Genome-wide analysis reveals molecular convergence underlying domestication in 7 bird and mammals.

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. 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. 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.

Hou Y ，Qi F ，Bai X ，Ren T ，Shen X ，Chu Q ，Zhang X ，Lu X ... -  《BMC GENOMICS》

Positive selection rather than relaxation of functional constraint drives the evolution of vision during chicken domestication.

As noted by Darwin, chickens have the greatest phenotypic diversity of all birds, but an interesting evolutionary difference between domestic chickens and their wild ancestor, the Red Junglefowl, is their comparatively weaker vision. Existing theories suggest that diminished visual prowess among domestic chickens reflect changes driven by the relaxation of functional constraints on vision, but the evidence identifying the underlying genetic mechanisms responsible for this change has not been definitively characterized. Here, a genome-wide analysis of the domestic chicken and Red Junglefowl genomes showed significant enrichment for positively selected genes involved in the development of vision. There were significant differences between domestic chickens and their wild ancestors regarding the level of mRNA expression for these genes in the retina. Numerous additional genes involved in the development of vision also showed significant differences in mRNA expression between domestic chickens and their wild ancestors, particularly for genes associated with phototransduction and photoreceptor development, such as RHO (rhodopsin), GUCA1A, PDE6B and NR2E3. Finally, we characterized the potential role of the VIT gene in vision, which experienced positive selection and downregulated expression in the retina of the village chicken. Overall, our results suggest that positive selection, rather than relaxation of purifying selection, contributed to the evolution of vision in domestic chickens. The progenitors of domestic chickens harboring weaker vision may have showed a reduced fear response and vigilance, making them easier to be unconsciously selected and/or domesticated.

Wang MS ，Zhang RW ，Su LY ，Li Y ，Peng MS ，Liu HQ ，Zeng L ，Irwin DM ，Du JL ，Yao YG ，Wu DD ，Zhang YP ... -  《-》

Large-scale genomic analysis reveals the genetic cost of chicken domestication.

Species domestication is generally characterized by the exploitation of high-impact mutations through processes that involve complex shifting demographics of domesticated species. These include not only inbreeding and artificial selection that may lead to the emergence of evolutionary bottlenecks, but also post-divergence gene flow and introgression. Although domestication potentially affects the occurrence of both desired and undesired mutations, the way wild relatives of domesticated species evolve and how expensive the genetic cost underlying domestication is remain poorly understood. Here, we investigated the demographic history and genetic load of chicken domestication. We analyzed a dataset comprising over 800 whole genomes from both indigenous chickens and wild jungle fowls. We show that despite having a higher genetic diversity than their wild counterparts (average π, 0.00326 vs. 0.00316), the red jungle fowls, the present-day domestic chickens experienced a dramatic population size decline during their early domestication. Our analyses suggest that the concomitant bottleneck induced 2.95% more deleterious mutations across chicken genomes compared with red jungle fowls, supporting the "cost of domestication" hypothesis. Particularly, we find that 62.4% of deleterious SNPs in domestic chickens are maintained in heterozygous states and masked as recessive alleles, challenging the power of modern breeding programs to effectively eliminate these genetic loads. Finally, we suggest that positive selection decreases the incidence but increases the frequency of deleterious SNPs in domestic chicken genomes. This study reveals a new landscape of demographic history and genomic changes associated with chicken domestication and provides insight into the evolutionary genomic profiles of domesticated animals managed under modern human selection.

Wang MS ，Zhang JJ ，Guo X ，Li M ，Meyer R ，Ashari H ，Zheng ZQ ，Wang S ，Peng MS ，Jiang Y ，Thakur M ，Suwannapoom C ，Esmailizadeh A ，Hirimuthugoda NY ，Zein MSA ，Kusza S ，Kharrati-Koopaee H ，Zeng L ，Wang YM ，Yin TT ，Yang MM ，Li ML ，Lu XM ，Lasagna E ，Ceccobelli S ，Gunwardana HGTN ，Senasig TM ，Feng SH ，Zhang H ，Bhuiyan AKFH ，Khan MS ，Silva GLLP ，Thuy LT ，Mwai OA ，Ibrahim MNM ，Zhang G ，Qu KX ，Hanotte O ，Shapiro B ，Bosse M ，Wu DD ，Han JL ，Zhang YP ... -  《BMC BIOLOGY》

Gastrocnemius transcriptome analysis reveals domestication induced gene expression changes between wild and domestic chickens.

Artificial selection of chicken for human-preferred traits has manifested great phenotypic differences between wild and domestic chickens. Study on the formation of these phenotypic variations will contribute to comprehensive understanding of the molecular mechanism of animal domestication. We used three kinds of chicken breeds for transcriptome analysis, including the red jungle fowl which was the wild ancestor of chickens, and two other domestic breeds, the chahua chicken and the avian broiler. More than 12,000 genes' expression levels were compared between different chicken breeds, and hundreds of genes displayed differential expression levels compared with wild chicken. Gene ontology analysis showed that differentially expressed genes in domestic chickens tended to be enriched in extracellular matrix, DNA binding and immune system development, etc. Some genes with important biological functions were differentially expressed in the domestic chickens, including titin, myostatin ubiquitin related genes, and transforming growth factor-beta receptor III, indicating possible selection pressures on these genes.

Li Q ，Wang N ，Du Z ，Hu X ，Chen L ，Fei J ，Wang Y ，Li N ... -  《-》

Annotating long intergenic non-coding RNAs under artificial selection during chicken domestication.

Numerous biological functions of long intergenic non-coding RNAs (lincRNAs) have been identified. However, the contribution of lincRNAs to the domestication process has remained elusive. Following domestication from their wild ancestors, animals display substantial changes in many phenotypic traits. Therefore, it is possible that diverse molecular drivers play important roles in this process. We analyzed 821 transcriptomes in this study and annotated 4754 lincRNA genes in the chicken genome. Our population genomic analysis indicates that 419 lincRNAs potentially evolved during artificial selection related to the domestication of chicken, while a comparative transcriptomic analysis identified 68 lincRNAs that were differentially expressed under different conditions. We also found 47 lincRNAs linked to special phenotypes. Our study provides a comprehensive view of the genome-wide landscape of lincRNAs in chicken. This will promote a better understanding of the roles of lincRNAs in domestication, and the genetic mechanisms associated with the artificial selection of domestic animals.

Wang YM ，Xu HB ，Wang MS ，Otecko NO ，Ye LQ ，Wu DD ，Zhang YP ... -  《BMC EVOLUTIONARY BIOLOGY》