A high-resolution comparative atlas across 74 fish genomes illuminates teleost evolution after whole-genome duplication

Teleost fish are one of the most species-rich and diverse clades amongst vertebrates, which makes them an outstanding model group for evolutionary, ecological and functional genomics. Yet, despite a growing number of sequence reference genomes, large-scale comparative analysis remains challenging in teleosts due to the specifics of their genomic organization. As legacy of a whole genome duplication dated 320 million years ago, a large fraction of teleost genomes remain in duplicate paralogous copies. This ancestral polyploidy confounds the detailed identification of orthologous genomic regions across teleost species. Here, we combine tailored gene phylogeny methodology together with the state-of-the art ancestral karyotype reconstruction to establish the first high resolution comparative atlas of paleopolyploid regions across 74 teleost fish genomes. We show that this atlas represents a unique, robust and reliable resource for fish genomics. We then use the comparative atlas to study the tetraploidization and rediploidization mechanisms that affected the ancestor of teleosts. Although the polyploid history of teleost genomes appears complex, we uncover that meiotic recombination persisted between duplicated chromosomes for over 60 million years after polyploidization, suggesting that the teleost ancestor was an autotetraploid.

Cognitive Phenotypic Plasticity: Environmental Enrichment Affects Learning but Not Executive Functions in a Teleost Fish, Poecilia reticulata

Many aspects of animal cognition are plastically adjusted in response to the environment through individual experience. A remarkable example of this cognitive phenotypic plasticity is often observed when comparing individuals raised in a barren environment to individuals raised in an enriched environment. Evidence of enrichment-driven cognitive plasticity in teleost fish continues to grow, but it remains restricted to a few cognitive traits. The purpose of this study was to investigate how environmental enrichment affects multiple cognitive traits (learning, cognitive flexibility, and inhibitory control) in the guppy, Poecilia reticulata. To reach this goal, we exposed new-born guppies to different treatments: an enrichment environment with social companions, natural substrate, vegetation, and live prey or a barren environment with none of the above. After a month of treatment, we tested the subjects in a battery of three cognitive tasks. Guppies from the enriched environment learned a color discrimination faster compared to guppies from the environment with no enrichments. We observed no difference between guppies of the two treatments in the cognitive flexibility task, requiring selection of a previously unrewarded stimulus, nor in the inhibitory control task, requiring the inhibition of the attack response toward live prey. Overall, the results indicated that environmental enrichment had an influence on guppies’ learning ability, but not on the remaining cognitive functions investigated.

Leptin Is an Important Endocrine Player That Directly Activates Gonadotropic Cells in Teleost Fish, Chub Mackerel

Leptin, secreted by adipocytes, directly influences the onset of puberty in mammals. Our previous study showed that leptin stimulation could promote the secretion of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) from pituitary cells in primary culture and ovarian development in chub mackerel. This study aimed to elucidate the detailed mechanism of leptin-induced effects on gonadotropin hormone-producing cells. We produced recombinant leptin using silkworm pupae and investigated the effects of leptin on FSH and LH secretion and gene expression in the primary culture of pituitary cells from chub mackerel. The presence or absence of co-expression of lepr mRNA, FSH and LH b-subunit mRNA in gonadotropic cells was examined by double-labeled in situ hybridization. The addition of leptin significantly increased the secretion and gene expression of FSH and LH from male and female pituitary cells in primary culture. In contrast, gonadotropin-releasing hormone 1 affected neither FSH secretion in cells from females nor fshb and lhb expression in cells from males and females. The expression of lepr was observed in FSH- and LH-producing cells of both males and females. The results indicate that leptin directly regulates gonadotropin synthesis and secretion and plays an important role in the induction of puberty in teleost fish.

Gill Transcriptomic Responses to Toxin-producing Alga Prymnesium parvum in Rainbow Trout

