Abstract

BackgroundWhile the song of all songbirds is controlled by the same neural circuit, the hormone dependence of singing behavior varies greatly between species. For this reason, songbirds are ideal organisms to study ultimate and proximate mechanisms of hormone-dependent behavior and neuronal plasticity.ResultsWe present the high quality assembly and annotation of a female 1.2-Gbp canary genome. Whole genome alignments between the canary and 13 genomes throughout the bird taxa show a much-conserved synteny, whereas at the single-base resolution there are considerable species differences. These differences impact small sequence motifs like transcription factor binding sites such as estrogen response elements and androgen response elements. To relate these species-specific response elements to the hormone-sensitivity of the canary singing behavior, we identify seasonal testosterone-sensitive transcriptomes of major song-related brain regions, HVC and RA, and find the seasonal gene networks related to neuronal differentiation only in the HVC. Testosterone-sensitive up-regulated gene networks of HVC of singing males concerned neuronal differentiation. Among the testosterone-regulated genes of canary HVC, 20% lack estrogen response elements and 4 to 8% lack androgen response elements in orthologous promoters in the zebra finch.ConclusionsThe canary genome sequence and complementary expression analysis reveal intra-regional evolutionary changes in a multi-regional neural circuit controlling seasonal singing behavior and identify gene evolution related to the hormone-sensitivity of this seasonal singing behavior. Such genes that are testosterone- and estrogen-sensitive specifically in the canary and that are involved in rewiring of neurons might be crucial for seasonal re-differentiation of HVC underlying seasonal song patterning.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-014-0578-9) contains supplementary material, which is available to authorized users.

Highlights

  • While the song of all songbirds is controlled by the same neural circuit, the hormone dependence of singing behavior varies greatly between species

  • We assembled a high quality 1.2 Gbp draft genome of the canary using a combination of short read and long read sequencing technologies

  • The use of collinearity as a bioinformatics tool shows that bird genome assemblies with chromosomal sized scaffolds are possible without the application of other mapping technologies

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Summary

Introduction

While the song of all songbirds is controlled by the same neural circuit, the hormone dependence of singing behavior varies greatly between species. Songbirds are a large taxonomic group with a large degree of species variation to the extent that song-related behaviour depends on gonadal hormones, especially testosterone and estrogens [2,3,4,5,6,7,8,9,10,11]. Estrogens, brainderived metabolites of testosterone, are known to be involved in the production of the canary song segments uttered with high repetition rates [18], which represent a key feature of the sexual attractiveness of songs for female canaries [19]

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