Comparative Satellitomics in Arowanas (Telostei, Osteoglossiformes) Sheds Light on the Evolution of Ancient Satellite DNAs

Abstract

A significant fraction of the genomes of most multicellular eukaryotes includes extensive arrays of tandemly repeated sequences, collectively referred to as satellite DNAs (satDNAs). However, the mechanisms responsible for generating and maintaining varying satDNA abundances across lineages and temporal scales are still unclear. This work focused on arowana fishes (Teleostei, Osteoglossiformes) as a model; their widespread intercontinental distribution and basal phylogenetic position within Teleostei make them a compelling model for evolutionary research, especially in the realm of satDNA molecular evolution. Through the integration of genomic and chromosomal data, we analyzed and compared the catalogs of satDNA families (i.e., satellitomes) of four out of the six extant arowana species, elucidating ancestral evolutionary trends and establishing their temporal history. Arowanas displayed a small number of satDNA families, ranging from 16 to 25 in Osteoglossum bicirrhosum and Scleropages formosus, respectively. Alongside the identification of some shared satDNAs, many considered species-specific, nonetheless possess a limited number of copies in other species. The minimal variation observed both within and across species highlights the long-term conservation of satDNAs during evolution, since specific ones (referred to as long-term conserved satDNAs) may have endured throughout a lengthy evolutionary period. Moreover, fluorescence in situ hybridization (FISH) investigations conducted with the most abundant satDNAs demonstrated unique hybridization patterns for homologous orthologous ones, signifying their dynamic genomic positioning. Besides, the similarities of satDNAs among species align with their phylogenetic relationships, showing the high dynamism of arowanas' satDNAs, with several evolutionary events driving their sequence diversity.