Turnover of Sex Chromosomes in the Stickleback Fishes (Gasterosteidae)

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.

Genetic interactions controlling sex and color establish the potential for sexual conflict in Lake Malawi cichlid fishes

“…In theory, it is possible that new and old sex-determining loci might remain polymorphic within and between populations, providing standing variation for interacting sex-determining systems (Wilkins, 1995;Kirkpatrick, 2007, 2010). The evolutionary dynamics of sex systems as a result of sexually antagonistic selection has been suggested as important for the high speciation rates of some fishes (Seehausen et al, 1999a;Lande et al, 2001;Kocher, 2004;Ross et al, 2009), including the cichlids of Lake Malawi (LM), East Africa.…”

No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution

“…This apparent association between the function of sex determination and suppression of recombination has led to the suggestion that restricted recombination in sex chromosomes evolves due to selection to resolve sexually antagonistic genetic interactions [2,[9][10][11]. This sexual antagonism hypothesis has assumed the status of conventional wisdom, to the extent that, in many recent publications, sexual antagonism is the only hypothesis suggested to account for restricted recombination in sex chromosomes [1,6,[12][13][14][15][16][17][18][19][20][21][22]. However, empirical support for the sexual antagonism hypothesis is equivocal [1].…”

Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena

“…Different sex chromosomes have been observed even in closely related fish species 29 , but most strikingly in the Oryzias fishes [30][31][32][33][34] . They show both XY and ZW systems, and their sexdetermining loci are located on different chromosomes, suggesting that these mechanisms are regulated by different genes and have evolved rapidly.…”