Evolution Of Fishes Research Articles

A classic key innovation constrains oral jaw functional diversification in fishes

Abstract Modifications to the pharyngeal jaws—a prey processing system located posterior to the mouth cavity—are widely considered a key innovation that enhanced diversification within several prominent fish clades. Seen in cichlids, damselfishes, wrasses, and a few other lineages, these musculoskeletal alterations are believed to increase the evolutionary independence and, thus, the diversification of the oral and pharyngeal jaw systems. To test this classic hypothesis, we conducted comparative phylogenetic analyses to assess the effect of the pharyngeal novelty on the diversification of feeding morphology and kinematics across a taxonomically diverse sample of spiny-rayed fishes. We quantified movements of the oral jaws and other craniofacial structures from 689 suction-feeding strikes using high-speed videos collected from 228 species with and without the pharyngeal jaw novelty. Contradicting long-held predictions, we find significantly greater disparity across all traits and faster rates of oral jaw functional evolution in fishes without the specialized prey processing system. The modified pharyngeal jaw is undoubtedly a functional innovation as it enhances the strength of the prey processing system, facilitating exceptional transition rates to feeding on hard and tough prey. However, it also restricts the diversification of the feeding system, revealing that the impact of pharyngognathy is more nuanced than previously thought. In light of these and other recent findings, a reinterpretation of the macroevolutionary consequences of the pharyngeal jaw novelty is needed.

Chromosome-level genome assembly and population genomic analysis provide insights into the genetic diversity and adaption of Schizopygopsis younghusbandi on the Tibetan Plateau.

The Yarlung Tsangpo River on the Tibetan Plateau provides a unique natural environment for studying fish evolution and ecology. However, the genomes and genetic diversity of plateau fish species have been rarely reported. Schizopygopsis younghusbandi, a highly specialized Schizothoracine species and economically important fish inhabiting the Yarlung Tsangpo River, is threatened by overfishing and biological invasion. Herein, we generated a chromosome-level genome of S. younghusbandi and whole-genome resequencing data for 59 individuals from six locations of the river. The results showed that the divergence time between S. younghusbandi and other primitive Schizothoracine species was ∼4.2 Mya, coinciding with the major phase of the Neogene Tibetan uplift. The expanded gene families enriched in DNA integration and replication, ion binding and transport, energy storage, and metabolism likely contribute to the adaption of this species. The S. younghusbandi may have diverged from other highly specialized Schizothoracine species in the Zanda basin during the Pliocene epoch, which underwent major population reduction possibly due to the drastic climate change during the last glacial period. Population analysis indicated that the ancient population might have originated upstream before gradually adapting to evolve into the populations inhabiting the mid-stream and downstream regions of the Yarlung Tsangpo River. In conclusion, the chromosome-level genome and population diversity of S. younghusbandi provide valuable genetic resources for the evolution, ecology, and conservation studies of endemic fishes on the Tibetan Plateau.

Assembly and annotation of a chromosome-level reference genome for the endangered Colorado pikeminnow Ptychocheilus lucius.

Advancements in genome sequencing technology have brought unprecedented accessibility of high-throughput sequencing to species of conservation interest. The potential knowledge gained from application of these techniques is maximized by availability of high-quality, annotated reference genomes for endangered species. However, these vital resources are often lacking for endangered minnows of North America (Cypriniformes: Leuciscidae). One such endangered species, Colorado pikeminnow (Ptychocheilus lucius) is the largest North American minnow and the top-level native aquatic predator in the Colorado River Basin of the southwestern United States and northwestern Mexico. Over the past century Colorado pikeminnow has suffered habitat loss and population declines due to anthropogenic habitat modifications and invasive species introductions. The lack of genetic resources for Colorado pikeminnow has hindered conservation genomic study of this unique organism. This study seeks to remedy this issue by presenting a high-quality reference genome for Colorado pikeminnow developed from Pacific Biosciences HiFi sequencing and Hi-C scaffolding. The final assembly was a 1.1 Gb genome comprised of 305 contigs including 25 chromosome-sized scaffolds. Measures of quality, contiguity, and completeness met or exceeded those observed for Danio rerio (Danionidae) and two other Colorado River Basin leuciscids (Meda fulgida and Tiaroga cobitis). Comparative genomic analyses identified enrichment of gene families for growth, development, immune activity, and gene transcription; all of which are important for a large-bodied piscivorous fish living in a dynamic environment. This reference genome will provide a basis for important conservation genomic study of Colorado pikeminnow and help efforts to better understand the evolution of desert fishes.

