Dynamic evolution of satellite DNAs drastically differentiates the genomes of <i>Tribolium</i> sibling species

Tandemly repeated satellite DNAs (satDNAs) are among the most abundant and fastest-evolving eukaryotic sequences, but the way they model genomes is still elusive. Here, we investigate the evolutionary dynamics of satDNAs in the extremely satDNA-rich genomes of two closely related <i>Tribolium</i> insects that produce sterile hybrids. In <i>Tribolium freemani</i>, we identify 135 satDNAs, accounting for 38.7% of the genome. Comparative analysis with the <i>Tribolium castaneum</i> satellitome reveals that the drastic difference occurs in their centromeric regions, which share orthologous organization characterized by totally different major satDNAs but related minor satDNAs. The <i>T. freemani</i> male sex chromosome, which lacks the major satDNA but contains a minor-like satDNA, further highlights the question of which satDNA is centromere-competent. By analyzing the long-range organization of the centromeric regions, we discover that both the major and minor satDNA arrays exhibit a strong tendency toward macro-dyad symmetry, suggesting that the secondary structures in the centromeres may be more important than the primary sequence itself. We find evidence that the centromeric satDNAs of <i>T. freemani</i> occur in extrachromosomal circular DNAs, which may contribute to their expansion and homogenization between nonhomologous chromosomes. We also identify numerous low-copy-number satDNAs that are orthologous between the siblings, some of which are associated with transposable elements, highlighting transposition as a mechanism of their spreading. The dynamic evolution of satDNAs has clearly influenced the differentiation of <i>Tribolium</i> genomes, but the question remains whether the differences in their satDNA profiles are a cause or consequence of speciation.