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Emergence of sex-specific transcriptomes in a sexually-dimorphic brain nucleus

ABSTRACT: Sexual dimorphisms in the brain give rise to sex differences in physiology and behavior, yet we have limited understanding of the transcriptomic changes underlying their development. We evaluated developmental transcriptome dynamics for one of the most extreme neuroanatomical sexual dimorphisms in vertebrates - the songbird robust nucleus of the arcopallium (RA). RA is the telencephalic motor output nucleus of the song system. It grows monomorphically for the first few weeks posthatch, then continues growing in males but regresses in females, becoming 5-7 times larger in males. We quantified RA gene expression from monomorphic and dimorphic stages of development in both sexes. Mirroring the morphology, male and female transcriptomes initially resembled one other, then diverged markedly. Thousands of genes showed developmental regulation, corresponding to highly sex-specific biological processes. Males showed enrichments for neuronal growth and morphogenesis, synapse organization, metabolism, and voltage-gated ion channels. Females showed enrichments for cell polarity and differentiation, chemotaxis inhibition, gene silencing, and hormone and immune signaling. Notably, the majority of sex-biased genes in monomorphic RA were sex chromosome Z genes. These findings reveal a profound, sex-specific reorganization of RA’s transcriptome, providing novel insights into potential targets and drivers of sexually dimorphic neurodevelopment.

ORGANISM(S): Taeniopygia guttata

PROVIDER: GSE191296 | GEO | 2022/07/14

REPOSITORIES: GEO

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Project description:Stalk-eyed flies (family Diopsidae) are a model system for studying sexual selection due to the elongated and sexually dimorphic eye-stalks found in many species. These flies are of additional interest because their X chromosome is derived largely from an autosomal arm in other flies. To identify candidate genes required for development of dimorphic eyestalks and investigate how sex-biased expression arose on the novel X we compared gene expression between males and females using oligonucleotide microarrays and RNA from developing eyestalk tissue or adult heads in the dimorphic diopsid, Teleopsis dalmanni. Microarray analysis revealed sex-biased expression for 26% of 3,748 genes expressed in eye-antennal imaginal discs and concordant sex-biased expression for 86 genes in adult heads. Overall, 415 female-biased and 482 male-biased genes were associated with dimorphic eyestalk development but not differential expression in the adult head. Functional analysis revealed that male-biased genes are disproportionately associated with growth and mitochondrial function while female-biased genes are associated with cell differentiation and patterning or are novel transcripts. With regard to chromosomal effects, dosage compensation occurs by elevated expression of X-linked genes in males. Genes with female-biased expression were more common on the X and less common on autosomes than expected, while male-biased genes exhibited no chromosomal pattern. Rates of protein evolution were lower for female-biased genes but higher for genes that moved on or off the novel X chromosome. These findings cannot be due to meiotic sex chromosome inactivation or by constraints associated with dosage compensation. Instead, they could be consistent with sexual conflict in which female-biased genes on the novel X act primarily to reduce eyespan in females while other genes increase eyespan in both sexes. Additional information on sex-biased gene expression in other tissues and related sexually monomorphic species could confirm this interpretation.

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Emergence of sex-specific transcriptomes in a sexually-dimorphic brain nucleus

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