Conserved satellite DNA motif and lack of interstitial telomeric sites in highly rearranged African Nothobranchius killifish karyotypes

Abstract

Repetitive DNA may have significant impact on genome evolution. African annual killifishes of the genus Nothobranchius (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)n repeat and Nfu-SatC satellite DNA (isolated formerly from N. furzeri) by fluorescence in situ hybridization in representatives across the Nothobranchius phylogeny (15 species), and with Fundulosoma thierryi as 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 of N. guentheri and N. melanospilus but slightly-to-moderately differed between populations of N. pienaari, and between closely related N. kuhntae and N. orthonotus. Inter-individual variability in Nfu-SatC patterns was found in N. orthonotus and N. krysanovi, including distinct segments present often in heterozygous condition. We revealed mostly no sex-linked patterns of studied repeats distribution in any of the sampled species including those with known sex chromosomes. Only in N. brieni (having an X1X2Y multiple sex chromosome system), Nfu-SatC probe covered substantial portion of the Y chromosome, similarly as formerly found in N. furzeri and N. kadleci (XY sex chromosomes), sister species not closely related to N. 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 in Nothobranchius clade (a rare pattern among ray-finned fishes), ii) independent trajectories of Nothobranchius sex 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 in Nothobranchius killifishes from the genus-wide perspective.