Fish Lineages Research Articles

Юрій Дуброва (1955–2023) — біолог з України, якого чув світ: нотатки до біографії

The future famous geneticist Prof. Yuri Dubrova (1955–2023) was born in Kyiv (Ukraine), where he received excellent secondary and higher education and was awarded with a gold medal upon graduating from school. Eventually, he became one of the best graduates of the Department of Vertebrate Zoology at the Faculty of Biology of Taras Shevchenko National University of Kyiv. His interests included theoretical biology, evolutionary theory, genetics, biometrics, and bionics (for some time he studied the lateral lineage of cyprinid fishes). In his last years at the university, he focused on the study of spontaneous mutations. At the Vavilov Institute of General Genetics in Moscow, Y. Dubrova continued his post-graduate studies and successfully defended his PhD thesis. After the collapse of the USSR, he moved to the UK in search of better scientific and technical opportunities, where he became a professor at the University of Leicester. The scientist lived and worked in Leicester until the end of his life. He devoted himself fully to science, especially to radiation, medical and population genetics, and to teaching, and tried to participate in the study of highly complex medical and genetic issues related, in particular, to the consequences of man-made disasters—Chornobyl (Ukraine, Belarus), Semipalatinsk (Kazakhstan)—and other cases of large-scale radiation effects on life. Dr. Dubrova is the author and co-author of more than 150 scientific articles published in leading journals, including the American Journal of Human Genetics, International Journal of Radiation Biology, Radiation Research, Molecular Biology and Evolution, International Journal of Cancer, British Journal of Cancer, Science, and Nature. He co-operated with many of the world’s leading geneticists and gave lectures in Ukraine, Russia, the USA, Canada, Japan, etc. The article uses fragments of the author’s long correspondence with Y. Dubrova, which may be of interest to biographers of F. Dobrzhansky, M. Tymofeiev-Resovsky, O. Sozinov, O. Yablokov, O. Kistiakowsky, as well as to students, teachers, and historians of Kyiv National University, Kaniv Nature Reserve, and the University of Leicester.

A chromosome-level genome of electric catfish (Malapterurus electricus) provided new insights into order Siluriformes evolution.

The online version contains supplementary material available at 10.1007/s42995-023-00197-8.

Evidence for selfing in a vertebrate from whole-genome sequencing.

A growing number of recent genomic studies report asexual parthenogenetic reproduction in a wide range of taxa, including vertebrate species from the reptile, bird, and fish lineages. Yet, self-fertilization (selfing) has been recorded only in a single vertebrate, the mangrove killifish Kryptolebias marmoratus In cichlid fishes, sex determination is notably diverse and can be influenced by the environment, and sequential hermaphroditism has been reported for some species. Here, we present evidence for a case of facultative selfing in the cichlid fish Benitochromis nigrodorsalis, which is otherwise known as biparentally reproducing ovophilic mouthbrooder from Western Africa. Our laboratory observations revealed that a wild-caught individual produced repeatedly viable offspring in absence of a mating partner. By analyzing genome-wide single-nucleotide polymorphism (SNP) data, we compare that individual and two of its offspring to shed light on its reproductive mode. First, our results confirm uniparental reproduction. Second, overall heterozygosity is reduced in the offspring compared with outbred individuals. Retained maternal heterozygosity in the offspring is ∼51%, which is close to the theoretically expected value of a heterozygosity reduction of 50% by selfing. Heterozygosity patterns along individual chromosomes do not point to alternative parthenogenetic reproductive mechanisms like automixis by terminal or central fusion. Facultative selfing may represent an adaptive strategy ensuring reproduction when mating partners are absent and, hence, contribute to the cichlids' enormous evolutionary success.