The Research Advances in Distant Hybridization and Gynogenesis in Fish

ABSTRACTDistant hybridization and gynogenesis are two prevalent breeding techniques for fishes. Drawing from the research achievements of our team and the existing literature, we summarize the reproductive traits and genetic features of fishes derived from distant hybridizations and gynogenesis, and we deduce the fundamental mechanisms of these two methods and compare them, discerning their common and different characteristics. Both distant hybridization and gynogenesis techniques can alter genotypes and phenotypes, thus establishing them as significant breeding methods. Additionally, the genetic principles and the basic biological characteristics of distant hybridization and gynogenesis in fish have been inferred. We propose the concepts of macro‐hybrid and micro‐hybrid based on extensive experimental findings from fish distant hybridizations and gynogenesis. The term “macro‐hybrid” refers to offspring from distant hybridization that possess two distinct subgenomes, each inherited from one of the two parental species, such as allodiploid and allotetraploid lineages. The concept of “micro‐hybrid” refers to offspring, including autodiploid and autotetraploid lineages, as well as those resulting from artificial gynogenesis, whose genome almost originates solely from the maternal parent but in which certain DNA fragments derived from the paternal parent insert. Distant hybridization and gynogenesis are vital techniques in fish genetics, breeding, and evolution. We highlight the prospective paths for research and application of distant hybridization and gynogenesis in fishes.

Discriminating the origin of fish from closely related water bodies by combining NMR spectroscopy with statistical analysis and machine learning

Pikeperch, perch and bream are among the most traded and valued fish species in North-Eastern Europe. Therefore, it is necessary to be able to distinguish fish from different lakes and coastal sea regions to ensure a good traceability of products in the fish market and to protect both consumers and fish stocks. Untargeted metabolomics using nuclear magnetic resonance (NMR) spectroscopy is a suitable tool for this purpose. It is an established method for determining various properties of biological and living systems, such as health, origin, type, etc. Statistical methods including principal component analysis (PCA) and linear discriminant analysis (LDA) are typically applied to NMR data to correlate spectra with a particular research question.Herein we examine fish from three closely related water bodies and demonstrate that reliable determination of the water body that a particular fish originates from by traditional statistical analysis (PCA and LDA) of fish NMR spectra is not possible. In contrast, determining the fish species is possible. We proceed to show that machine learning methods perform better and that a combination of statistical analysis (LDA) and random forest (RF), a supervised machine learning technique, allows reliable determination of the originating water body, while being also tolerant to seasonal variations. This is an improvement over prior work, which has dealt with more clearly distinguished origins of fish. Exceptional accuracy was achieved in correctly assigning fish to their origin even in a scenario where two of the water bodies are connected by a river through which the fish are known to migrate. Since determining the origin of fish is important in environmental protection, we recommend following up this approach and using it as the basis of a robust tool for environmental protection and other monitoring purposes.

Hypothalamic integration of nutrient sensing in fish.

The hypothalamus plays a crucial role in regulating feeding behavior in fish. In this Review, we aim to summarise current knowledge on specific mechanisms for sensing glucose, fatty acids and amino acids in fish, and to consider how this information is integrated in the hypothalamus to modulate feed intake. In fish, specific neuronal populations in the nucleus lateralis tuberalis (NLTv) of the hypothalamus are equipped with nutrient sensors and hormone receptors, allowing them to respond to changes in metabolite levels and hormonal signals. These neurons produce orexigenic (Npy and Agrp) and anorexigenic (Pomc and Cart) neuropeptides, which stimulate and suppress appetite, respectively. The modulation of feeding behavior involves adjusting the expression of these neuropeptides based on physiological conditions, ultimately influencing feeding through reciprocal inhibition of anorexigenic and orexigenic neurons and signalling to higher-order neurons. The activation of nutrient sensors in fish leads to an enhanced anorexigenic effect, with downregulation of agrp and npy, and upregulation of cart and pomc. Connections between hypothalamic neurons and other populations in various brain regions contribute to the intricate regulation of feeding behaviour in fish. Understanding how feed intake is regulated in fish through these processes is relevant to understanding fish evolution and is also important in the context of aquaculture.

