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Genetic sex determination by W and Z chromosomes has developed independently in different groups of organisms. To better understand the evolution of sex chromosomes and the plasticity of sex-determination mechanisms, we sequenced the whole genomes of a male (ZZ) and a female (ZW) half-smooth tongue sole (Cynoglossus semilaevis). In addition to insights into adaptation to a benthic lifestyle, we find that the sex chromosomes of these fish are derived from the same ancestral vertebrate protochromosome as the avian W and Z chromosomes. Notably, the same gene on the Z chromosome, dmrt1, which is the male-determining gene in birds, showed convergent evolution of features that are compatible with a similar function in tongue sole. Comparison of the relatively young tongue sole sex chromosomes with those of mammals and birds identified events that occurred during the early phase of sex-chromosome evolution. Pertinent to the current debate about heterogametic sex-chromosome decay, we find that massive gene loss occurred in the wake of sex-chromosome 'birth'.

Background Sexual growth dimorphism is a unique trait of the Chinese tongue sole ( Cynoglossus semilaevis ) where female fish grow much faster and bigger than their male counterparts. In tongue sole, the transcription factor dmrt1 is essential for testis formation and germ cell maintenance, but its disruption not only causes sterility but also leads to enhanced somatic growth in males. Results To study how dmrt1 links reproduction and growth, homozygous dmrt1 -knockout males were treated with LNP- dmrt1 , which carries dmrt1 mRNA inside. After several weeks of repeated injections, histological examination revealed some recovery of spermatogenesis, while some seminiferous tubules contained developing sperms. The transcriptome across the brain, blood, and gonad showed that the dmrt1 knock out changed steroidogenesis, meiosis, and hormone signaling, but LNP- dmrt1 treatment turned on many pathways involved in extracellular matrix interaction and steroid biosynthesis. Using circRNA, miRNA, and mRNA expression data together we built a ceRNA network, showing a couple of main controllers linked to cell cycle and neural signaling. Conclusions Our results show that although LNP-mediated dmrt1 mRNA delivery was able to partially rebuild testicular structure and reactivate some key pathways related to steroid synthesis and tissue organization, full recovery of normal spermatogenesis was not achieved. The involvement of circRNA–miRNA–mRNA regulatory networks further suggesting that post-transcriptional regulation may be involved in the limited rescue effect, rather than dmrt1 acting alone. These findings deepen our understanding of how reproductive capacity and growth are coordinated in sexually dimorphic fish and provide a potential foundation for developing more effective strategies to improve fertility and breeding efficiency in tongue sole aquaculture.

The substitution of fish resources as ingredients for aquafeeds by those based on vegetable sources is needed to ensure aquaculture sustainability in the future. It is known that Senegalese sole (Solea senegalensis) accepts high dietary content of plant ingredients without altering growth or flesh quality parameters. However, scarce information is available regarding the long-term impact of vegetable diets (combining the inclusion of both vegetable protein and oils) on the stress response and immunity of this fish species. This study aims to evaluate the concomitant effect of the extended use of vegetable protein-based diets with fish oil (FO) replacement (0, 50 or 100%) by vegetable oils (VO), on the response to acute (10 min) or prolonged (4 days) stress, induced by thermal shock. Plasma levels of cortisol, glucose and lactate as well as hepatic levels of glucose, glycogen and lactate were evaluated as primary and secondary responses to stress, 6 and 18 months after feeding the experimental diets (6 and 18 MAF). The brain monoaminergic activity in telencephalon and hypothalamus, and non-specific immune parameters were also evaluated. As expected, thermal shock induced an increase in values of plasma parameters related to stress, which was more evident in acute than in prolonged stress. Stress also affected lactate levels in the liver and the values of the alternative complement pathway-ACH50 in the plasma. Dietary substitution of FO induced an effect per se on some parameters such as decreased hepatic glucose and glycogen levels and peroxidase activity in plasma as well enhanced serotonergic activity in brain of non-stressed fish. The results obtained in some parameters indicate that there is an interaction between the use of vegetable diets with the physiological response to thermal stress, as is the case of the hepatic lactate, serotonergic neurotransmission in brain, and the activity of ACH50 in plasma. These results suggest that the inclusion of VO in plant protein based diets point to a slightly inhibited stress response, more evident for an acute than a prolonged stress. © 2018 Conde-Sieira et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

The evolutionary and genetic origins of the specialized body plan of flatfish are largely unclear. We analyzed the genomes of 11 flatfish species representing 9 of the 14 Pleuronectiforme families and conclude that Pleuronectoidei and Psettodoidei do not form a monophyletic group, suggesting independent origins from different percoid ancestors. Genomic and transcriptomic data indicate that genes related to WNT and retinoic acid pathways, hampered musculature and reduced lipids might have functioned in the evolution of the specialized body plan of Pleuronectoidei. Evolution of Psettodoidei involved similar but not identical genes. Our work provides valuable resources and insights for understanding the genetic origins of the unusual body plan of flatfishes. Analysis of 11 flatfish genomes indicates that Pleuronectoidei and Psettodoidei are not a monophyletic group. Genomic and transcriptomic data suggest that the WNT and RA pathways played a role in the evolution of the specialized body of flatfish.