Diversity of movement patterns of Longnose Gar tracked in coastal waters of western Lake Ontario

AbstractUnderstanding the spatial ecology of fish is critical for effective conservation and management. Gar (Lepisosteidae spp.) are an ancient lineage of freshwater fishes that have long been thought of as having high site fidelity with limited large-scale movements. We acoustically tagged Longnose Gar (L. osseus) in a large freshwater embayment (Hamilton Harbour) and tracked the movements of 12 individuals within this system and throughout the coastal waters of Lake Ontario for up to 4 years. Three distinct movement patterns were observed: migrants (N = 7), which moved throughout much of western Lake Ontario and had a maximum displacement of 184 km (linear distance); residents (N = 3), which remained in or near the original tagging location (an industrial slip with year-round warmwater outfall); and sporadic migrants (N = 2), which showed both migratory and resident behavioural patterns in different years. Seasonally, gar were most active during the summer and then fall, with more restricted home ranges and movements during winter suggestive of more quiescent behaviour. This study represents the first use of acoustic telemetry to track Longnose Gar movements year-round in a large lake and confirmed that a majority of tracked fishes make large-scale movements in Lake Ontario. Such results reframe the presumption that gar are more resident fishes with restricted space use.

Evolutionary origins of the lampriform pelagic radiation

Abstract Ray-finned fishes, which compose nearly half of living vertebrate diversity, provide an excellent system for studying the evolution of novel body forms. Lampriformes is a species-poor lineage of acanthomorph ray-finned fishes that has evolved two very different and highly specialized body plans suited to life in pelagic oceanic habitats: the deep, round-bodied bathysomes and the ribbon-like taeniosomes. Here, we present a new phylogenetic hypothesis and divergence time estimates for lampriform fishes based on an updated morphological dataset and DNA sequences from nuclear genes for all but one of the living lampriform families and 55% of recognized extant genera. Our analyses resolve two major clades in Lampriformes: the Bathysomi and the Taeniosomi. A time calibrated phylogeny shows that the origin of living lampriforms coincides with the aftermath of the Cretaceous–Palaeogene extinction and that anatomically modern pelagic morphotypes evolved 10 Myr after the start of the Palaeogene.

A continuous fish fossil record reveals key insights into adaptive radiation

Adaptive radiations have been instrumental in generating a considerable amount of life’s diversity. Ecological opportunity is thought to be a prerequisite for adaptive radiation1, but little is known about the relative importance of species’ ecological versatility versus effects of arrival order in determining which lineage radiates2. Palaeontological records that could help answer this are scarce. In Lake Victoria, a large adaptive radiation of cichlid fishes evolved in an exceptionally short and recent time interval3. We present a rich continuous fossil record extracted from a series of long sediment cores along an onshore–offshore gradient. We reconstruct the temporal sequence of events in the assembly of the fish community from thousands of tooth fossils. We reveal arrival order, relative abundance and habitat occupation of all major fish lineages in the system. We show that all major taxa arrived simultaneously as soon as the modern lake began to form. There is no evidence of the radiating haplochromine cichlid lineage arriving before others, nor of their numerical dominance upon colonization; therefore, there is no support for ecological priority effects. However, although many taxa colonized the lake early and several became abundant, only cichlids persisted in the new deep and open-water habitats once these emerged. Because these habitat gradients are also known to have played a major role in speciation, our findings are consistent with the hypothesis that ecological versatility was key to adaptive radiation, not priority by arrival order nor initial numerical dominance.

Teleost genomic repeat landscapes in light of diversification rates and ecology

Repetitive DNA make up a considerable fraction of most eukaryotic genomes. In fish, transposable element (TE) activity has coincided with rapid species diversification. Here, we annotated the repetitive content in 100 genome assemblies, covering the major branches of the diverse lineage of teleost fish. We investigated if TE content correlates with family level net diversification rates and found support for a weak negative correlation. Further, we demonstrated that TE proportion correlates with genome size, but not to the proportion of short tandem repeats (STRs), which implies independent evolutionary paths. Marine and freshwater fish had large differences in STR content, with the most extreme propagation detected in the genomes of codfish species and Atlantic herring. Such a high density of STRs is likely to increase the mutational load, which we propose could be counterbalanced by high fecundity as seen in codfishes and herring.