The gill of teleost fish is a multifunctional organ involved in many physiological processes, including protection of the mucosal gill surface against pathogens and other environmental antigens by the gill-associated lymphoid tissue (GIALT). Climate change associated phenomena, such as increasing frequency and magnitude of harmful algal blooms (HABs) put extra strain on gill function, contributing to enhanced fish mortality and fish kills. However, the molecular basis of the HAB-induced gill injury remains largely unknown due to the lack of high-throughput transcriptomic studies performed on teleost fish in laboratory conditions. We used juvenile rainbow trout (Oncorhynchus mykiss) to investigate the transcriptomic responses of the gill tissue to two (high and low) sublethal densities of the toxin-producing alga Prymnesium parvum, in relation to non-exposed control fish. The exposure time to P. parvum (4–5 h) was sufficient to identify three different phenotypic responses among the exposed fish, enabling us to focus on the common gill transcriptomic responses to P. parvum that were independent of dose and phenotype. The inspection of common differentially expressed genes (DEGs), canonical pathways, upstream regulators and downstream effects pointed towards P. parvum-induced inflammatory response and gill inflammation driven by alterations of Acute Phase Response Signalling, IL-6 Signalling, IL-10 Signalling, Role of PKR in Interferon Induction and Antiviral Response, IL-8 Signalling and IL-17 Signalling pathways. While we could not determine if the inferred gill inflammation was progressing or resolving, our study clearly suggests that P. parvum blooms may contribute to the serious gill disorders in fish. By providing insights into the gill transcriptomic responses to toxin-producing P. parvum in teleost fish, our research opens new avenues for investigating how to monitor and mitigate toxicity of HABs before they become lethal.

Effects of Hydrostatic Pressure Treatment of Newly Fertilized Eggs on the Ploidy Level and Karyotype of Pikeperch Sander lucioperca (Linnaeus, 1758)

We studied the effect of different magnitudes (7000 PSI (48.26 MPa), 8000 PSI (55.16 MPa), and 9000 PSI (62.05 MPa)) of hydrostatic pressure on the ploidy of pikeperch larvae. Pressure shock was applied 5 min after the fertilization of eggs at a water temperature of 14.8 ± 1 °C. A 7000 PSI pressure shock was applied for 10 or 20 min, while 8000 and 9000 PSI treatments lasted for 10 min. Each treatment with its respective control was completed in triplicate, where different females’ eggs served as a replicate. In the treatment groups exposed to 7000 PSI for 10 min, only diploid and triploid larvae were identified, while 2n/3n mosaic individuals were found after a 20-min exposure to a 7000 PSI pressure shock. The application of 8000 or 9000 PSI pressure shocks resulted in only triploid and mosaic individuals. Among larvae from eggs treated with 8000 PSI, three mosaic individuals with 2n/3n karyotype were identified (4.0 ± 6.9%), while a single (2.0 ± 3.5%) 1n/3n mosaic individual was found in the 9000 PSI-treated group. To our knowledge, this is the first report that demonstrates the induction of a haplo-triploid karyotype by hydrostatic pressure shock in teleost fish. The dominance of triploid individuals with a reasonable survival rate (36.8 ± 26.1%) after 8000 PSI shock supports the suitability of the hydrostatic pressure treatment of freshly fertilized eggs for triploid induction in pikeperch.

Adaptive Immune System in Fish

The immune system of all jawed vertebrates is composed of two major subsystems, the innate (non-specific) and adaptive (specific) immune system. The innate immune system is the first to respond to infectious agents; however, it does not provide longlasting protection. The adaptive immune system is activated later and responds to pathogens with specificity and memory. The main components of the adaptive immune system, including T cell receptors (TCRs), major histocompatibility complex (MHC), immunoglobulins (Igs), and recombination-activating gene (RAG) arose in the first jawed fish (cartilaginous and teleost fish). This review explores and discusses components of the adaptive immune system in teleost fish and recent developments in comparative immunology. Similar to mammals, the adaptive immune system in teleost fish is divided into two components: cellular-mediated responses and humoralmediated responses. T cells, the principal elements of cellular-mediated adaptive immune responses, differentiate into effector helper T (Th) cells or effector cytotoxic T cells (CTLs). The central elements involved in the differentiation of Th subsets in mammals, cytokines and master transcription factors, have also been identified in teleost fish. In addition, each subset of Th cells, defined with a particular cytokine to control the immune responses, has been described in teleost fish. Similarly, to mammals, CTLs contribute to cellular cytotoxicity in teleost fish. B cells act as a central player in humoral-mediated adaptive immunity by producing opsonizing, neutralizing and complement-binding antibodies and inducing antibody-dependent cellular cytotoxicity (ADCC). Three classes of antibodies named IgM, IgD, and IgT/Z have been characterized in teleost fish. The presence of an adaptive immune system and consequent immune memory in teleost fish allows vaccination, the most appropriate method for disease control in aquaculture. Immunological studies in fish provide a comprehensive assessment of the fish immune system, which is crucial for understanding the evolution of the mammalian immune system.