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How the birds obtain flight ability and other bird-specific traits like the feathers has long been a puzzle. A new study on avian-specific highly conserved elements (ASHCEs) was published in Nature Communications on February 6, 2017. This study was led by an international team including researchers from China National GeneBank, BGI, Tohoku University, Tokyo University，Kunming Institute of Zoology at Chinese Academy Sciences and other institutes. The study revealed the important roles of avian-specific conserved genomic sequences in shaping the bird specific features.
Birds are the most abundant class among the terrestrial vertebrates with more than 10,500 extant species and they are also the only existing descendants of dinosaurs. About 66 million years ago, around the period of Cretaceous-Paleogene extinction, birds evolved explosively and gave rise to a rich diversity of bird species in diverse environments on the earth. In spite of their large diversity, birds still maintain many lineage-specific developmental, behavioral and physiological traits during long-term macroevolution, such as beaks, light bone, feathers, and flight ability. Elucidating the genetic basis of these key innovations is a fundamental mission in evolutionary study.
Fig. 1 Characteristic of birds: the flight feathers develop at wings and tails. Figure edited from Koji Tamura.
In 2014, this research team have published a series of papers about the genomes for 48 bird species representing nearly all-extant orders of birds. In this study, researchers hypothesized that the avian-specific conserved genomic regions, which experienced very few changes since the emergence of early avian species, might contribute to the development of avian-specific traits. To identify the avian-specific highly conserved elements (named ASHCEs hereafter), researchers compared 48 avian genomes and 9 other vertebrate genomes (including reptiles, mammals, amphibians and fishes). They found about 11 Mb of ASHCEs, covering about 1% of the bird genome. Surprisingly, more than 99% of ASHCEs are in the non-coding regions of the genome. On the other hand, researchers found that a smaller number of new coding genes have evolved in bird lineages. Researchers concluded that the emergence of avian-specific traits during the macroevolutionary transitions was mainly due to the innovation of non-coding regions with gene expression regulation functions.
Fig. 2 There is almost no new coding gene in evolution of birds: by compared 48 avian genomes and 9 other animal genomes, avian specific conserved DNA sequences were almost all at non-coding genes (99.69%). Figure edited from Koji Tamura.
By investigating the chromatin states of ASHCEs in chicken embryos at different developmental stages, researchers found that the ASHCEs were significantly enriched with histone modifications, and some ASHCEs showed different histone modification patterns between different developmental stages, suggesting regulatory roles of these ASHCEs during development.
Fig. 3 Acquisition of new enhancers during avian evolution changed the gene activations: birds obtained the regulatory DNA sequences to alter gene expression.
By comparing gene expression patterns in the arms (wings) and legs of chicken, gecko and mouse embryos, the researchers identified ASHCE-associated genes that are unique to chicken limbs. The most interesting gene is Sim1, which was expressed only in chicken embryonic regions that develop flight feather, one of the most important avian-specific traits that enable birds’ flight. The researchers confirmed that birds have evolved with this unique expression pattern because the bird ancestors have obtained an ASHCE near Sim1 gene after splitting with other dinosaurs that could intrigue the specific expression pattern of this gene that was not observed in other vertebrate species.
Fig. 4 Gene activation by one of the avian enhancers: Sim1 gene is a conserved protein coding gene in avian and non-avian animals, which is involved in brain functions. But Sim1 gene with an avian specific enhancer can be activated in the forelimb of birds and involves in the development of flight feathers (first line figure); This Sim1 expression cannot be detected in other vertebrate species (mouse, second line figure); however, the expression in the forelimb can be driven by artificially introducing the enhancer into the mouse genome (third line figure). Reporter gene is often used as a marker for testing if a DNA sequence (here is Sim1 avian enhancer) can trigger the activity of the gene.
Fig. 5 Acquisition of Sim1 avian enhancer at dinosaur ages: the strong natural selection on Sim1 enhancer started at the time when the first ‘modern’ flight feathers appeared.
Researchers found that Sim1 gene was expressed not only in the forelimb but also in the tail, both of which develop with the long flight feathers. It is interesting that its expression could also be found in the leg of Cochin bantam, a special chicken breed which also develops flight feathers on its legs. These results suggest that Sim1 gene is involved in flight feather development, and this special role is mainly created by its associated ASHCE.
Guojie Zhang, the leader of B10K project and co-corresponding author of the paper, said in a statement: “It is intriguing that the birds have found its own way to maintain a simplified genome in adapt to the flying lifestyle, at the same time gain lots of lineage specific morphologies by modification on non-coding sequences that can change the expression level of their associated genes. Our study provided a rich candidate list of genes that might explain the development of bird unique features.”