Key role of estrogen receptor β in the organization of brain and behavior of the Japanese quail

Court, Lucas; Vandries, Laura M.; Balthazart, Jacques; Cornil, Charlotte

doi:10.1016/j.yhbeh.2020.104827

Cited by 16 publications

(11 citation statements)

References 57 publications

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“…Yet, we found that the expression of SDR42E1 and aromatase genes were positively correlated in both Independents and Satellites, but not in Faeders. This result points to a putatively novel relationship between the inversion and estrogen synthesis, which is an exciting avenue for future research given the well-documented importance of estrogen in brain organization and courtship behavior in other birds (Steimer and Hutchison, 1980;Fusani et al, 2001;Gahr, 2001;Court et al, 2020). However, because both Satellites and Faeders share the deletion that is upstream from SDR42E1, identifying which sequence elements (i.e., mutations unique to the Satellite allele or shared between Independents and Satellites) can account for the Satellite and Faeder differences concerning SDR42E1 and aromatase co-expression will require further study.…”

Section: Morphs Can Be Discriminated Based On Expression Differences Of Multiple Genesmentioning

confidence: 85%

“…Remarkably, neither removal of HSD17B2 nor ESR2, the genes with heaviest positive and negative loadings, respectively, did fully abolish clustering of the three morph groups. ESR2 may be involved in encoding the behavioral differences between males, as a recent study showed that during embryological development the expression of ESR2, and not ESR1, mediates the organizational de-masculinization of the brain with permanent effects into adulthood in the Japanese quail (Coturnix japonica) (Court et al, 2020). When we sequentially removed genes according to their descending loadings, the separation of Faeders from Independents and Satellites persisted until we reached four genes: STAR, HSD17B3, HSD3B2, AROM (Supplementary Figures 3E-H).…”

Section: Morphs Can Be Discriminated Based On Expression Differences Of Multiple Genesmentioning

confidence: 99%

“…Steroid hormones often have widespread pleiotropic effects and modulate gene expression genome-wide across many different tissues (Beato, 1993). In addition, steroids such as testosterone and estrogen are extremely important for determining the sexual differentiation of the brain (Steimer and Hutchison, 1980;Balthazart and Ball, 1995;Court et al, 2020). These two hormones can have long-lasting organizational effects on brain development, which is an effective way to exert an entire morph-specific neural circuit by virtue of the delicate relationship between genetic sex, hormonal environment and genetic background.…”

Section: Introductionmentioning

confidence: 99%

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Gene Expression Modification by an Autosomal Inversion Associated With Three Male Mating Morphs

2021

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Chromosomal inversions are structural rearrangements that frequently provide genomic substrate for phenotypic diversity. In the ruff Philomachus pugnax, three distinct male reproductive morphs (Independents, Satellites and Faeders) are genetically determined by a 4.5 Mb autosomal inversion. Here we test how this stable inversion polymorphism affects gene expression in males during the lekking season. Gene expression may be altered through disruptions at the breakpoints and the accumulation of mutations due to suppressed recombination. We used quantitative PCR to measure expression of 11 candidate inversion genes across three different tissues (liver, adrenal glands and gonads) and tested for allelic imbalance in four inversion genes across 12 males of all three morphs (8 Independents, 2 Satellites, 2 Faeders). We quantified transcripts of CENPN, an essential gene disrupted by the inversion at the proximal breakpoint, at different exons distributed near and across the breakpoint region. Consistent with dosage dependent gene expression for the breakpoint gene CENPN, we found that expression in Independents was broadly similar for transcripts segments from inside and outside the inversion regions, whereas for Satellites and Faeders, transcript segments outside of the inversion showed at least twofold higher expression than those spanning over the breakpoint. Within the inversion, observed expression differences for inversion males across all four genes with allele-specific primers were consistent with allelic imbalance. We further analyzed gonadal expression of two inversion genes, HSD17B2 and SDR42E1, along with 12 non-inversion genes related to steroid metabolism and signaling in 25 males (13 Independents, 7 Satellites, 5 Faeders). Although we did not find clear morph differentiation for many individual genes, all three morphs could be separated based on gene expression differences when using linear discriminant analysis (LDA), regardless of genomic location (i.e., inside or outside of the inversion). This was robust to the removal of genes with the highest loadings. Pairwise correlations in the expression of genes showed significant correlations for 9–18 pairs of genes within morphs. However, between morphs, we only found a single association between genes SDR42E1 and AROM for Independents and Satellites. Our results suggest complex and wide-ranging changes in gene expression caused by structural variants.

