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Sex-biased gene expression across tissues reveals unexpected differentiation in the gills of the threespine stickleback

ABSTRACT: Sexual dimorphism can evolve through sex-specific regulation of the same gene set. However, sex chromosomes can also facilitate this by directly linking gene expression to sex. Moreover, heteromorphic sex chromosomes often exhibit different gene content, which contributes to sexual dimorphism. Understanding patterns of sex-biased gene expression across organisms is important for gaining insight about the evolution of sexual dimorphism and sex chromosomes. Moreover, studying gene expression in species with recently established sex chromosomes can help understand the evolutionary dynamics of gene loss and dosage compensation. The threespine stickleback is known for its strong sexual dimorphism, especially during the reproductive period. Sex is determined by a young XY sex chromosome pair with three non-recombining regions that have started to degenerate. Using the high multiplexing capability of 3′ QuantSeq to sequence the sex-biased transcriptome of liver, gills and brain, we provide the first characterization of sex-specific transcriptomes from ~80 stickleback (40 males and 40 females) collected from a natural population during the reproductive period. We find that the liver is extremely differentiated (36% of autosomal genes) and reflects ongoing reproduction, while the brain shows very low levels of differentiation (0.78%) with no particular functional enrichment. Finally, the gills exhibit high levels of differentiation (5%), suggesting that sex should be considered in physiological and ecotoxicological studies of gill responses in fishes. We also find that sex-biased gene expression in X-linked genes is mainly driven by a lack of dosage compensation. However, sex-biased expression of genes that have conserved copies on both sex chromosomes is likely driven by the degeneration of Y allele expression and a down-regulation of male-beneficial mutations on the X chromosome.

ORGANISM(S): Gasterosteus aculeatus

PROVIDER: GSE269432 | GEO | 2024/06/09

REPOSITORIES: GEO

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Project description:Background: Stalk-eyed flies (family Diopsidae) are a model system for studying sexual selection due to the presence of elongated and sexually dimorphic eye-stalks in many species. Recent genomic studies on these flies have revealed a neo-X chromosome and evidence of gene movement onto or off of this X chromosome. To determine if sex linkage and gene movement are related to sexual dimorphism and sexual conflict, we compared gene expression between males and females using oligonucleotide microarrays and RNA from either developing eyestalk tissue or adult heads from a dimorphic species, Teleopsis dalmanni, or from developing eyestalk tissue in a congeneric monomorphic species, T. quinqueguttata. Results: Comparison of gene expression between the sexes for 3,748 genes indicates that dosage compensation is present due to elevated expression of X-linked genes in males. However, sex-biased expression was detected in 26% of the genes present in eye-antennal imaginal discs of larval T. dalmanni. Functional annotation reveals that female-biased genes are associated with transcription, anatomical development and cell communication in the nucleus, while male-biased genes are associated with metabolism and the mitochondria. Comparison of gene expression between experiments identified 140 genes with concordant sex-biased expression in the larval and adult tissues of T. dalmanni and 17 genes with identical sex-biased expression between species. There were only five reversals of sex-biased expression across experiments. In T. dalmanni, male-biased genes are more common on autosomes than on the X while female-biased genes are more common on the X in T. quinqueguttata. Female-biased expression is especially common among genes that moved onto the ancestral X while male-biased expression is more common among genes that moved onto an autosome. Conclusions: Genes with sex-biased expression exhibit different functions in each sex as expected if sexual conflict has influenced their evolution. The strong relationship between sex-biased expression and gene movement found in this study is consistent with resolution of sexual conflict by an RNA- or DNA-mediated process that moves genes between chromosomes. Measurement of gene expression in additional species should provide a more complete picture of how gene expression change occurs over evolutionary time in these extraordinary flies. Two-condition experiment, female vs. male RNA using larval eye discs for two species (Teleopsis dalmanni, Teleopsis quinqueguttata), and adult heads for one species (Teleopsis dalmanni).

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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Sex-biased gene expression across tissues reveals unexpected differentiation in the gills of the threespine stickleback

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