Phylogeographic relationships and morphological evolution between cave and surface Astyanax mexicanus populations (De Filippi 1853) (Actinopterygii, Characidae).

The Astyanax mexicanus complex includes two different morphs, a surface- and a cave-adapted ecotype, found at three mountain ranges in Northeastern Mexico: Sierra de El Abra, Sierra de Guatemala and Sierra de la Colmena (Micos). Since their discovery, multiple studies have attempted to characterize the timing and the number of events that gave rise to the evolution of these cave-adapted ecotypes. Here, using RADseq and genome-wide sequencing, we assessed the phylogenetic relationships, genetic structure and gene flow events between the cave and surface Astyanax mexicanus populations, to estimate the tempo and mode of evolution of the cave-adapted ecotypes. We also evaluated the body shape evolution across different cave lineages using geometric morphometrics to examine the role of phylogenetic signal versus environmental pressures. We found strong evidence of parallel evolution of cave-adapted ecotypes derived from two separate lineages of surface fish and hypothesize that there may be up to four independent invasions of caves from surface fish. Moreover, a strong congruence between the genetic structure and geographic distribution was observed across the cave populations, with the Sierra de Guatemala the region exhibiting most genetic drift among the cave populations analysed. Interestingly, we found no evidence of phylogenetic signal in body shape evolution, but we found support for parallel evolution in body shape across independent cave lineages, with cavefish from the Sierra de El Abra reflecting the most divergent morphology relative to surface and other cavefish populations.

Whole-genome Comparisons Identify Repeated Regulatory Changes Underlying Convergent Appendage Evolution in Diverse Fish Lineages.

Fins are major functional appendages of fish that have been repeatedly modified in different lineages. To search for genomic changes underlying natural fin diversity, we compared the genomes of 36 percomorph fish species that span over 100 million years of evolution and either have complete or reduced pelvic and caudal fins. We identify 1,614 genomic regions that are well-conserved in fin-complete species but missing from multiple fin-reduced lineages. Recurrent deletions of conserved sequences in wild fin-reduced species are enriched for functions related to appendage development, suggesting that convergent fin reduction at the organismal level is associated with repeated genomic deletions near fin-appendage development genes. We used sequencing and functional enhancer assays to confirm that PelA, a Pitx1 enhancer previously linked to recurrent pelvic loss in sticklebacks, has also been independently deleted and may have contributed to the fin morphology in distantly related pelvic-reduced species. We also identify a novel enhancer that is conserved in the majority of percomorphs, drives caudal fin expression in transgenic stickleback, is missing in tetraodontiform, syngnathid, and synbranchid species with caudal fin reduction, and alters caudal fin development when targeted by genome editing. Our study illustrates a broadly applicable strategy for mapping phenotypes to genotypes across a tree of vertebrate species and highlights notable new examples of regulatory genomic hotspots that have been used to evolve recurrent phenotypes across 100 million years of fish evolution.

Abandoning the Isochore Theory Can Help Explain Genome Compositional Organization in Fish.

The organization of the genome nucleotide (AT/GC) composition in vertebrates remains poorly understood despite the numerous genome assemblies available. Particularly, the origin of the AT/GC heterogeneity in amniotes, in comparison to the homogeneity in anamniotes, is controversial. Recently, several exceptions to this dichotomy were confirmed in an ancient fish lineage with mammalian AT/GC heterogeneity. Hence, our current knowledge necessitates a reevaluation considering this fact and utilizing newly available data and tools. We analyzed fish genomes in silico with as low user input as possible to compare previous approaches to assessing genome composition. Our results revealed a disparity between previously used plots of GC% and histograms representing the authentic distribution of GC% values in genomes. Previous plots heavily reduced the range of GC% values in fish to comply with the alleged AT/GC homogeneity and AT-richness of their genomes. We illustrate how the selected sequence size influences the clustering of GC% values. Previous approaches that disregarded chromosome and genome sizes, which are about three times smaller in fish than in mammals, distorted their results and contributed to the persisting confusion about fish genome composition. Chromosome size and their transposons may drive the AT/GC heterogeneity apparent on mammalian chromosomes, whereas far less in fishes.

