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

Abstract

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 Tribolium insects that produce sterile hybrids. In Tribolium freemani, we identify 135 satDNAs, accounting for 38.7% of the genome. Comparative analysis with the Tribolium castaneum satellitome reveals that the drastic difference occurred in their centromeric regions, which share orthologous organization characterized by totally different major satDNAs but related minor satDNAs. The T. freemani male sex chromosome, which lacks the major satDNA but contains a minor-like satDNA, further highlighted 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 T. freemani 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 Tribolium genomes, but the question remains whether the differences in their satDNA profiles are a cause or consequence of speciation.