Sexual Antagonism and Sex Determination in Three Syngnathid Species Alongside a Male Pregnancy Gradient

The allocation of energy toward gamete production, parental care, mate choice, and secondary sexual signals fosters divergence in selection between the sexes, giving rise to opposing fitness strategies and sexual antagonism. The shared genetic makeup results in single genomic loci that harbor a gene or variant with varying fitness impacts on each sex. The resolution of this intralocus sexual conflict relies on intersex bias in gene expression and/or the formation of sex-linked genomic regions, which may also play a role in regulating sex determination. Shifts in the sex determination locus may happen. While the precise mechanisms driving these shifts are unknown, sexual antagonism was long believed to be a major contributor. To investigate the link between sexual antagonism and sex determination, we selected three syngnathid species along the gradient of their unique male pregnancy that evolved with different intensities of precopulatory sexual selection, i.e. sex-specific roles in mate choice. Examining intersex genetic divergence (Fst) and patterns of sex-biased expression, we revealed that precopulatory sexual selection and male pregnancy, rather than male pregnancy alone, are the primary drivers of sexual antagonism. In addition, we identified processes involving noncoding RNAs and biased variant expression as mediators of sexual antagonism. Notably, we discovered an intraspecies sex chromosome polymorphism in the seahorse Hippocampus erectus. The polymorphism may have resulted from generations of captive breeding or represents a natural polymorphism in wild populations. Our findings suggest that sexual antagonism resolution mechanisms can directly shape sex determination evolution across species, providing key insights into the molecular pathways underlying reproductive adaptation and diversification.