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Using the canary genome to decipher the evolution of hormone-sensitive gene regulation in seasonal singing birds.

Frankl-Vilches C, Kuhl H, Werber M, Klages S, Kerick M, Bakker A, de Oliveira EH, Reusch C, Capuano F, Vowinckel J, Leitner S, Ralser M, Timmermann B, Gahr M - Genome Biol. (2015)

Bottom Line: Testosterone-sensitive up-regulated gene networks of HVC of singing males concerned neuronal differentiation.The 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Neurobiology, Max Planck Institute for Ornithology, 82319, Seewiesen, Germany. frankl@orn.mpg.de.

ABSTRACT

Background: While 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.

Results: We 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.

Conclusions: The 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.

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Schematic of the song control system of songbirds and seasonal features of the canary song. (A) HVC and RA are essential nuclei of the descending motor pathway of the song system that controls song production. All interconnected areas are parts of loops that feed back to the song motor pathway. The androgen receptors (red dots) are expressed in both the HVC and RA of canaries, while only HVC contains estrogen receptors (green dots) among song areas. Both areas express the 5α-reductase gene (blue squares) but only HVC expresses aromatase (yellow squares). The entopallium (ENT; the bird visual cortex) expresses neither androgen or estrogen receptors nor androgen- or estrogen-producing enzymes and was used as a contrasting brain area [20-23] (this study). (B) Song features such as song length, the number of non-repeated syllables, the number of sexy syllables and the maximal repetition rate of syllables change seasonally while the syllable repertoire of canaries does not change between their breeding and non-breeding season. The abundance of song segments with high repetition rates is a sexually attractive song pattern in canaries. Plotted are the percent differences between the breeding males (control) producing high testosterone levels and the non-breeding males producing low testosterone levels (redrawn after [16]).
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Fig1: Schematic of the song control system of songbirds and seasonal features of the canary song. (A) HVC and RA are essential nuclei of the descending motor pathway of the song system that controls song production. All interconnected areas are parts of loops that feed back to the song motor pathway. The androgen receptors (red dots) are expressed in both the HVC and RA of canaries, while only HVC contains estrogen receptors (green dots) among song areas. Both areas express the 5α-reductase gene (blue squares) but only HVC expresses aromatase (yellow squares). The entopallium (ENT; the bird visual cortex) expresses neither androgen or estrogen receptors nor androgen- or estrogen-producing enzymes and was used as a contrasting brain area [20-23] (this study). (B) Song features such as song length, the number of non-repeated syllables, the number of sexy syllables and the maximal repetition rate of syllables change seasonally while the syllable repertoire of canaries does not change between their breeding and non-breeding season. The abundance of song segments with high repetition rates is a sexually attractive song pattern in canaries. Plotted are the percent differences between the breeding males (control) producing high testosterone levels and the non-breeding males producing low testosterone levels (redrawn after [16]).

Mentions: The prototypical songbird species for seasonal singing is the canary (Serinus canaria) [12,15,16], a Carduelid songbird that originates from the Canary islands and was domesticated in the last centuries for various purposes, including being bred to win song contests [17]. The song of male canaries is highly stereotyped and includes syllables repeated with high frequency in the spring breeding season (long-day) while the songs uttered during the autumnal non-breeding period (short-day) are variable and contain few high-speed segments (Figure 1B). In wild and domesticated canaries, testis size and testosterone production are seasonally modulated, with high levels restricted to the breeding season, during which males sing intensely [12,15,16], a correlation that is confirmed experimentally by castration and testosterone treatment [3]. Estrogens, brain-derived metabolites of testosterone, are known to be specifically 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].Figure 1


Using the canary genome to decipher the evolution of hormone-sensitive gene regulation in seasonal singing birds.

Frankl-Vilches C, Kuhl H, Werber M, Klages S, Kerick M, Bakker A, de Oliveira EH, Reusch C, Capuano F, Vowinckel J, Leitner S, Ralser M, Timmermann B, Gahr M - Genome Biol. (2015)

Schematic of the song control system of songbirds and seasonal features of the canary song. (A) HVC and RA are essential nuclei of the descending motor pathway of the song system that controls song production. All interconnected areas are parts of loops that feed back to the song motor pathway. The androgen receptors (red dots) are expressed in both the HVC and RA of canaries, while only HVC contains estrogen receptors (green dots) among song areas. Both areas express the 5α-reductase gene (blue squares) but only HVC expresses aromatase (yellow squares). The entopallium (ENT; the bird visual cortex) expresses neither androgen or estrogen receptors nor androgen- or estrogen-producing enzymes and was used as a contrasting brain area [20-23] (this study). (B) Song features such as song length, the number of non-repeated syllables, the number of sexy syllables and the maximal repetition rate of syllables change seasonally while the syllable repertoire of canaries does not change between their breeding and non-breeding season. The abundance of song segments with high repetition rates is a sexually attractive song pattern in canaries. Plotted are the percent differences between the breeding males (control) producing high testosterone levels and the non-breeding males producing low testosterone levels (redrawn after [16]).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4373106&req=5

Fig1: Schematic of the song control system of songbirds and seasonal features of the canary song. (A) HVC and RA are essential nuclei of the descending motor pathway of the song system that controls song production. All interconnected areas are parts of loops that feed back to the song motor pathway. The androgen receptors (red dots) are expressed in both the HVC and RA of canaries, while only HVC contains estrogen receptors (green dots) among song areas. Both areas express the 5α-reductase gene (blue squares) but only HVC expresses aromatase (yellow squares). The entopallium (ENT; the bird visual cortex) expresses neither androgen or estrogen receptors nor androgen- or estrogen-producing enzymes and was used as a contrasting brain area [20-23] (this study). (B) Song features such as song length, the number of non-repeated syllables, the number of sexy syllables and the maximal repetition rate of syllables change seasonally while the syllable repertoire of canaries does not change between their breeding and non-breeding season. The abundance of song segments with high repetition rates is a sexually attractive song pattern in canaries. Plotted are the percent differences between the breeding males (control) producing high testosterone levels and the non-breeding males producing low testosterone levels (redrawn after [16]).
Mentions: The prototypical songbird species for seasonal singing is the canary (Serinus canaria) [12,15,16], a Carduelid songbird that originates from the Canary islands and was domesticated in the last centuries for various purposes, including being bred to win song contests [17]. The song of male canaries is highly stereotyped and includes syllables repeated with high frequency in the spring breeding season (long-day) while the songs uttered during the autumnal non-breeding period (short-day) are variable and contain few high-speed segments (Figure 1B). In wild and domesticated canaries, testis size and testosterone production are seasonally modulated, with high levels restricted to the breeding season, during which males sing intensely [12,15,16], a correlation that is confirmed experimentally by castration and testosterone treatment [3]. Estrogens, brain-derived metabolites of testosterone, are known to be specifically 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].Figure 1

Bottom Line: Testosterone-sensitive up-regulated gene networks of HVC of singing males concerned neuronal differentiation.The 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Neurobiology, Max Planck Institute for Ornithology, 82319, Seewiesen, Germany. frankl@orn.mpg.de.

ABSTRACT

Background: While 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.

Results: We 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.

Conclusions: The 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.

Show MeSH
Related in: MedlinePlus