Genome Sequencing Provides Novel Insights into Mudflat Burrowing Adaptations in Eel Goby Taenioides sp. (Teleost: Amblyopinae).

Amblyopinae is one of the lineage of bony fish that preserves amphibious traits living in tidal mudflat habitats. In contrast to other active amphibious fish, Amblyopinae species adopt a seemly more passive lifestyle by living in deep burrows of mudflat to circumvent the typical negative effects associated with terrestriality. However, little is known about the genetic origin of these mudflat deep-burrowing adaptations in Amblyopinae. Here we sequenced the first genome of Amblyopinae species, Taenioides sp., to elucidate their mudflat deep-burrowing adaptations. Our results revealed an assembled genome size of 774.06 Mb with 23 pseudochromosomes anchored, which predicted 22,399 protein-coding genes. Phylogenetic analyses indicated that Taenioides sp. diverged from the active amphibious fish of mudskipper approximately 28.3 Ma ago. In addition, 185 and 977 putative gene families were identified to be under expansion, contraction and 172 genes were undergone positive selection in Taenioides sp., respectively. Enrichment categories of top candidate genes under significant expansion and selection were mainly associated with hematopoiesis or angiogenesis, DNA repairs and the immune response, possibly suggesting their involvement in the adaptation to the hypoxia and diverse pathogens typically observed in mudflat burrowing environments. Some carbohydrate/lipid metabolism, and insulin signaling genes were also remarkably alterated, illustrating physiological remolding associated with nutrient-limited subterranean environments. Interestingly, several genes related to visual perception (e.g., crystallins) have undergone apparent gene losses, pointing to their role in the small vestigial eyes development in Taenioides sp. Our work provide valuable resources for understanding the molecular mechanisms underlying mudflat deep-burrowing adaptations in Amblyopinae, as well as in other tidal burrowing teleosts.

Social experience influences thermal sensitivity: lessons from an amphibious mangrove fish.

Understanding the factors affecting the capacity of ectothermic fishes to cope with warming temperature is critical given predicted climate change scenarios. We know that a fish's social environment introduces plasticity in how it responds to high temperature. However, the magnitude of this plasticity and the mechanisms underlying socially modulated thermal responses are unknown. Using the amphibious hermaphroditic mangrove rivulus fish Kryptolebias marmoratus as a model, we tested three hypotheses: (1) social stimulation affects physiological and behavioural thermal responses of isogenic lineages of fish; (2) social experience and acute social stimulation result in distinct physiological and behavioural responses; and (3) a desensitization of thermal receptors is responsible for socially modulated thermal responses. To test the first two hypotheses, we measured the temperature at which fish emerged from the water (i.e. pejus temperature) upon acute warming with socially naive isolated fish and with fish that were raised alone and then given a short social experience prior to exposure to increasing temperature (i.e. socially experienced fish). Our results did not support our first hypothesis as fish socially stimulated by mirrors during warming (i.e. acute social stimulation) emerged at similar temperatures to isolated fish. However, in support of our second hypothesis, a short period of prior social experience resulted in fish emerging at a higher temperature than socially naive fish suggesting an increase in pejus temperature with social experience. To test our third hypothesis, we exposed fish that had been allowed a brief social interaction and naive fish to capsaicin, an agonist of TRPV1 thermal receptors. Socially experienced fish emerged at significantly higher capsaicin concentrations than socially naive fish suggesting a desensitization of their TRPV1 thermal receptors. Collectively, our data indicate that past and present social experiences impact the behavioural response of fish to high temperature. We also provide novel data suggesting that brief periods of social experience affect the capacity of fish to perceive warm temperature.

Visualization of electric fields and associated behavior in fish and other aquatic animals.

