Sexual antagonism and sex determination in three syngnathid species alongside male pregnancy gradient and varying sex roles.

Abstract

The allocation of energy towards gamete production, parental care, mate choice, sex roles, and sexual dimorphism generates divergence in selection pressures between the sexes, leading to opposing fitness strategies and sexual antagonism (SA). Due to the shared genetic makeup, a single genomic locus can contain a gene or allele with differing fitness impacts on each sex. This intralocus sexual conflict can be resolved via intersex bias in gene expression and/or formation of sex-linked genomic regions, that may also regulate sex determination. Sex determination (SD) encompasses environmental SD (ESD), monogenic SD, and polygenic SD. Occasionally, shifts from one SD locus to another can occur. While the precise mechanisms driving these shifts are unknown, SA is believed to be a major contributor. To investigate the link between SA and SD, we selected three syngnathid species along the gradient of male pregnancy that evolved with different sex roles and intensities of sexual dimorphism. By looking at intersex genetic divergence (Fst) and sex-biased expression patterns, we uncovered that sex role and mate competition, rather than male pregnancy, primarily drive SA. Furthermore, we identified processes related to non-coding RNAs and biased allele expression as mediators of SA. Most notably, we discovered intraspecies sex chromosome polymorphism in Hippocampus erectus. Overall, we report important details on the interplay between SA and SD, and suggest that understanding SA and its resolution mechanisms is crucial for unraveling the evolution of SD in diverse species.