High-quality chromosome-level genomes of two tilapia species reveal their evolution of repeat sequences and sex chromosomes

Background Tilapias are one of the most farmed fishes that are coined as ‘aquatic chicken’ by the food industry. Like many other teleosts, Nile tilapia and blue tilapia exhibit very recent transition of sex chromosome systems since their divergence about 5 million years ago, making them a great model for elucidating the molecular and evolutionary mechanisms of sex chromosome turnovers. Studies into their sex-determining pathways are also critical for developing genetic sex control in aquaculture.

Results We report here the newly produced genomes of Nile tilapia and blue tilapia that integrate long-read sequencing and chromatin conformation data. The two nearly complete genomes have anchored over 97% of the sequences into linkage groups (LGs), and assembled majorities of complex repetitive regions including telomeres, centromeres and rDNA clusters. In particular, we inferred two episodes of repeat expansion at LG3 respectively in the ancestor of cichlids and that of tilapias. The consequential large heterochromatic region concentrated at one end of LG3 comprises tandem arrays of mRNA and small RNA genes, among which we have identified a candidate female determining gene Paics in blue tilapia. Paics show female-specific patterns of single-nucleotide variants, copy numbers and expression patterns in gonads during early gonadogenesis.

Conclusions Our work provide a very important genomic resource for functional studies of cichlids, and suggested that unequal distribution of repeat content that impacts the local recombination rate might make some chromosomes more likely to become sex chromosomes.