In some fish lineages, evolution has led to unique sensory adaptations that provide information which is not available to terrestrial animals. These sensory systems include, among others, electroreception, which together with the ability of fish to generate electric discharges plays a role in social communication and object location. Most studies on electric phenomena in aquatic animals are dedicated to selected groups of electric fishes that regularly generate electric signals (Mormyriformes, Gymnotiformes). There exist, however, several species (hitherto described as non-electric) which, though able to perceive electric signals, have now been found to also generate them. In this article, we introduce a tool that we have designed to investigate such electric activity. This required significant adaptations of the equipment used in fish with regular discharge generation. The necessary improvements were realized by using a multielectrode registration setup allowing simultaneous visualization and quantification of behavior and associated electric activity of fish, alone or in groups, with combined electro-video clips. Precise synchronization of locomotor and electric behaviors made it possible to determine the electrically active fish in a group, and also the location of the electrogenic structure inside the fish's body. Our simple registration procedure, together with data presentation, should attract a broad audience of scientists taking up the challenge of uncovering electric phenomena in aquatic animals currently treated as electrically inactive.

Ancient fish lineages illuminate toll-like receptor diversification in early vertebrate evolution.

Since its initial discovery over 50years ago, understanding the evolution of the vertebrate RAG- mediated adaptive immune response has been a major area of research focus for comparative geneticists. However, how the evolutionary novelty of an adaptive immune response impacted the diversity of receptors associated with the innate immune response has received considerably less attention until recently. Here, we investigate the diversification of vertebrate toll-like receptors (TLRs), one of the most ancient and well conserved innate immune receptor families found across the Tree of Life, integrating genomic data that represent all major vertebrate lineages with new transcriptomic data from Polypteriformes, the earliest diverging ray-finned fish lineage. Our analyses reveal TLR sequences that reflect the 6 major TLR subfamilies, TLR1, TLR3, TLR4, TLR5, TLR7, and TLR11, and also currently unnamed, yet phylogenetically distinct TLR clades. We additionally recover evidence for a pulse of gene gain coincident with the rise of the RAG-mediated adaptive immune response in jawed vertebrates, followed by a period of rapid gene loss during the Cretaceous. These gene losses are primarily concentrated in marine teleost fish and synchronous with the mid Cretaceous anoxic event, a period of rapid extinction for marine species. Finally, we reveal a mismatch between phylogenetic placement and gene nomenclature for up to 50% of TLRs found in clades such as ray-finned fishes, cyclostomes, amphibians, and elasmobranchs. Collectively, these results provide an unparalleled perspective of TLR diversity and offer a ready framework for testing gene annotations in non-model species.

The Cretaceous–Paleogene transition in spiny-rayed fishes: surveying “Patterson’s Gap” in the acanthomorph skeletal record

In contrast to the rich collections of articulated spiny-rayed fishes from early Late Cretaceous and Eocene Lagerstätten, similar skeletal remains are sparse in Maastrichtian–Paleocene strata. Here we coin this poorly understood span “Patterson’s Gap” and review known articulated skeletons from it, summarizing available information on their phylogenetic affinities, age, and environmental context. Roughly fifty percent of taxa in both the Maastrichtian and Paleocene come from Europe and North America, with percomorphs representing around 60% of the skeletal acanthomorph taxa in each interval. This is higher than the only pre-Maastrichtian assemblage with a reasonable sample of percomorphs, but lower than most Eocene and younger sites. Fossils from Patterson’s Gap show a steady accumulation of the principal lineages of spiny-rayed fishes. Material from Paleocene or older strata provides evidence for most of the roughly 20 major acanthomorph divisions recovered by molecular studies. Many fossils from Patterson’s Gap remain undescribed and unnamed, and almost none have been included within formal phylogenetic analyses. Revision of existing material, combined with additional fieldwork, should be a priority for future efforts seeking to clarify this murky but significant interval in the evolutionary history of a major vertebrate radiation.

