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"Songbird" is a popular song by British American rock band Fleetwood Mac. It first appeared on the album Rumours and was released as the B-side of the.
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In addition to evidence for developmental regulation, these reads show further splice forms, new exons and untranslated sequences Supplementary Figs 1 and 2. To address issues of large-scale genome structure and evolution, we compared the chromosomes of zebra finch and chicken using both sequence alignment and fluorescent in situ hybridization.
These analyses showed overall conservation of synteny and karyotype in the two species, although the rate of intrachromosomal rearrangement was high Supplementary Note 2. We were also surprised to see genes of the major histocompatibility complex MHC dispersed across several chromosomes in the zebra finch, in contrast to the syntenic organization of both chicken and human MHCs Supplementary Note 2. We assessed specific gene losses and expansions in the zebra finch lineage by constructing phylogenies of genes present in the last common ancestor of birds and mammals Supplementary Note 2 and Supplementary Fig.
Both the zebra finch and the chicken genome assemblies lack genes encoding vomeronasal receptors, casein milk proteins, salivary-associated proteins and enamel proteins—not surprisingly, as birds lack vomeronasal organs, mammary glands and teeth.
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Unexpectedly, both species lack the gene for the neuronal protein synapsin 1 SYN1 ; comparative analyses suggest that the loss of SYN1 and flanking genes probably occurred in an ancestor to modern birds, possibly within the dinosaur lineage Supplementary Note 2 , Supplementary Table 2 and Supplementary Fig. Both zebra finch and chicken have extensive repertoires of olfactory receptor-like sequences Supplementary Note 2 and Supplementary Fig. Compared to mammals, zebra finch has duplications of genes encoding several proteins with known neural functions, including growth hormone, Supplementary Fig.
Two large expansions of gene families expressed in the brain seem to have occurred in the zebra finch lineage after the split from mammals. One involves a family related to the PAK3 pactivated kinase gene. The second involves the PHF7 gene, which encodes a zinc-finger-containing transcriptional control protein. Humans only have a single PHF7 gene, but remarkably the gene has been duplicated independently, many times in both the zebra finch and chicken lineages to form species-specific clades of 17 and 18 genes, respectively Supplementary Fig.
In the zebra finch these genes are expressed in the brain Supplementary Note 2. An intriguing puzzle in avian genomics has been the evident lack of a chromosome-wide dosage compensation mechanism to balance the expression of genes on the Z sex chromosome, which is present in two copies in males but only one in females 22 , The zebra finch genome assembly, however, lacks an MHM sequence, and genes adjacent to the comparable MHM chromosomal position show no special cluster of dosage compensation Fig.
Thus, the putative MHM-mediated mechanism of restricted Z-chromosome dosage compensation is not common to all birds. Chromosomal sex differences in the brain could have a direct role in the sex differences so evident in zebra finch neuroanatomy and singing behaviour. PowerPoint slide.
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In mammals, as much as half of their genomes represent interspersed repeats derived from mobile elements, whereas the interspersed repeat content of the chicken genome is only 8. We find that the zebra finch genome also has a low overall interspersed repeat content 7. The zebra finch, however, has about three times as many retrovirus-derived long terminal repeat LTR element copies as the chicken, and a low copy number of short interspersed elements SINEs , which the chicken lacks altogether.
Figure 2 shows an example of an RNA that was identified in a microarray screening for genes specifically enriched in song control nuclei 26 and now seems to represent a long non-coding RNA ncRNA containing a CR1-like mobile element. These results indicate that further experiments investigating a possible role of mobile-element-derived repeated sequences in vocal communication are warranted. The diagram in b indicates areas shown in photomicrographs in c and d. Cb, cerebellum; Hp, hippocampus; Meso, mesopallium; Nido, nidopallium; Shelf, nidopallial shelf region; St, striatum.
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Scale bars, 0. A large portion of the genome is directly engaged by vocal communication. A recent study 27 defined distinct sets of RNAs in the auditory forebrain that respond in different ways to song playbacks during the process of song-specific habituation, a form of learning Indeed we find that miR, a conserved microRNA implicated in neurological function in other species 28 , is rapidly suppressed in response to song playbacks Fig.
We independently measured this effect by direct Illumina sequencing of small RNAs in the auditory forebrain, and also identified other known and new microRNAs, several of which also change in expression after song stimulation Supplementary Note 2. Error bars denote s. Within these segments we find conserved predicted binding sites for 11 different microRNAs, including five new microRNAs found by direct sequencing of small RNAs from the zebra finch forebrain Fig.
