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.

Complex evolutionary history of the Y chromosome in flies of theDrosophila obscuraspecies group

“…If not on the dot chromosome, where are ancestral Y genes found in affinis flies? Consistent with our coverage analysis and PCR results [28], we find kl--3 and Ppr--Y to be contained in both of our female assemblies of EA and EB D. athabasca, but not Ary, kl--2 and Ory. Surprisingly, however, both of these genes are located on Muller B, in different chromosomal locations (Figure 4, Supplemental Table 1).…”

“…Thus, unlike the Y--to dot translocation in the pseudoobscura subgroup, we find that kl--3 and Ppr--Y moved independently away from the Y chromosome to a different autosome in D. athabasca. We could not find Ary, kl--2 and Ory in our female assembly by BLAST, consistent with our Illumina read mapping and PCR results [28]. Ancestral Y genes in D. melanogaster are expressed almost exclusively in testis [30].…”

“…these genes are located on the Y chromosome in this species. This is consistent with the PCR results of [28]. However, while they assumed that the Y--dot translocation was shared by pseudoobscura/affinis flies and therefore interpreted their PCR screen of Ary, kl--2 and Ory being only present in males as them becoming Y--linked secondarily, a simpler explanation is that these genes never left the Y.…”

“…This is unexpected, since the Y--dot translocation is thought to be shared by members of the affinis and pseudoobscura subgroups. As mentioned above, none of the ancestral Y genes were found to be male--limited in D. affinis and most other species in this subgroup, and Y--linkage of Ary, kl--2 and Ory in some lineages was interpreted as these genes gaining Y--linkage secondarily [28]. Consistent with the PCR results [28], we find all five ancestral Y genes in female Illumina libraries from D. affinis and D. azteca (Figure 3).…”

“…In most species in the affinis subgroup (of which D. athabasca is a member), ancestral Drosophila Y genes are present in both sexes (Figure 3) [20,28]. This was interpreted as a single Y--dot translocation moving all ancestral Y genes to an autosome [22,28], but a lack of Y genes on the dot of D. athabasca and D. affinis argues against this scenario, and our results from D. athabasca suggest that ancestral Y genes may have been moved independently to autosomal locations in different species. To test this hypothesis, we analyzed high--quality genomes from D. affinis, a sister species to D. athabasca from which it diverged <3MY ago [31], and D. azteca (which diverged <6MY ago; Beckenbach et al 1993), two species for which all ancestral Y genes were found in both sexes.…”