Lysosome-associated membrane glycoproteins (LAMPs), including lysosomal membrane protein 1 (Lamp1) and lysosomal membrane protein 2 (Lamp2), are involved in phagocytosis, chaperone-mediated autophagy (CMA), and other pathways that interact with lysosomal activity. However, the role of Lamp2 in teleosts has not been clarified. In this study, we investigated the functions of lamp2 genes during Vibrio vulnificus infection. We achieved subcellular localization of the lamp2 gene at the cellular level and performed overexpression and RNA interference experiments followed by Lipopolysaccharides (LPS) stimulation to probe the expression changes of related genes. Ultrapathology analysis of the head-kidney revealed an increase in lysosomes and the formation of autophagosomal vesicles after V. vulnificus infection, suggesting that lysosomes bind to autophagosomes. The lamp2 gene, encoding 401 amino acids in Cynoglossus semilaevis, was constitutively expressed in all examined tissues of healthy half-smooth tongue sole, with the highest expression in blood. A challenge test was conducted to assess the response of half-smooth tongue sole (Cynoglossus semilaevis) to different concentrations of V. vulnificus. The results showed that the relative expression of lamp2 and its related genes—lc3, rab7, vamp8, atg14, stx17, snap29, ctsb, and ctsd—varied with time and concentration in the gill, spleen, head-kidney, blood, liver, and gut tissues. From the results of lamp2 gene overexpression and RNA interference experiments, it is hypothesized that lamp2 positively regulates lc3, rab7, vamp8, snap29, and stx17, and negatively regulates ctsd and ctsb. Our findings provide new primary data for the function of lamp2 gene in the half-smooth tongue sole., particularly its role in regulating the immune response against V. vulnificus.

Reproductive dysfunction in captive-bred males of the flatfish Solea senegalensis remains a major bottleneck for its aquaculture. To clarify the molecular basis underlying these impairments, we performed an integrated analysis of transcriptomes, proteomes and methylomes from gonads of wild-type individuals and first-generation (F1) captive fish of both sexes. Nineteen RNA-seq libraries and eighteen LC–MS/MS proteomes were generated, allowing the quantification of more than 32,000 genes and 2221 proteins. Differential expression and principal component analyses revealed that sex was the primary driver of molecular variation, whereas origin (F1 vs. wild-type) had a more moderate effect. Multi-omics integration showed a partial and comparison-dependent correspondence between RNA and protein levels, with a marked RNA–protein decoupling in F1 males. Despite this limited concordance, functional enrichment analyses identified consistent regulation of key biological processes, including translation, energy metabolism, and reproductive pathways such as gametogenesis, fertilization, and early embryonic development. Within this regulatory framework, previously characterized DNA methylation landscapes in gonadal tissue suggest an additional epigenetic layer modulating the transcriptional potential of reproductive genes, particularly in captive-bred males. F1 males exhibited coordinated down-regulation of reproductive functions across omic layers, consistent with altered post-transcriptional and post-translational regulation. Overall, this study provides the first comprehensive multi-omics framework integrating transcriptomic, proteomic, and epigenetic information in S. senegalensis gonads, offering mechanistic insights into the molecular basis of reproductive dysfunction in F1 broodstock and supporting future strategies to improve reproductive performance in aquaculture.

Hsp40–Hsp70 typically function in concert as molecular chaperones, and their roles in post-infection immune responses are increasingly recognized. However, in the economically important fish species Scophthalmus maximus (turbot), there is still a lack in the systematic identification, interaction models, and binding site analysis of these proteins. Herein, 62 Hsp40 genes and 16 Hsp70 genes were identified in the turbot at a genome-wide level and were unevenly distributed on 22 chromosomes through chromosomal distribution analysis. Phylogenetic and syntenic analysis provided strong evidence in supporting the orthologies and paralogies of these HSPs. Protein–protein interaction and expression analysis was conducted to predict the expression profile after challenging with Aeromonas salmonicida. dnajb1b and hspa1a were found to have a co-expression trend under infection stresses. Molecular docking was performed using Auto-Dock Tool and PyMOL for this pair of chaperone proteins. It was discovered that in addition to the interaction sites in the J domain, the carboxyl-terminal domain of Hsp40 also plays a crucial role in its interaction with Hsp70. This is important for the mechanistic understanding of the Hsp40–Hsp70 chaperone system, providing a theoretical basis for turbot disease resistance breeding, and effective value for the prevention of certain diseases in turbot.

