Abstract
Arapaima gigas is one of the largest freshwater fish species of high ecological and economic importance. Overfishing and habitat destruction are severe threats to the remaining wild populations. By incorporating a chromosomal Hi-C contact map, we improved the arapaima genome assembly to chromosome-level, revealing an unexpected high degree of chromosome rearrangements during evolution of the bonytongues (Osteoglossiformes). Combining this new assembly with pool-sequencing of male and female genomes, we identified id2bbY, a duplicated copy of the inhibitor of DNA binding 2b (id2b) gene on the Y chromosome as candidate male sex-determining gene. A PCR-test for id2bbY was developed, demonstrating that this gene is a reliable male-specific marker for genotyping. Expression analyses showed that this gene is expressed in juvenile male gonads. Its paralog, id2ba, exhibits a male-biased expression in immature gonads. Transcriptome analyses and protein structure predictions confirm id2bbY as a prime candidate for the master sex-determiner. Acting through the TGFβ signaling pathway, id2bbY from arapaima would provide the first evidence for a link of this family of transcriptional regulators to sex determination. Our study broadens our current understanding about the evolution of sex determination genetic networks and provide a tool for improving arapaima aquaculture for commercial and conservation purposes.
Highlights
Sex determination (SD) is the process of commitment of the undifferentiated bipotential gonad to develop towards testis or ovary
Sry is specific for therian mammals, and a high diversity of SD genes is observed in different groups of vertebrates, especially in fish[4,5]
With all id2b genes set to one ω value and the id2/id2a genes to a different one in PAML, we found that the two-ratio branch model fits significantly better than the one-ratio model, and the ω value of id2b (0.21) is two times that of the other id[2] genes (0.10) (Fig. S1)
Summary
Sex determination (SD) is the process of commitment of the undifferentiated bipotential gonad to develop towards testis or ovary. Arapaima gigas known in Brazil as pirarucu (“red fish” in the Tupi-Guarani language) is one of the largest freshwater fish on earth It inhabits the Amazon River and its tributaries. The scales can be used as nail file, spoon and handicraft, and the bony tongue serves to grate guarana seeds[9] As a dish this fish is known as the “Amazon cod”, having a central and important relevance for the economy in the Amazon region, comprising Northern Brazil, Peru, Ecuador, and C olombia[10]. We produced a whole genome sequence of arapaima, and identified that this species has a XX/XY sex chromosome system, meaning that males are h eterogametic[13]. We performed transcriptome and protein structure analyses, which provided further evidence for id2bbY is an excellent candidate as for the male SD gene of arapaima
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