Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish
Duílio Mazzoni Zerbinato de Andrade Silva,
Francisco J. Ruiz-Ruano,
Ricardo Utsunomia,
María Martín-Peciña,
Jonathan Pena Castro,
Paula Paccielli Freire,
Robson Francisco Carvalho,
Diogo T. Hashimoto,
Alexander Suh,
Claudio Oliveira,
Fábio Porto-Foresti,
Roberto Ferreira Artoni,
Fausto Foresti,
Juan Pedro M. Camacho
Affiliations
Duílio Mazzoni Zerbinato de Andrade Silva
Departamento de Biologia Estrutural e Funcional, Instituto de Biociências de Botucatu, Universidade Estadual Paulista, UNESP, Distrito de Rubião Junior
Francisco J. Ruiz-Ruano
Department of Organismal Biology – Systematic Biology, Evolutionary Biology Centre, Uppsala University
Ricardo Utsunomia
Departamento de Genética, Instituto de Ciências Biológicas e da Saúde, ICBS, Universidade Federal Rural do Rio de Janeiro
María Martín-Peciña
Departamento de Genética, Universidad de Granada
Jonathan Pena Castro
Departamento de Genética e Evolução, Universidade Federal de São Carlos, UFSCAR
Paula Paccielli Freire
Departamento de Biologia Estrutural e Funcional, Instituto de Biociências de Botucatu, Universidade Estadual Paulista, UNESP, Distrito de Rubião Junior
Robson Francisco Carvalho
Departamento de Biologia Estrutural e Funcional, Instituto de Biociências de Botucatu, Universidade Estadual Paulista, UNESP, Distrito de Rubião Junior
Diogo T. Hashimoto
Centro de Aquicultura, Universidade Estadual Paulista, UNESP
Alexander Suh
Department of Organismal Biology – Systematic Biology, Evolutionary Biology Centre, Uppsala University
Claudio Oliveira
Departamento de Biologia Estrutural e Funcional, Instituto de Biociências de Botucatu, Universidade Estadual Paulista, UNESP, Distrito de Rubião Junior
Fábio Porto-Foresti
Departamento de Ciências Biológicas, Faculdade de Ciências, Universidade Estadual Paulista, UNESP, Campus de Bauru
Roberto Ferreira Artoni
Departamento de Genética e Evolução, Universidade Federal de São Carlos, UFSCAR
Fausto Foresti
Departamento de Biologia Estrutural e Funcional, Instituto de Biociências de Botucatu, Universidade Estadual Paulista, UNESP, Distrito de Rubião Junior
Abstract 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.