Dynamic evolution of satellite DNAs drastically differentiates the genomes of Tribolium sibling species

Tandemly repeated sequences, known as satellite DNAs (satDNAs), belong to the most rapidly evolving elements in eukaryotic genomes. Notwithstanding their plentitude and diverse, yet often inconsistent functions, the evolutionary dynamics of satDNAs and the way they model genomes are still poorly understood. In this study, we explored satDNA dynamics in satDNA-rich genomes by focusing on two insect species from the genus Tribolium , so closely related that they can produce sterile hybrids. We identified 135 satDNAs in the Tribolium freemani satellitome, accounting for 38.7% of the genome. By comparing the satellitome of T. freemani with that of Tribolium castaneum , we deciphered the origins of their predominant, species-specific major satellites, which evolved from different repetitive elements still present in both genomes. Importantly, we discovered that the centromeric regions of the two species share an orthologous organization, characterized by different major satDNAs and related minor satDNAs. The T. freemani male sex chromosome, which lacks the major satDNA but contains a minor-like satDNA, further heightened the question of which satDNA might be centromere-competent. By analyzing the long-range organization of centromeric regions, we discovered that both major and minor satDNA arrays exhibit a strong tendency toward macro-dyad symmetry, suggesting that the secondary structures in these regions may be more important than the primary sequence itself. We also found evidence that the centromeric satDNAs of T. freemani are present in extrachromosomal circular DNAs, which thus may be responsible for their expansion and homogenization between non-homologous chromosomes. Throughout the T. freemani genome, we identified 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. These findings demonstrate that satDNAs with different genomic proportions and locations are subject to different DNA turnover mechanisms. While the dynamic evolution of satDNAs has undeniably played an important role in shaping and differentiating the genomes of Tribolium siblings, it remains to be determined whether the differences in their satDNA profiles are a cause or a consequence of speciation.