An investigation of Y chromosome incorporations in 400 species of <i>Drosophila</i> and related genera

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.普遍认为，Y染色体（Y chromosome）起源于普通常染色体（autosome），其演化过程伴随大规模基因丢失（仅保留部分雄性相关基因），并受性拮抗选择（sex-antagonistic selection）塑造，同时偶有雄性相关基因的插入补充。上述过程共同作用的最终结果，便是形成一条特化于雄性功能的染色体。这一过程曾被认为是不可逆的，但2005年研究者发现拟暗果蝇（Drosophila pseudoobscura）的Y染色体整合进入了常染色体中。Y染色体整合事件会带来重要影响：原本仅在雄性中存在的染色体将恢复常染色体遗传模式，该物种的性染色体系统也可能从XY/XX型转变为X0/XX型。为了评估这一现象的发生频率与诱因，我们对果蝇属（Drosophila）及其近缘属的400个物种开展了Y染色体整合事件的筛查。本次筛查额外发现了一次大规模Y染色体整合事件，该事件波及整个山果蝇亚组（montium subgroup），本次样本中包含该亚组的40个物种；总体而言，本次抽样的400个物种中有13%（52/400）存在Y染色体整合现象。尽管既往研究数据表明，Y染色体整合后，祖先游离状态的Y染色体便会消失，但本次分析使用的更大规模数据集显示，山果蝇亚组与拟暗果蝇类群中均有游离状态的Y染色体拷贝存活下来；且拟暗果蝇支系当前的Y染色体，正是由该游离Y染色体与新Y染色体（neoY）融合而来。本次400个物种的抽样分析还证实，此前提出的X染色体-常染色体融合（X-autosome fusion）与Y染色体整合之间的因果关联，至多只能说是微弱的：新发现的山果蝇亚组Y整合事件并未伴随X-常染色体融合，而已知的9次独立X-常染色体融合事件均未伴随Y染色体整合。Y染色体整合是一种长期未受到足够重视的Y染色体演化机制；我们的研究结果表明，至少在果蝇类群中，该机制发挥了重要作用，同时也凸显了在其他类群中开展同类研究的必要性。