Expanded olfactory system in ray-finned fishes capable of terrestrial exploration

BackgroundSmell abilities differ greatly among vertebrate species due to distinct sensory needs, with exceptional variability reported in the number of olfactory genes and the size of the odour-processing regions of the brain. However, key environmental factors shaping genomic and phenotypic changes linked to the olfactory system remain difficult to identify at macroevolutionary scales. Here, we investigate the association between diverse ecological traits and the number of olfactory chemoreceptors in approximately two hundred ray-finned fishes.ResultsWe found independent expansions producing large gene repertoires in several lineages of nocturnal amphibious fishes, generally able to perform active terrestrial exploration. We reinforced this finding with on-purpose genomic and transcriptomic analysis of Channallabes apus, a catfish species from a clade with chemosensory-based aerial orientation. Furthermore, we also detected an augmented information-processing capacity in the olfactory bulb of nocturnal amphibious fishes by estimating the number of cells contained in this brain region in twenty-four actinopterygian species.ConclusionsOverall, we report a convergent genomic and phenotypic magnification of the olfactory system in nocturnal amphibious fishes. This finding suggests the possibility of an analogous evolutionary event in fish-like tetrapod ancestors during the first steps of the water-to-land transition, favouring terrestrial adaptation through enhanced aerial orientation.

Early Mesozoic burst of morphological disparity in the slow-evolving coelacanth fish lineage

Since the split of the coelacanth lineage from other osteichthyans 420 million years ago, the morphological disparity of this clade has remained remarkably stable. Only few outliers with peculiar body shape stood out over the evolutionary history, but they were phylogenetically and stratigraphically independent of each other. Here, we report the discovery of a new clade of ancient latimeriid coelacanths representing a small flock of species present in the Western Tethys between 242 and 241 million years ago. Among the four species, two show highly derived anatomy. A new genus shows reversal to plesiomorphic conditions in its skull and caudal fin organisation. The new genus and its sister Foreyia have anatomical modules that moved from the general coelacanth Bauplau either in the same direction or in opposite direction that affect proportions of the body, opercle and fins. Comparisons with extant genetic models shows that changes of the regulatory network of the Hedgehog signal gene family may account for most of the altered anatomy. This unexpected, short and confined new clade represents the only known example of a burst of morphological disparity over the long history of coelacanths at a recovery period after the Permian–Triassic Mass Extinction.

Sequences analysis and pituitary actions of tachykinins in Chinese sturgeon (Acipenser sinensis)

Tachykinins belong to a large, evolutionarily conserved family of brain/gut peptides that are involved in a variety of physiological functions in mammals, such as reproductive regulation. However, little information was available about tachykinins in ancient fish lineage. In the present study, we firstly identified three tachykinin genes (named tac1, tac3 and tac4) and three neurokinin receptors (named nk1r, nk2r and nk3r) from Chinese sturgeon brain and pituitary. Sequence analysis showed that tac1 encoded substance P (SP) and neurokinin A (NKA), tac3 encoded neurokinin B (NKB) and NKB-related peptide (NKBRP), and tac4 encoded hemokin 1 (HK-1) and hemokin 2 (HK-2), respectively. The luciferase reporter assay results showed that NK1R preferentially selected asSP, NK2R preferentially selected asNKA, and NK3R preferentially selected asNKB. Tissue expression analysis showed that the three tac genes were highly detected in the telencephalon and hypothalamus, whereas nkr genes were widely expressed in peripheral tissues. Spatio-temporal expression analysis showed that all three tac genes were highly expressed in unknown sex individuals. Intraperitoneal injection experiments showed that both asSP and asNKB could stimulate luteinizing hormone (LH) release in Chinese sturgeon serum. At the transcriptional level, asSP and asNKB could significantly reduce pituitary follicle-stimulating hormone beta (fshβ) mRNA expression, but induce pituitary growth hormone (gh) mRNA expression. In addition, estradiol (E2) could stimulate tac3 mRNA expression in hypothalamus. Taken together, this study provided information on the tachykinin family in Chinese sturgeon and demonstrates that asNKB and asSP could be involved in reproductive and growth regulation in pituitary.

