Navigating sex and sex roles: deciphering sex-biased gene expression in a species with sex-role reversal (Syngnathus typhle)

Abstract

Sex-specific lifespan dimorphism is observed in many species, with females often outliving males. This is thought to be due to sex-specific and unequal resource allocation between reproduction and maintenance. However, most studies on ageing focus on animals with traditional sex roles, where females have the highest energy burden with both egg production and parental care. This leaves a gap in our understanding of how resource allocation and senescence are linked in species with non-traditional roles. To address this, we investigated the relationship between sex (biological) and sex role (behavioural) on resource allocation trade-offs in somatic maintenance in the broad-nosed pipefish Syngnathus typhle. This species is sex-role reversed, with males acting as the primary caretaker for offspring through their unique male pregnancy, providing the opportunity to decouple the roles of sex and sex role in resource allocation. Our results suggest that while some gene groups are influenced by sex roles (e.g., genome maintenance and immune defence), others depend on biological sex and hormones (e.g., energy and fat storage), with differences becoming more pronounced with age. These findings challenge traditional ageing theories and improve our understanding of how sex-specific differences in ageing are shaped.

Sexual selection on non-ornamental traits is underpinned by evidence of genetic constraints on sex-biased expression in dusky pipefish

“…We found that the gonads especially, but livers as well, displayed sex-biased patterns of expression, and the genes that were sex-biased in one organ were generally not sex-biased in the others. In the gills, which do not serve a reproductive function, we observed only a small number of differentially expressed genes, but those that were differentially expressed generally were related to immunity, similar to other pipefishes (Dubin et al, 2023;Pappert et al, 2023). Genes that had the largest bias in expression while still being expressed in both sexes also tended to be tissue specific in their expression patterns, suggesting that sex-biased expression might more readily evolve in genes with fewer pleiotropic constraints.…”

“…Several sex-specific genes reinforce this pattern of sex differences in immune function in the gill, such as vascular cell adhesion protein 1 and galactose-specific lectin nattectin, which are male-specific in both gonads and gills and have been shown in zebrafish and multiple finfish to be related to immune responses (Elumalai et al, 2019;Hsieh et al, 2018). Differences in immune function between males and females have previously been demonstrated in pipefish (Dubin et al, 2023;Pappert et al, 2023;Roth et al, 2011), and the male-specific patterns of expression we observed could support the hypothesis the pregnant male pipefish experience different selection pressures with regard to immunity compared to female and non-pregnant pipefish (J. Parker et al, 2023;Roth et al, 2020).…”

Navigating sex and sex roles: deciphering sex-biased gene expression in a species with sex-role reversal ( Syngnathus typhle )

“…Data accessibility. Supplemental information include additional figures (electronic supplementary material, figures S1, S2), morphology measurements (electronic supplementary material, table S1), the significant differentially expressed genes (electronic supplementary material, tables S2, S3), the gene set enrichment analysis results as tables (electronic supplementary material, table S4) and information on quality and quantity of RNA for RNA-Seq (electronic supplementary material, table S5) [97]. The raw sequencing data and metadata used in this study is available from the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) under BioProject ID PRJNA943164 with submission ID SUB12940929.…”