Abstract
Diverse sex-chromosome systems are found in vertebrates, particularly in teleost fishes, where different systems can be found in closely related species. Several mechanisms have been proposed for the rapid turnover of sex chromosomes, including the transposition of an existing sex-determination gene, the appearance of a new sex-determination gene on an autosome, and fusions between sex chromosomes and autosomes. To better understand these evolutionary transitions, a detailed comparison of sex chromosomes between closely related species is essential. Here, we used genetic mapping and molecular cytogenetics to characterize the sex-chromosome systems of multiple stickleback species (Gasterosteidae). Previously, we demonstrated that male threespine stickleback fish (Gasterosteus aculeatus) have a heteromorphic XY pair corresponding to linkage group (LG) 19. In this study, we found that the ninespine stickleback (Pungitius pungitius) has a heteromorphic XY pair corresponding to LG12. In black-spotted stickleback (G. wheatlandi) males, one copy of LG12 has fused to the LG19-derived Y chromosome, giving rise to an X1X2Y sex-determination system. In contrast, neither LG12 nor LG19 is linked to sex in two other species: the brook stickleback (Culaea inconstans) and the fourspine stickleback (Apeltes quadracus). However, we confirmed the existence of a previously reported heteromorphic ZW sex-chromosome pair in the fourspine stickleback. The sex-chromosome diversity that we have uncovered in sticklebacks provides a rich comparative resource for understanding the mechanisms that underlie the rapid turnover of sex-chromosome systems.
Highlights
Genetic sex determination (GSD) is prevalent in vertebrates and is often accompanied by the presence of a heteromorphic chromosome pair in one sex
sexdetermination locus (SEX) Is Linked to Both LG12 and LG19 in G. wheatlandi Master sex-determination loci map to different Y chromosomes in G. aculeatus (LG19) and P. pungitius (LG12) [38,40]
The nomenclature for the P. pungitius linkage groups corresponds to the G. aculeatus nomenclature, and LG12 and LG19 represent distinct chromosomes in these two species [40]
Summary
Genetic sex determination (GSD) is prevalent in vertebrates and is often accompanied by the presence of a heteromorphic chromosome pair in one sex. Most mammals have an XY heteromorphic pair [2], and the male-limited Y sex chromosome bears SRY, a male-determining gene [3,4,5] that is found in all but a handful of mammals [6,7,8,9,10]. This broad conservation of sex-chromosome systems across large taxonomic groups is not universal in vertebrates. The only other known vertebrate sex-determining gene, DMY in the medaka fish Oryzias latipes [11,12], is not found in many closely related Oryzias species [13,14]
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