Salinity plays a limited role in determining rates of size evolution in fishes globally across multiple scales

Salinity plays a limited role in determining rates of size evolution in fishes globally across multiple scales

Ecological evolution of salmonids

For the first time, ecological evolution of salmonid fishes is analyzed using the method of historical biogeography, considering formation of ecology and reproductive biology for these species under planetary climatic and geological changes. Climate cooling in the Cenozoic and associated reconstruction of the food base for salmonids had a major impact on evolution of their ecology. This process began at the Asian coast of the North Pacific much earlier than at the American coast and was much more intense there. The salmonids developed marine and oceanic feeding that led to their stocks increasing and a subsequent imbalance with freshwater prey. Adapting to this imbalance, the species of gen. Oncorhynchus came to irreversible reduction of organs and functions in the fresh water and absolute mortality of producers. Egg development lengthened in cold environments, and anadromous and semi-anadromous salmonid species were forced to spawn earlier, so that the larvae would hatch during the spring bloom of their prey. Gradually, the timing of their spawning shifted from early spring to winter and then to fall; accordingly, the spawning run to the rivers began earlier, in particular in the northern areas. The spawning season of atlantic salmon Salmo salar and brown trout Salmo trutta shifted to a fall and spring-summer spawning run in the north of their range and to a winter-spring and fall spawning run in the south of their range, but there is currently no reason to consider these runs as seasonal races, given that both cases evolved from a single run in the process of evolutionary changes when the spawning season was interrupted by either winter cooling or summer warming in the lower river reaches and at the coast. The northern and southern populations of salmonid fishes in the Pacific separated, too, because of these ecological changes in the late Pliocene, in conditions of cold climate. Being in isolation, they diverged enough to be considered as separate taxa rather than seasonal races.

Molecular Dating of the Teleost Whole Genome Duplication (3R) Is Compatible With the Expectations of Delayed Rediploidization.

Vertebrate evolution has been punctuated by three whole genome duplication events that have been implicated causally in phenotypic evolution, from the origin of phenotypic novelties to explosive diversification. Arguably, the most dramatic of these is the 3R whole genome duplication event associated with the origin of teleost fishes which comprise more than half of all living vertebrate species. However, tests of a causal relationship between whole genome duplication and teleost diversification have proven difficult due to the challenge of establishing the timing of these phenomena. Here we show, based on molecular clock dating of concatenated gene alignments, that the 3R whole genome duplication event occurred in the early-middle Permian (286.18 to 267.20 million years ago; Ma), 52.02 to 12.84 million years (Myr) before the divergence of crown-teleosts in the latest Permian-earliest Late Triassic (254.36 to 234.16 Ma) and long before the major pulses of teleost diversification in Ostariophysi and Percomorpha (56.37 to 100.17 Myr and at least 139.24 to 183.29 Myr later, respectively). The extent of this temporal gap between putative cause and effect precludes 3R as a deterministic driver of teleost diversification. However, these age constraints remain compatible with the expectations of a prolonged rediploidization process following whole genome duplication which, through the effects of chromosome rearrangement and gene loss, remains a viable mechanism to explain the evolution of teleost novelties and diversification.

Enhancing Guided Bone Regeneration with a Novel Carp Collagen Scaffold: Principles and Applications.

