Independent evolution of sex chromosomes and male pregnancy-related genes in two seahorse species

Unlike birds and mammals, many teleosts have homomorphic sex chromosomes and changes in the chromosome carrying the sex-determining locus, termed “turnovers”, are common. Recent turnovers allow studies of several interesting questions. One question is whether the new sex-determining regions evolve to become completely non-recombining, and if so, how and why. Another is to test the prediction that evolutionary changes that benefit one sex will accumulate in the newly sex-linked region. To study these questions, we analyzed the genome sequences of two seahorse species of the Syngnathidae, a fish group in which many species evolved a unique structure, the male brood pouch. We find that both seahorse species have XY sex chromosome systems, and their sex chromosome pairs are not homologs, implying that at least one turnover event has occurred. The Y-linked regions respectively occupy 63.9% and 95.1% of the entire chromosome of the two species, and do not exhibit extensive sequence divergence with their X-linked homologs. We find evidence for occasional recombination between the extant sex chromosomes that may account for their homomorphic pattern. We argue that these Y-linked regions did not evolve by recombination suppression after the turnover. Instead, it can be explained by the ancestral nature of low crossover rate at the corresponding chromosome location. With such an ancestral crossover landscape, a turnover can instantly create an extensive Y-linked region. Finally, we investigate the adaptive evolution of male pouch related genes after they become Y-linked in the seahorse.