Conserved satellite DNA motif and lack of interstitial telomeric sites in highly rearranged AfricanNothobranchiuskillifish karyotypes

AbstractRepetitive DNA may have significant impact on genome evolution. African annual killifishes of the genusNothobranchius(Teleostei: Nothobranchiidae), which has adapted to temporary water pools in African savannahs, possess genomes with high repeat content. They are also characterized by rapid karyotype and sex chromosome evolution but the role of genome repeats in these processes remains largely unknown. Here, we analyzed the distribution of telomeric (TTAGGG)nrepeat and Nfu-SatC satellite DNA (isolated formerly fromN. furzeri) by fluorescencein situhybridization in representatives across theNothobranchiusphylogeny (15 species), and withFundulosoma thierryias an outgroup. All analyzed taxa shared the presence of Nfu-SatC repeat but with diverse organization and distribution on chromosomes (from small clusters scattered genome-wide, to large localized accumulations, or a combined pattern). Nfu-SatC landscape was similar in conspecific populations ofN. guentheriandN. melanospilusbut slightly-to-moderately differed between populations ofN. pienaari, and between closely relatedN. kuhntaeandN. orthonotus. Inter-individual variability in Nfu-SatC patterns was found inN. orthonotusandN. krysanovi, including distinct segments present often in heterozygous condition. We revealed mostly no sex-linked patterns of studied repeat’s distribution in any of the sampled species including those with known sex chromosomes. Only inN. brieni(having an X1X2Y multiple sex chromosome system), Nfu-SatC probe covered substantial portion of the Y chromosome, similarly as formerly found inN. furzeriandN. kadleci(XY sex chromosomes), sister species not closely related toN. brieni. All studied species further shared patterns of telomeric FISH, with expected signals at the ends of all chromosomes and no additional interstitial telomeric sites. In summary, we revealed i) the presence of conserved satDNA class inNothobranchiusclade (a rare pattern among ray-finned fishes), ii) independent trajectories ofNothobranchiussex chromosome diferentiation, with recurrent and convergent accumulation of Nfu-SatC on the Y chromosome in some species, and iii) genus-wide shared propensity to loss of telomeric repeats during the mechanism of interchromosomal rearrangements. Collectively, our findings advance our understanding of genome structure, mechanisms of karyotype reshuffling and sex chromosome differentiation inNothobranchiuskillifishes from the genus-wide perspective.