Cyclical evolution of centromere architecture across 193 eukaryote species

Eukaryotic chromosomes rely on centromeres for attachment to spindle microtubules and segregation during cell division, yet exhibit a paradoxical diversity of architectures, including satellite arrays, transposon clusters, and holocentricity1–3. To explore the evolution of centromere diversity, we analyzed 193 Darwin Tree of Life genomes from a range of plant, animal, and fungal eukaryotes4. Nearly half of the species exhibited satellite array architecture, but this pattern showed frequent gains and losses across the phylogeny. While satellites vary in their primary DNA sequence between species, their higher-order repeat structures are conserved, implying shared recombination dynamics across eukaryotes. The satellite arrays were frequently invaded by diverse centrophilic transposons, from both RNA and DNA classes. In 54 species, transposons themselves dominate the centromere. Recombination following integration has generated transposon-tandem repeats at multiple scales, revealing mechanisms to recreate satellite-like structures after invasion. We also analyzed 29 holocentric plants and animals, which varied in the presence of periodic satellite arrays, and the centromeric histone CENP-A/CENH3. Our findings suggest that eukaryotic centromeres have repeatedly transitioned between satellite- and transposon-dominated architectures, alongside multiple independent origins of holocentricity. These results are consistent with widespread meiotic drive driving cyclical centromere turnover5,6, despite the conserved requirement for accurate chromosome segregation.