Influence of ecological traits on spatio-temporal dynamics of an elasmobranch community in a heavily exploited basin

Elasmobranchs, which include sharks and batoids, play critical roles in maintaining the integrity and stability of marine food webs. However, these cartilaginous fish are among the most threatened vertebrate lineages due to their widespread depletion. Consequently, understanding dynamics and predicting changes of elasmobranch communities are major research topics in conservation ecology. Here, we leverage long-term catch data from a standardized bottom trawl survey conducted from 1996 to 2019, to evaluate the spatio-temporal dynamics of the elasmobranch community in the heavily exploited Adriatic Sea, where these fish have historically been depleted. We use joint species distribution modeling to quantify the responses of the species to environmental variation while also including important traits such as species age at first maturity, reproductive mode, trophic level, and phylogenetic information. We present spatio-temporal changes in the species community and associated modification of the trait composition, highlighting strong spatial and depth-mediated patterning. We observed an overall increase in the abundance of the dominant elasmobranch species, except for spurdog, which has shown a continued decline. However, our results showed that the present community displays lower age at first maturity and a smaller fraction of viviparous species compared to the earlier observed community due to changes in species’ relative abundance. The selected traits contributed considerably to explaining community patterns, suggesting that the integration of trait-based approaches in elasmobranch community analyses can aid efforts to conserve this important lineage of fish.

Unique nucleolar dominance patterns in different ploidy hybrid lineages derived from Cyprinus carpio (♀) × Megalobrama amblycephala (♂)

Nucleolar dominance is one of the epigenetic phenomena that refers to the dominance effect exhibited by the suppression of ribosomal RNA gene loci from one parent in heterozygous organisms. In this paper, the genetic and expression changes of 45S rRNA genes in different generations of the crucian carp-like homodiploid fish lineage (2nNCRC, F1, F2, F3, F5) and the autotetraploid carp lineage (4nNC, F1-F3) formed by distant hybridization of common carp (Cyprinus carpio, COC) (♀) × blunt snout bream (Megalobrama amblycephala, BSB) (♂) were mainly studied. The results showed that the nucleolar dominance patterns were different in different generations of the 2nNCRC lineage and the 4nNC lineage. In the different generations of the 2nNCRC lineage, 2nNCRC-F1 (F3, F5) exhibited the phenomenon of nucleolar dominance, while 2nNCRC-F2 did not and expressed the mutant 45S rRNA. The establishment of the nucleolar dominance pattern presented a more complicated situation, which may be related to the inconsistent coping mechanism among different generations after suffering the effect of “genome shock” at the early stage of the formation of the 2nNCRC lineage. Among the different generations of the 4nNC lineage, 4nNC-F2 existed the phenomenon of nucleolar dominance and expressed mutant 45S rRNA. However, 4nNC-F1 (F3) did not exist in the phenomenon of nucleolar dominance. The establishment of the nucleolar dominance pattern showed a process of instability-stability-instability, revealing the epigenetic instability of this lineage. This result may be related to the comprehensive effect caused by the continuous “genome shock” at the early stage of the formation of the 4nNC lineage, which can provide clues for further revealing the possible mechanism of occurrence and survival of polyploidization vertebrates. Moreover, this study found that the nucleolar dominance was biased towards BSB in the 2nNCRC lineage, while it was biased towards COC in the 4nNC lineage. The inconsistent results appeared in the different ploidy lineages formed by the same distant hybridization combination, which further verified that the dominance of transcription advantages species did not necessarily determine the biased characteristics of nucleolar dominance. Two lineages derived a mutant ITS1 sequence, which the mechanism may be related to some mechanisms triggered by the “genome shock” effect. This study will further fill a gap in studying nucleolar dominance in the early stage of the formation of homodiploid and polyploid vertebrates and provide important experimental data for studying fish epigenetics, which is of great significance in fish genetic breeding and biological evolution.