Genomic analysis of Sparus aurata reveals the evolutionary dynamics of sex-biased genes in a sequential hermaphrodite fish

Abstract

Sexual dimorphism is a fascinating subject in evolutionary biology and mostly results from sex-biased expression of genes, which have been shown to evolve faster in gonochoristic species. We report here genome and sex-specific transcriptome sequencing of Sparus aurata, a sequential hermaphrodite fish. Evolutionary comparative analysis reveals that sex-biased genes in S. aurata are similar in number and function, but evolved following strikingly divergent patterns compared with gonochoristic species, showing overall slower rates because of stronger functional constraints. Fast evolution is observed only for highly ovary-biased genes due to female-specific patterns of selection that are related to the peculiar reproduction mode of S. aurata, first maturing as male, then as female. To our knowledge, these findings represent the first genome-wide analysis on sex-biased loci in a hermaphrodite vertebrate species, demonstrating how having two sexes in the same individual profoundly affects the fate of a large set of evolutionarily relevant genes.

Genome Sequencing and Transcriptome Analysis Reveal Recent Species-specific Gene Duplications in the Plastic Gilthead Sea Bream

“…Super-scaffolding assembly was performed using 7,700 CNEs derived from the genetic linkage map of the first gilthead sea bream genome release (Pauletto et al, 2018). These CNEs, associated to unique positions within 932 scaffolds, served for ordering and orienting 57.8% of the scaffold assembly length (∼732 Mb) in 24 super-scaffolds (Supplementary Figure 2).…”

“…(B) Venn diagram showing the overlap between unique gene annotation expression signatures in all analyzed tissues. Homology-based annotation was done according to the gilthead sea bream transcriptome (Pauletto et al, 2018) and NCBI non-redundant (Nr) database. (C) Percentage of duplicated genes among tissues or groups of tissues (blue columns).…”

“…For instance, the public genomes of European sea bass ( Dicentrarchus labrax ; 680 Mb), spotted green pufferfish ( T. nigroviridis ; 342 Mb) or the Amazon molly ( Poecilia formosa ; 830 Mb) are split in 46,509, 27,918 and 25,474 scaffolds, respectively (Jaillon et al, 2004; Tine et al, 2014; Warren et al, 2018). Likewise, the first gilthead sea bream genome draft comprised 55,202 scaffolds in a 760 Mb assembly (Pauletto et al, 2018). In concurrence with the present study, a new genome draft of gilthead sea bream was submitted to NCBI (Bioproject accession PRJEB31901), comprising ∼833 Mb, which is still below our assembly.…”

“…Highly conserved non-coding elements (CNEs) present in 3 hermaphrodite genomes ( S. aurata, Lates calcarifer, Monopterus albus ) were released by Pauletto et al, (2018), and the super-scaffold coordinates related to these CNEs (200-800 bp interval length) were then retrieved. Sequences were aligned against our assembly for increasing the super-scaffolding by means of the BLAST package.…”

“…Here we produced a high quality draft sequence of the gilthead sea bream genome by combining high-throughput sequencing with genetic linkage maps. The current draft assembly spans ∼1.24 Gb with 932 scaffolds ordered and oriented along 24 chromosomes derived from the genetic linkage map of the first gilthead sea bream genome release (Pauletto et al, 2018). Homology-based functional annotation, supported by RNA-seq transcripts, identified 55,423 actively transcribed genes corresponding to 21,275 unique descriptions.…”