Background Pleuronectiformes, also known as flatfish, are important model and economic animals. However, a comprehensive genome survey of their important organelles, mitochondria, has been limited. Therefore, we aim to analyze the genomic structure, codon preference, nucleotide diversity, selective pressure and repeat sequences, as well as reconstruct the phylogenetic relationship using the mitochondrial genomes of 111 flatfish species. Results Our analysis revealed a conserved gene content of protein-coding genes and rRNA genes, but varying numbers of tRNA genes and control regions across species. Various gene rearrangements were found in flatfish species, especially for the rearrangement of nad5 - nad6 - cytb block in Samaridae family, the swapping rearrangement of nad6 and cytb gene in Bothidae family, as well as the control region translocation and tRNA-Gln gene inversion in the subfamily Cynoglossinae, suggesting their unique evolutionary history and/or functional benefit. Codon usage showed obvious biases, with adenine being the most frequent nucleotide at the third codon position. Nucleotide diversity and selective pressure analysis suggested that different protein-coding genes underwent varying degrees of evolutionary pressure, with cytb and cox genes being the most conserved ones. Phylogenetic analysis using both whole mitogenome information and concatenated independently aligned protein-coding genes largely mirrored the taxonomic classification of the species, but showed different phylogeny. The identification of simple sequence repeats and various long repetitive sequences provided additional complexity of genome organization and offered markers for evolutionary studies and breeding practices. Conclusions This study represents a significant step forward in our comprehension of the flatfish mitochondrial genomes, providing valuable insights into the structure, conservation and variation within flatfish mitogenomes, with implications for understanding their evolutionary history, functional genomics and fisheries management. Future research can delve deeper into conservation biology, evolutionary biology and functional usages of variations.

For many years, parasite ecologists have debated the relative importance of phylogeny and ecology as drivers of parasite community structure. Here, we address this issue using data on the metazoan ectoparasite communities of different flatfish species. Twenty species of flatfish were collected along the continental shelf of the Southern Gulf of Mexico and examined for ectoparasites. Eight flatfish species were parasitized by at least one ectoparasite species. In total, 326 ectoparasites, representing 11 species (4 monogeneans, 4 copepods, 1 isopod, 1 branchiurid, and 1 leech) were removed from 1622 hosts examined. The highest prevalence (37.5%) occurred in Bomolochus sp1 from Trinectes maculatus, while the lower (0.1%) for Argulus sp., Gnathia sp. and Trachellobdella lubrica from Cyclopsetta chittendeni. Changes in the ectoparasite community structure per host species and region were evaluated using a Permutational Multivariate Analysis of Variance and represented by a multidimensional scaling analysis. Significant differences in the parasite species composition among regions and hosts were detected, but no significant interaction between regions and hosts occurred. A multivariate pairwise t-test detected significant differences in the parasite infracommunities between the Yucatan Shelf and the other two regions; in addition, significant differences were detected between C. chittendeni and the Syacium species as well as between Ancylopsetta dilecta and Syacium papillosum. In this case, there is no relationship between the patterns of ectoparasitic community structure and the inherent phylogenetic affinity of the hosts; instead, the variations in ectoparasitic communities are determined by a regional ecological component.

Background Flatfish cranial asymmetry represents one of the most remarkable morphological innovations among vertebrates, and has fueled vigorous debate on the manner and rate at which strikingly divergent phenotypes evolve. A surprising result of many recent molecular phylogenetic studies is the lack of support for flatfish monophyly, where increasingly larger DNA datasets of up to 23 loci have either yielded a weakly supported flatfish clade or indicated the group is polyphyletic. Lack of resolution for flatfish relationships has been attributed to analytical limitations for dealing with processes such as nucleotide non-stationarity and incomplete lineage sorting (ILS). We tackle this phylogenetic problem using a sequence dataset comprising more than 1,000 ultraconserved DNA element (UCE) loci covering 45 carangimorphs, the broader clade containing flatfishes and several other specialized lineages such as remoras, billfishes, and archerfishes. Results We present a phylogeny based on UCE loci that unequivocally supports flatfish monophyly and a single origin of asymmetry. We document similar levels of discordance among UCE loci as in previous, smaller molecular datasets. However, relationships among flatfishes and carangimorphs recovered from multilocus concatenated and species tree analyses of our data are robust to the analytical framework applied and size of data matrix used. By integrating the UCE data with a rich fossil record, we find that the most distinctive carangimorph bodyplans arose rapidly during the Paleogene (66.0–23.03 Ma). Flatfish asymmetry, for example, likely evolved over an interval of no more than 2.97 million years. Conclusions The longstanding uncertainty in phylogenetic hypotheses for flatfishes and their carangimorph relatives highlights the limitations of smaller molecular datasets when applied to successive, rapid divergences. Here, we recovered significant support for flatfish monophyly and relationships among carangimorphs through analysis of over 1,000 UCE loci. The resulting time-calibrated phylogeny points to phenotypic divergence early within carangimorph history that broadly matches with the predictions of adaptive models of lineage diversification.