Abstract

BackgroundSongbirds (oscine Passeriformes) are among the most diverse and successful vertebrate groups, comprising almost half of all known bird species. Identifying the genomic innovations that might be associated with this success, as well as with characteristic songbird traits such as vocal learning and the brain circuits that underlie this behavior, has proven difficult, in part due to the small number of avian genomes available until recently. Here we performed a comparative analysis of 48 avian genomes to identify genomic features that are unique to songbirds, as well as an initial assessment of function by investigating their tissue distribution and predicted protein domain structure.ResultsUsing BLAT alignments and gene synteny analysis, we curated a large set of Ensembl gene models that were annotated as novel or duplicated in the most commonly studied songbird, the Zebra finch (Taeniopygia guttata), and then extended this analysis to 47 additional avian and 4 non-avian genomes. We identified 10 novel genes uniquely present in songbird genomes. A refined map of chromosomal synteny disruptions in the Zebra finch genome revealed that the majority of these novel genes localized to regions of genomic instability associated with apparent chromosomal breakpoints. Analyses of in situ hybridization and RNA-seq data revealed that a subset of songbird-unique genes is expressed in the brain and/or other tissues, and that 2 of these (YTHDC2L1 and TMRA) are highly differentially expressed in vocal learning-associated nuclei relative to the rest of the brain.ConclusionsOur study reveals novel genes unique to songbirds, including some that may subserve their unique vocal control system, substantially improves the quality of Zebra finch genome annotations, and contributes to a better understanding of how genomic features may have evolved in conjunction with the emergence of the songbird lineage.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-1082) contains supplementary material, which is available to authorized users.

Highlights

  • IntroductionSongbirds (oscine Passeriformes) are among the most diverse and successful vertebrate groups, comprising almost half of all known bird species

  • Songbirds are among the most diverse and successful vertebrate groups, comprising almost half of all known bird species

  • We show that some of these genes are expressed in the brain, and that a small subset are differentially expressed in song nuclei relative to surrounding areas, representing molecular specializations of the songbird vocal control system; others are expressed in various non-neural tissues

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Summary

Introduction

Songbirds (oscine Passeriformes) are among the most diverse and successful vertebrate groups, comprising almost half of all known bird species. Identifying the genomic innovations that might be associated with this success, as well as with characteristic songbird traits such as vocal learning and the brain circuits that underlie this behavior, has proven difficult, in part due to the small number of avian genomes available until recently. We performed a comparative analysis of 48 avian genomes to identify genomic features that are unique to songbirds, as well as an initial assessment of function by investigating their tissue distribution and predicted protein domain structure. The vast majority of these are oscine passerines, or songbirds (suborder: Passeri), with far fewer species of suboscines (suborder: Tyranni) and just 2 extant species of basal New Zealand wrens (suborder: Acanthisitti) (Figure 1A). Unique to songbirds is the complex syringeal morphology and underlying brain A.

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