Sequences of probes used for FISH.

Centromeres reside in rapidly evolving, repeat-rich genomic regions, despite their essential function in chromosome segregation. Across organisms, centromeres are rich in selfish genetic elements such as transposable elements and satellite DNAs that can bias their transmission through meiosis. However, these elements still need to cooperate at some level and contribute to, or avoid interfering with, centromere function. To gain insight into the balance between conflict and cooperation at centromeric DNA, we take advantage of the close evolutionary relationships within the Drosophila simulans clade—D. simulans, D. sechellia, and D. mauritiana—and their relative, D. melanogaster. Using chromatin profiling combined with high-resolution fluorescence in situ hybridization on stretched chromatin fibers, we characterize all centromeres across these species. We discovered dramatic centromere reorganization involving recurrent shifts between retroelements and satellite DNAs over short evolutionary timescales. We also reveal the recent origin (D. sechellia, where the X and fourth centromeres now sit on telomere-specific retroelements. Finally, the Y chromosome centromeres, which are the only chromosomes that do not experience female meiosis, do not show dynamic cycling between satDNA and TEs. The patterns of rapid centromere turnover in these species are consistent with genetic conflicts in the female germline and have implications for centromeric DNA function and karyotype evolution. Regardless of the evolutionary forces driving this turnover, the rapid reorganization of centromeric sequences over short evolutionary timescales highlights their potential as hotspots for evolutionary innovation.

着丝粒（Centromeres）定位于快速演化、重复序列富集的基因组区域，尽管其在染色体分离过程中发挥着不可或缺的核心功能。在各类生物中，着丝粒富含自私遗传元件（selfish genetic elements），例如转座因子（transposable elements）与卫星DNA（satellite DNAs），这类元件可通过减数分裂（meiosis）实现自身的偏向传递。然而，这些元件仍需在一定程度上协同合作，要么助力着丝粒功能的正常运转，要么避免对着丝粒功能造成干扰。

为深入探究着丝粒DNA层面冲突与合作间的平衡机制，我们借助拟果蝇类群（Drosophila simulans clade）——包括拟果蝇（D. simulans）、塞舌尔果蝇（D. sechellia）、毛里求斯果蝇（D. mauritiana）——及其近缘物种黑腹果蝇（D. melanogaster）之间紧密的演化亲缘关系展开研究。我们结合染色质图谱分析（chromatin profiling）与针对拉伸染色质纤维的高分辨率荧光原位杂交（high-resolution fluorescence in situ hybridization）技术，全面表征上述所有物种的全部着丝粒。

我们发现了显著的着丝粒重排现象：在较短的演化时间尺度内，逆转录因子（retroelements）与卫星DNA之间会反复发生位置切换。我们还揭示了近期的起源事件：在塞舌尔果蝇（D. sechellia）中，X染色体与第四号染色体的着丝粒如今定位于端粒特异性逆转录因子（telomere-specific retroelements）之上。最后，仅有的不经历雌性减数分裂的Y染色体着丝粒，并未表现出卫星DNA与转座因子间的动态循环模式。

这些物种中着丝粒快速周转的模式，与雌性生殖系（female germline）中的遗传冲突相符，且对着丝粒DNA功能与核型进化（karyotype evolution）具有重要启示意义。无论驱动这种周转的演化力量为何，着丝粒序列在短演化时间尺度内的快速重排，均凸显了其作为演化创新（evolutionary innovation）热点区域的潜力。