An investigation of Y chromosome incorporations in 400 species of Drosophila and related genera

Abstract

Y chromosomes are widely believed to evolve from a normal autosome through a process of massive gene loss (with preservation of some male genes), shaped by sex-antagonistic selection and complemented by occasional gains of male-related genes. The net result of these processes is a male-specialized chromosome. This might be expected to be an irreversible process, but it was found in 2005 that the Drosophila pseudoobscura Y chromosome was incorporated into an autosome. Y chromosome incorporations have important consequences: a formerly male-restricted chromosome reverts to autosomal inheritance, and the species may shift from an XY/XX to X0/XX sex-chromosome system. In order to assess the frequency and causes of this phenomenon we searched for Y chromosome incorporations in 400 species from Drosophila and related genera. We found one additional large scale event of Y chromosome incorporation, affecting the whole montium subgroup (40 species in our sample); overall 13% of the sampled species (52/400) have Y incorporations. While previous data indicated that after the Y incorporation the ancestral Y disappeared as a free chromosome, the much larger data set analyzed here indicates that a copy of the Y survived as a free chromosome both in montium and pseudoobscura species, and that the current Y of the pseudoobscura lineage results from a fusion between this free Y and the neoY. The 400 species sample also showed that the previously suggested causal connection between X-autosome fusions and Y incorporations is, at best, weak: the new case of Y incorporation ( montium) does not have X-autosome fusion, whereas nine independent cases of X-autosome fusions were not followed by Y incorporations. Y incorporation is an underappreciated mechanism affecting Y chromosome evolution; our results show that at least in Drosophila it plays a relevant role and highlight the need of similar studies in other groups.

Author summary

In contrast to other chromosomes (X and autosomes), which are present in males and females, Y chromosomes spend all time in males. Hence it is not surprising that along evolution they became male specialized, e. g., containing a disproportionate amount of male-fertility genes. Interestingly it was found in 2005 that in Drosophila pseudoobscura the Y chromosome reverted to "male-female existence", being incorporated into an autosome. These "Y chromosome incorporations" have important consequences on sex-chromosome evolution, and allow the study of the evolutionary forces that shaped Y chromosomes as they act backwards. As D. pseudoobscura was the second Drosophila species investigated in this respect, it is likely that other cases exist, and that perhaps it is a common phenomenon. In order to answer this question we studied 400 Drosophila species. We found one additional case of Y incorporation, which occurred in the ancestor of Drosophila montium, and currently affects a large number of species; overall 13% of the species we sampled (52/400) have Y incorporations. We also found that a previously suggested cause of Y incorporations (X-autosome fusions) is not a general explanation. Our results show that in Drosophila Y incorporations play a relevant role and highlight the need of similar studies in other groups.