing underlying domestication and artificial selection, in spite of partially direct guidance. Through a systematic survey of the selective genes across five domesticated species, we recapitulated a comprehensive mechanism combining convergent evolution and complex genetic regulatory network underlying convergent behavior modification across species. This study systematically traced the genomic and transcriptomic dynamics and functional changing patterns underlying chicken domestication and selection, provided promising insight into the putative genetic architectures of complex traits and system-wide evidence for the propagation of selective sweeps on the transcriptomes. As well, our analyses provided valuable theories to the mechanism of domesticated phenotypes underlying convergent evolution across different species.