Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish
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AuthorSilva, Duílio M. Z. de A.; Ruiz-Ruano, Francisco J.; Martín Peciña, María; Martínez Camacho, Juan Pedro
Silva, D.M., Ruiz-Ruano, F.J., Utsunomia, R. et al. Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish. BMC Biol 19, 52 (2021). [https://doi.org/10.1186/s12915-021-00991-9]
SponsorshipFundacao de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP) 2014/09634-5 2013/24143-5 2017/22447-8 2018/20610-1 2016/09204-6 2014/26508-3; CAPES; National Council for Scientific and Technological Development (CNPq) 306054/2006-0; Spanish Secretaria de Estado de Investigacion, Desarrollo e Innovacion CGL2015-70750-P; Junta de Andalucia; Sven och Lilly Lawskis fond (Sweden); Marie Sklodowska-Curie Individual Fellowship (European Commission) 875732; Uppsala University
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 singlenucleotide 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.