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Section: Morphs Can Be Discriminated Based On Expression Differences Of Multiple Genesmentioning

confidence: 85%

Section: Morphs Can Be Discriminated Based On Expression Differences Of Multiple Genesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Gene Expression Modification by an Autosomal Inversion Associated With Three Male Mating Morphs

2021

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“…Moreover, ER paralogues show sex differences in expression levels and tissue specificity (Zhang et al, 2017). In quail, the administration of an agonist specific to ERβ on embryonic day 7 demasculinizes male sexual behaviour and midbrain nuclei characteristics in Japanese quails, whereas an agonist specific to ERα does not exert this effect (Court et al, 2020). The specific roles of each ER paralogue in the adult HVC of male and female songbirds warrant further investigation.…”

Section: Resultsmentioning

confidence: 99%

The gene expression profile of the song control nucleus HVC shows sex specificity, hormone responsiveness, and species specificity among songbirds

Frankl-Vilches

Bakker

et al. 2021

Preprint

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Singing occurs in songbirds of both sexes, but some species show typical degrees of sex-specific performance. We studied the transcriptional sex differences in the HVC, a brain nucleus critical for song pattern generation, of the forest weaver (Ploceus bicolor), the blue-capped cordon-bleu (Uraeginthus cyanocephalus), and the canary (Serinus canaria), which are species that show low, medium, and high levels of sex-specific singing, respectively. We observed persistent sex differences in gene expression levels regardless of the species-specific sexual singing phenotypes. We further studied the HVC transcriptomes of defined phenotypes of canary, known for its testosterone-sensitive seasonal singing. By studying both sexes of canaries during both breeding and nonbreeding seasons, nonbreeding canaries treated with testosterone, and spontaneously singing females, we found that the circulating androgen levels and sex were the predominant variables associated with the variations in the HVC transcriptomes. The comparison of natural singing with testosterone-induced singing in canaries of the same sex revealed considerable differences in the HVC transcriptomes. Strong transcriptional changes in the HVC were detected during the transition from nonsinging to singing in canaries of both sexes. Although the sex-specific genes of singing females shared little resemblance with those of males, our analysis showed potential functional convergences. Thus, male and female songbirds achieve comparable singing behaviours with sex-specific transcriptomes.

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“…day 7 demasculinises male sexual behaviour and midbrain nuclei characteristics in Japanese quails, whereas an agonist specific to ERα does not exert this effect (Court et al, 2020). The specific roles of each ER paralog in the adult HVC of male and female songbirds warrant further investigation.…”

Section: The Sex-specific Genes Show Functional Overlapmentioning

confidence: 96%

The Gene Expression Profile of the Song Control Nucleus HVC Shows Sex Specificity, Hormone Responsiveness, and Species Specificity Among Songbirds

Frankl-Vilches

Bakker

et al. 2021

Front. Neurosci.

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Singing occurs in songbirds of both sexes, but some species show typical degrees of sex-specific performance. We studied the transcriptional sex differences in the HVC, a brain nucleus critical for song pattern generation, of the forest weaver (Ploceus bicolor), the blue-capped cordon-bleu (Uraeginthus cyanocephalus), and the canary (Serinus canaria), which are species that show low, medium, and high levels of sex-specific singing, respectively. We observed persistent sex differences in gene expression levels regardless of the species-specific sexual singing phenotypes. We further studied the HVC transcriptomes of defined phenotypes of canary, known for its testosterone-sensitive seasonal singing. By studying both sexes of canaries during both breeding and non-breeding seasons, non-breeding canaries treated with testosterone, and spontaneously singing females, we found that the circulating androgen levels and sex were the predominant variables associated with the variations in the HVC transcriptomes. The comparison of natural singing with testosterone-induced singing in canaries of the same sex revealed considerable differences in the HVC transcriptomes. Strong transcriptional changes in the HVC were detected during the transition from non-singing to singing in canaries of both sexes. Although the sex-specific genes of singing females shared little resemblance with those of males, our analysis showed potential functional convergences. Thus, male and female songbirds achieve comparable singing behaviours with sex-specific transcriptomes.

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Key role of estrogen receptor β in the organization of brain and behavior of the Japanese quail

Cited by 16 publications

References 57 publications

Gene Expression Modification by an Autosomal Inversion Associated With Three Male Mating Morphs

Gene Expression Modification by an Autosomal Inversion Associated With Three Male Mating Morphs

The gene expression profile of the song control nucleus HVC shows sex specificity, hormone responsiveness, and species specificity among songbirds

The Gene Expression Profile of the Song Control Nucleus HVC Shows Sex Specificity, Hormone Responsiveness, and Species Specificity Among Songbirds

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