Sex-biased gene expression across tissues reveals unexpected differentiation in the gills of the threespine stickleback
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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, differences in gene content between heteromorphic sex chromosomes contribute to sexual dimorphism. Understanding patterns of sex-biased gene expression across organisms is important for gaining insight into 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 three-spined stickleback is known for its strong sexual dimorphism, especially during the reproductive period. Sex is determined by a young XY sex chromosome pair with a non-recombining region divided into three strata, which have started to degenerate. Using the high multiplexing capability of 3′ QuantSeq to sequence the sex-biased transcriptome of the liver, gills, and brain, we provide the first characterization of sex-specific transcriptomes from ~80 sticklebacks (40 males and 40 females) collected from a natural population during the reproductive period. We find that the liver is extremely differentiated between sexes (36% of autosomal genes) and reflects ongoing reproduction, while the brain shows very low levels of differentiation (0.78%) with no 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 hemizygous 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.
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There is a heavy body of literature on sex-biased gene expression, which can easily be tricky. One reason is that expression data are multi-dimensional, notoriously noisy, and highly sensitive to experimental conditions. Achieving reproducibility is, therefore, a challenge, especially in non-model organisms. Another reason is that the evolutionary forces shaping gene expression variation are complex, involving processes such as intra- and inter-locus conflicts between sexes, sex-chromosome evolution and degeneration, dosage compensation, cis vs. trans regulation, dominance, linkage, drift, etc... Not surprisingly, the field is rich in discordant studies, and a wide variety of situations have been described.
The three-spined stickleback is a good illustration. This widely-studied fish displays conspicuous sexual dimorphisms, both …
There is a heavy body of literature on sex-biased gene expression, which can easily be tricky. One reason is that expression data are multi-dimensional, notoriously noisy, and highly sensitive to experimental conditions. Achieving reproducibility is, therefore, a challenge, especially in non-model organisms. Another reason is that the evolutionary forces shaping gene expression variation are complex, involving processes such as intra- and inter-locus conflicts between sexes, sex-chromosome evolution and degeneration, dosage compensation, cis vs. trans regulation, dominance, linkage, drift, etc... Not surprisingly, the field is rich in discordant studies, and a wide variety of situations have been described.
The three-spined stickleback is a good illustration. This widely-studied fish displays conspicuous sexual dimorphisms, both morphological and behavioural. Yet, the existing literature regarding which genes and tissues are involved is remarkably unclear due to the lack of a comprehensive data set. Sylvestre et al. (1) here fix this issue. They sampled 40 wild-caught individuals in each of the two sexes and performed high-throughput sequencing of the transcriptome in three somatic tissues, dissected and preserved in the exact same conditions. This is an impressive effort, well above current standards. Data analysis delivered a series of neat results: gene expression in the liver is particularly sex-biased; the brain, in contrast, is remarkably little sex-differentiated despite the presence of courtship and paternal care in this species; gills show significantly sex-biased gene expression, which had been unnoticed previously despite the importance of this organ in fish ecotoxicology; the relatively young sex-chromosomes, finally, do not seem to experience dosage compensation, and are therefore enriched in sex-biased genes.
Some of these results are consistent with previous studies in other fish species (2), here confirmed or demonstrated with a high degree of certainty. Others are new and worth considering in future studies of stickleback ecology and reproduction. We simply need more studies of this sort: well-conducted and clear-cut, recalling the career of its last author.
References
(1) Florent Sylvestre, Nadia Aubin-Horth, Louis Bernatchez (2024) Sex-biased gene expression across tissues reveals unexpected differentiation in the gills of the threespine stickleback. bioRxiv, ver.2 peer-reviewed and recommended by PCI Evol Biol https://doi.org/10.1101/2024.06.09.597944
(2) Iulia Darolti I, Judith E. Mank (2023). Sex-biased gene expression at single-cell resolution: cause and consequence of sexual dimorphism. Evolution Letters 7(3):148-156. https://doi.org/10.1093/evlett/qrad013
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