Bone defects resulting from trauma, surgery, and congenital, infectious, or oncological diseases are a functional and aesthetic burden for patients. Bone regeneration is a demanding procedure, involving a spectrum of molecular processes and requiring the use of various scaffolds and substances, often yielding an unsatisfactory result. Recently, the new collagen sponge and its structural derivatives manufactured from European carp (Cyprinus carpio) were introduced and patented. Due to its fish origin, the novel scaffold poses no risk of allergic reactions or transfer of zoonoses and additionally shows superior biocompatibility, mechanical stability, adjustable degradation rate, and porosity. In this review, we focus on the basic principles of bone regeneration and describe the characteristics of an "ideal" bone scaffold focusing on guided bone regeneration. Moreover, we suggest several possible applications of this novel material in bone regeneration processes, thus opening new horizons for further research.

A comprehensive genome survey study unveils the genomic characteristics and phylogenetic evolution of fishes in the Uranoscopidae family

The construction of high-quality genomes is fundamental for molecular studies of species. Currently, there are no published genome sequences within the Uranoscopidae family, and research on the genomic characteristics of this family is lacking. In this study, genomic analyses of seven species from the Uranoscopidae family which captured from the southeastern coast of China were conducted using next-generation sequencing technology. The results revealed that the genomic characteristics of the seven species are relatively similar. The genome sizes of the seven Uranoscopidae species ranged from 536.00 Mb to 652.49 Mb, with repeat sequence proportions between 20.09% and 36.64%, and heterozygosity levels ranging from 0.41% to 0.88%. The assembled draft genomes exhibited GC contents of these species ranging from approximately 42.14% to 43.53%. Furthermore, the mitochondrial sequences for the seven species were assembled, with sizes ranging from 14,966 to 18,446 bp. The evolutionary relationships between different species were depicted through the mapping of conserved genes, whole-genome variances and mitochondrial genome sequences. Besides, the historical effective population sizes of all species experienced rapid expansion after the Last Interglacial Period, with three species undergoing bottleneck effects. In conclusion, this study provides a reference for the subsequent construction of high-quality genomes for species within the Uranoscopidae family and offers a rich data resource for further evolutionary research.

Growth and replication of infectious bursal disease virus in the fish cell line as an experimental vaccine

Recently, several attempts have been made to replace egg-based with cell-based vaccines to prevent and control Infectious Bursal Disease Virus (IBDV). This study aimed to evaluate a new fish cell line (M99) for culturing and replicating IBDV. After observing complete cytopathic effects (CPE) on the M99 cell line, virus titers were determined using the TCID50 test, and the presence of the virus was confirmed using an RT-PCR test. Subsequently, 135 broiler chickens (14 days old) were randomly divided into three equal groups for immune response measurements: G1: immunized with a commercial vaccine, G2: immunized with an experimental vaccine, and G3: control. Antibody responses, bursal index, and histopathological evaluations were examined on different days after immunization. Based on the results, CPE of the virus was noticeable from the first passage, becoming complete by the third passage. The infectious titer of the virus was log106.9. Antibody titer measured 21 days after immunization in both vaccinated groups were significantly differed from the control group (p < 0.05). The results obtained from examining the bursal index and histopathological evaluations showed no significant difference between the studied groups at different times. Overall, this research is the first report on the successful cultivation of infectious bursal virus on a permanent cell line of fish origin, with the advantages of tolerance to a wide temperature range (26–40 degrees Celsius). Therefore, this cell line has potential for use to attenuate, cultivate, and adapt other pathogens to cold temperatures in future studies.

A rapid and simple procedure for the whole-mount bone staining of small fish

ABSTRACT The cartilage and bone structure has provided insightful knowledge about evolution and ecology of fish, which is an important component of biological oceanography. However, the whole-body bone staining is a lengthy and complicated process that typically takes five days to several months, and the improvement of the conventional method has been one of the important issues in this field. Here we report a quick and easy whole-mount bone staining method for small fish, in which a newly designed fixative is applied. Compared to conventional methods, this novel protocol is a straightforward process that could be adopted for small estuarine fish and other small vertebrates.

The origins of gas exchange and ion regulation in fish gills: evidence from structure and function.

