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Background  Eukaryote genomes frequently harbor supernumerary B chromosomes in addition to the “standard” A chromosome set. B chromosomes are thought to arise as byproducts of genome rearrangements and have mostly been considered intraspecific oddities. However, their evolutionary transcendence beyond species level has remained untested.    Results  Here we reveal that the large metacentric B chromosomes reported in several fish species of the genus  Astyanax  arose in a common ancestor at least 4 million years ago. We generated transcriptomes of  A. scabripinnis  and  A. paranae  0B and 1B individuals and used these assemblies as a reference for mapping all gDNA and RNA libraries to quantify coverage differences between B-lacking and B-carrying genomes. We show that the B chromosomes of  A. scabripinnis  and  A. paranae  share 19 protein-coding genes, of which 14 and 11 were also present in the B chromosomes of  A. bockmanni  and  A. fasciatus , respectively. Our search for B-specific single-nucleotide polymorphisms (SNPs) identified the presence of B-derived transcripts in B-carrying ovaries, 80% of which belonged to  nobox , a gene involved in oogenesis regulation. Importantly, the B chromosome  nobox  paralog is expressed > 30× more than the A chromosome paralog. This indicates that the normal regulation of this gene is altered in B-carrying females, which could potentially facilitate B inheritance at higher rates than Mendelian law prediction.    Conclusions  Taken together, our results demonstrate the long-term survival of B chromosomes despite their lack of regular pairing and segregation during meiosis and that they can endure episodes of population divergence leading to species formation.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12915-021-00991-9.

Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish