Abstract
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.
Highlights
Most of the genomes of male and female individuals of the same species are the same but stark sex differences in physiological, phenotypical, or behavioural traits between the sexes are common and widespread in the animal kingdom
Canaries seldom sing (Shoemaker, 1939; Herrick and Harris, 1957; Pesch and Güttinger, 1985; Vallet et al, 1996; Hartley et al, 1997; Ko et al, 2020). Such substantial sex differences in singing behaviour are commonly found in the majority of northern temperate songbird species, even though females of many tropical and southern temperate species sing regularly, and their songs play an important role in inter-sexual communication (Slater and Mann, 2004; Price et al, 2009; Hall et al, 2015; Price, 2019)
We quantified the total mRNA from the HVC of male and female birds belonging to three songbird species during the breeding season (Table 1)
Summary
Most of the genomes of male and female individuals of the same species are the same but stark sex differences in physiological, phenotypical, or behavioural traits between the sexes are common and widespread in the animal kingdom. The extent of sex differences in singing behaviour varies greatly in the songbird clade (Ball, 2016), the song quality and occurrence in males and females of many songbird species are dependent on testosterone (Nottebohm et al, 1987; Leitner et al, 2001b; Fusani et al, 2003; Voigt and Leitner, 2008; Dittrich et al, 2014; Ko et al, 2020). An intrinsic limit to the alterations induced by testosterone appears to exist, and this limit prevents female songbirds from reaching the same levels of “maleness” in terms of song characteristics and HVC anatomy How are such sex-specific differences in singing and HVC anatomy achieved in different species? Our results indicate that the extent of sex-biased gene expression is context-dependent, it is persistent regardless of hormonal manipulation, behavioural phenotypes, and distinct genetic backgrounds
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