Gill function in gas exchange and ion regulation has played key roles in the evolution of fishes. In this review, we summarize data from the fields of palaeontology, developmental biology and comparative physiology for when and how the gills first acquired these functions. Data from across disciplines strongly supports a stem vertebrate origin for gas exchange structures and function at the gills with the emergence of larger, more active fishes. However, the recent discovery of putative ionocytes in extant cephalochordates and hemichordates suggests that ion regulation at gills might have originated much earlier than gas exchange, perhaps in the ciliated pharyngeal arches in the last common ancestor of deuterostomes. We hypothesize that the ancestral form of ion regulation served a filter-feeding function in the ciliated pharyngeal arches, and was later coopted in vertebrates to regulate extracellular ion and acid-base balance. We propose that future research should explore ionocyte homology and function across extant deuterostomes to test this hypothesis and others in order to determine the ancestral origins of ion regulation in fish gills.

Whole genome assembly and annotation of the King Angelfish (Holacanthus passer) gives insight into the evolution of marine fishes of the Tropical Eastern Pacific.

Holacanthus angelfishes are some of the most iconic marine fishes of the Tropical Eastern Pacific (TEP). However, very limited genomic resources currently exist for the genus. In this study we: (i) assembled and annotated the nuclear genome of the King Angelfish (Holacanthus passer), and (ii) examined the demographic history of H. passer in the TEP. We generated 43.8 Gb of ONT and 97.3 Gb Illumina reads representing 75× and 167× coverage, respectively. The final genome assembly size was 583 Mb with a contig N50 of 5.7 Mb, which captured 97.5% of the complete Actinoterygii Benchmarking Universal Single-Copy Orthologs (BUSCOs). Repetitive elements accounted for 5.09% of the genome, and 33,889 protein-coding genes were predicted, of which 22,984 were functionally annotated. Our demographic analysis suggests that population expansions of H. passer occurred prior to the last glacial maximum (LGM) and were more likely shaped by events associated with the closure of the Isthmus of Panama. This result is surprising, given that most rapid population expansions in both freshwater and marine organisms have been reported to occur globally after the LGM. Overall, this annotated genome assembly provides a novel molecular resource to study the evolution of Holacanthus angelfishes, while facilitating research into local adaptation, speciation, and introgression in marine fishes.

Convergent and environmentally associated chromatic polymorphism in Bryconops Kner, 1858 (Ostariophysi: Characiformes: Iguanodectidae).

Bryconops Kner, 1858, includes two well defined subgenera based on morphological evidence, with each containing at least one species (B. (Bryconops) caudomaculatus and B. (Creatochanes) melanurus) with a very wide distribution, within which regional populations present color variations. To test if phenotypic variation is related to cladogenetic events, we performed tests for phylogenetic independence and determined the strength of convergence for color characters in relation to water type, as the variation between clear, black and white waters is considered to be one of the major driving forces in the evolution of Amazonian fishes. Color characters for fins above the median line of the body were generally found to be independent from phylogeny and the Wheatsheaf test strongly supports convergence of the dorsal fin color between populations of species in the same type of water, with a similar trend suggested for the color of the dorsal lobe of the caudal fin. This means that simple color characters cannot necessarily be relied upon for taxonomic revisions of the genus as local phenotypic variants may represent environmentally determined plasticity or convergent evolution. Further studies are required to determine the validity of these characters.

Upstream experience and experimental translocation of invasive bigheaded carps results in increased upstream passage success at a navigation lock in a large river

AbstractFish movements in regulated rivers can be challenging to study because anthropogenic modifications, such as locks and dams, can influence animal behavior. Upper Mississippi River Lock and Dam 19 (LD 19), for example, is an invasive carp movement bottleneck due to an impassable dam. Upstream fish passage at LD19 is restricted to the lock chamber, making it an optimal location to test invasive fish deterrents that could limit further range expansion. Evaluating the effectiveness of experimental deterrents requires baseline knowledge of fish movements and suitable sample sizes of fish encountering the deterrents to ensure adequate statistical power. Some evidence indicates fish with prior upstream experience may return upstream or challenge potential deterrents at a higher rate than fish without such experience. To test how previous upstream experience could increase the rate at which fish moved upstream through a navigation lock chamber, we compared upstream passage through LD 19 using bigheaded carp captured below the dam (downstream‐origin) and two groups of bigheaded carp captured upstream from the dam: those that swam downstream on their own volition (upstream‐origin fish) and those that were captured upstream and translocated downstream of LD 19 (translocated upstream‐origin). Translocated upstream‐origin carp demonstrated the highest rate of upstream passage, with 59% of the fish detected downstream from LD 19 passing upstream during our study. In contrast, downstream‐origin carp made no upstream passages over 2 years. Fish origin was shown to influence upstream passage success. This may be an important consideration for fish passage studies and deterrent evaluations.