These findings indicate that this NR4A3 transcript element may function in both humans and songbirds to integrate many conserved microRNA regulatory pathways. The act of singing also alters gene expression in song control nuclei 29 , and we used the genome assembly to analyse the transcriptional control structure of this response.
Using oligonucleotide microarrays, we identified genes in which expression significantly changed as a result of singing. These were grouped by k -means clustering into 20 distinct expression profile clusters Fig. Gene regulatory sequences transcription-factor-binding sites were predicted across the genome using a new motif-scanning approach Supplementary Note 1 , and we observed significant correlation between changes in expression of transcription factor genes and their predicted targets Fig. Thus, the experience of singing and hearing song engages complex gene regulatory networks in the forebrain, altering the expression of microRNAs, transcription factor genes, and their targets, as well as of non-coding RNA elements that may integrate transcriptional and post-transcriptional control systems.
Learned vocal communication is crucial to the reproductive success of a songbird, and this behaviour evolved after divergence of the songbird lineage 5. Thus, it seems likely that genes involved in the neurobiology of vocal communication have been influenced by positive selection in songbirds. With this in mind, we examined the intersection of two sets of genes: 1 those that respond to song exposure in the auditory forebrain as discussed in the previous section; and 2 those that contain residues that seem to have been positively selected in the zebra finch lineage, as determined using phylogenetic analysis by maximum likelihood PAML Supplementary Note 4.
There are genes that are common to both lists. Of these, 49 are suppressed by song exposure Supplementary Table 7 , and 6 of these 49 are explicitly annotated for ion channel activity Table 2. Independent evidence has also demonstrated differential anatomical expression of ion channel genes in song control nuclei 26 , Ion channel genes have important roles in many aspects of behaviour, neurological function and disease This class of genes is highly likely to be linked to song behaviour and should be a major target for future functional studies.
Passerines represent one of the most successful and complex radiations of terrestrial animals 7. Here we present the first, to our knowledge, analysis of the genome of a passerine bird. The zebra finch was chosen because of its well-developed status as a model organism for a number of fields in biology, including neurobiology, ethology, ecology, biogeography and evolution.
In the zebra finch as in the chicken, we see a smaller, tighter genome compared to mammals, with a marked reduction of interspersed repeats. The zebra finch presents a picture of greater genomic plasticity than might have been expected from the chicken and other precedents, with a high degree of intrachromosomal rearrangements between the two avian species, gene copy number variations and transcribed mobile elements. Yet we also see an overall similarity to mammals in protein-coding gene content and core transcriptional control systems.
Our analysis suggests several channels through which evolution may have acted to produce the unique neurobiological properties of songbirds compared to the chicken and other animals. These include the management of sex chromosome gene expression, accelerated evolution of neuronal ion transport genes, gene duplications to produce new variants of PHF7 , PAK3 and other neurobiologically important genes, and a new arrangement of MHC genes.
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Most notably, our analyses suggest a large recruitment of the genome during vocal communication, including the extensive involvement of ncRNAs. It has been proposed that ncRNAs have a contributing role in enabling or driving the evolution of greater complexity in humans and other complex eukaryotes Seeing that learned vocal communication itself is a phenomenon that has emerged only in some of the most complex organisms, perhaps ncRNAs are a nexus of this phenomenon.
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Much work will be needed to establish the actual functional significance of many of these observations and to determine when they arose in avian evolution. This work can now be expedited with the recent development of a method for transgenesis in the zebra finch An important general lesson, however, is that dynamic and serendipitous aspects of the genome may have unexpected roles in the elaborate vocal communicative capabilities of songbirds. In all cases, codon frequencies were estimated from the nucleotide composition at each codon position F3X4 model.
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Clayton, D. Integrating genomes, brain and behavior in the study of songbirds. Nottebohm, F. New York Academy of Science, Doupe, A. Birdsong and human speech: common themes and mechanisms. Jarvis, E.
Learned birdsong and the neurobiology of human language. NY Acad. Hillier, L. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature , — Hackett, S. A phylogenomic study of birds reveals their evolutionary history. Science , — Zeigler, H. Behavioral Neurobiology of Bird Song Vol. Hahnloser, R. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature , 65—70 Mooney, R.
Neural mechanisms for learned birdsong. Konishi, M. Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Goldman, S. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain.
Natl Acad. USA 80 , — The road we travelled: discovery, choreography, and significance of brain replaceable neurons. London, S.