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

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Zerbinato de Andrade Silva, Duilio Mazzoni ; Ruiz-Ruano, Francisco J. ; Utsunomia, Ricardo ; Martin-Pecina, Maria ; Pena Castro, Jonathan ; Paccielli Freire, Paula ; Francisco Carvalho, Robson ; Hashimoto, Diogo T. ; Suh, Alexander ; Oliveira, Claudio ; Porto-Foresti, Fabio ; Ferreira Artoni, Roberto ; Foresti, Fausto ; Camacho, Juan Pedro M.

• Document type: Journal article
• Source: BMC Biology; v. 19, n. 1, p. 17-pg., 2021-03-19.

Abstract

BackgroundEukaryote 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.ResultsHere 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 >30x 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.ConclusionsTaken 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. (AU)

• FAPESP's process: 14/09634-5 - Functional and evolutionary analysis of b chromosomes using the Astyanax paranae fish (Characiformes Characidae) as model
• Grantee: Fausto Foresti
• Support Opportunities: Regular Research Grants
• FAPESP's process: 16/09204-6 - Biodiversity and Biogeography in marine-estuarine fishes (Teleostei) from Brazil
• Grantee: Claudio de Oliveira
• Support Opportunities: Regular Research Grants
• FAPESP's process: 18/20610-1 - Study of the biogeography of the Brazilian coast using data population genetic data of marine catfish of the genera Cathorops and Genidens
• Grantee: Claudio de Oliveira
• Support Opportunities: Regular Research Grants
• FAPESP's process: 14/26508-3 - Phylogeny of the hyperdiverse order Characiformes (Teleostei: Ostariophysi) using ultraconserved elements
• Grantee: Claudio de Oliveira
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 17/22447-8 - Comparative Genetic Activity on B Chromosomes of Astyanax species (Teleostei, Characiformes)
• Grantee: Duílio Mazzoni Zerbinato de Andrade Silva
• Support Opportunities: Scholarships in Brazil - Post-Doctoral