Characterization of fish-specific IFNγ-related binding with a unique receptor complex and signaling through a novel pathway.

Unlike mammals, fish express two type II interferons, IFNγ and fish-specific IFNγ (IFNγ-related or IFNγrel). We previously reported the presence of two IFNγrel genes, IFNγrel 1 and IFNγrel 2, which exhibit potent antiviral activity in the Ginbuna crucian carp, Carassius auratus langsdorfii. We also found that IFNγrel 1 increased allograft rejection; however, the IFNγrel 1 receptor(s) and signaling pathways underlying this process have not yet been elucidated. In this study, we examined the unique signaling mechanism of IFNγrel 1 and its receptors. The phosphorylation and transcriptional activation of STAT6 in response to recombinant Ginbuna IFNγrel 1 (rgIFNγrel 1) was observed in Ginbuna-derived cells. Binding of rgIFNγrel 1 to Class II cytokine receptor family members (Crfbs), Crfb5 and Crfb17, which are also known as IFNAR1 and IFNGR1-1, respectively, was detected by flow cytometry. Expression of the IFNγrel 1-inducible antiviral gene, Isg15, was highest in Crfb5- and Crfb17-overexpressing GTS9 cells. Dimerization of Crfb5 and Crfb17 was detected by chemical crosslinking. The results indicate that IFNγrel 1 activates Stat6 through an interaction with unique pairs of receptors, Crfb5 and Crfb17. Indeed, this cascade is distinct from not only that of IFNγ but also that of known IFNs in other vertebrates. IFNs may be classified by their receptor and signal transduction pathways. Taken together, IFNγrel 1 may be classified as a novel type of IFN family member in vertebrates. Our findings provide important information on interferon gene evolution in bony fish.

Complete mitochondrial genome of larged-eye pygmy goby Trimma macrophthalmus (Teleostei, Gobiidae) and its phylogenetic implications

Trimma macrophthalmus is a colorful pygmy goby that is widely associated with coral and distributed in the Indo-Pacific Ocean. Here, the complete mitochondrial genome of T. macrophthalmus was first sequenced and annotated. The entire mitogenome is a typical circular molecule (16,943 bp in total length) containing 13 protein-coding genes, 2 ribosomal RNA genes, 22 transfer RNA genes, and 1 control region (CR). The overall base composition is 29.6% for A, 15.6% for G, 27.9% for C and 26.9% for T. Phylogenetic tree was reconstructed using concatenated 13 protein coding genes sequences of the 38 related taxa. The phylogenetic analysis indicated that T. macrophthalmus was most closely related to T. okinawae. These findings will contribute for further genetic studies such as evolution, DNA barcoding and molecular phylogeny of genus Trimma and related gobiid fishes.

Using scale-derived estimates of body size in analyses of Atlantic salmon life-history variation: a cautionary note

Measurements of individual body length at different life stages are critical in understanding fish ecology and evolution. Such data can be obtained via back-calculation from measurements of fish scales or by using the size of the scale as a direct proxy for body length. Using data from Atlantic salmon, we test key assumptions associated with each approach and their implications for investigating how variation in growth earlier in life is associated with age at maturity. The scaling of scale size approximated isometry and was similar among individuals who matured at different ages—validating a key assumption of back-calculation. However, we observed that individuals genetically predisposed to delay maturation have smaller scales for their body size—challenging a key assumption of the “direct scale-size” approach. Depending on the method of body length estimation, the relationship between body length growth earlier in life and age at maturity was observed to differ. Thus, when using scale material to study the relationship between growth and maturation in salmon, we recommend back-calculation and an assumed allometric scaling coefficient.