Fin Skeleton Research Articles

Unexpected diversity of median caudal cartilages in teleosts

Caudal fin skeletons of teleost fishes have been well-studied in the context of phylogenetic relationships. However, the small cartilages at the distal end of the diastema, the ‘median caudal cartilages’, have gained only little attention so far. For the first time we here report their taxa-dependent variable three-dimensional structure. We investigated 143 species of 62 teleost families for this study. The shape and arrangement of these cartilages is uniform in some systematic groups, e.g. Alepocephalidae, Platytroctidae or Myctophiformes; in other taxa there is high intrataxon variability, e.g. Stomiiformes or Aulopiformes. Shape, number and presence/absence may even vary in certain species, e.g. Osmerus eperlanus, Thymallus thymallus or Gymnocorymbus ternetzi. The function of median caudal cartilages remains unclear. It has been suggested that they might be related to fin-ray support, although an obvious relation to fin rays is lacking in several taxa. Their presence and size is not dependent on the size of the diastema. Median caudal cartilages seem to have evolved at the base of clupeocephalans and occur in many taxa up to about aulopiforms, as well as single beryciforms. It seems that they are often reduced at different systematic levels and may have re-evolved in some taxa.

Skeletal development in the heterocercal caudal fin of spotted gar (lepisosteus oculatus) and other lepisosteiformes.

The caudal fin of actinopterygians experienced substantial morphological changes during evolution. In basal actinopterygians, the caudal fin skeleton supports an asymmetrical heterocercal caudal fin, while most teleosts have a symmetrical homocercal caudal fin. The transition from the ancestral heterocercal form to the derived homocercal caudal fin remains poorly understood. Few developmental studies provide an understanding of derived and ancestral characters among basal actinopterygians. To fill this gap, we examined the development of the caudal fin of spotted gar Lepisosteus oculatus, one of only eight living species of Holostei, the sister group to the teleosts. Our observations of animals from fertilization to more than a year old provide the most detailed description of the development of caudal fin skeletal elements in any Holostean species. We observed two different types of distal caudal radials replacing two transient plates of connective tissue, identifying two hypaxial ensembles separated by a space between hypurals 2 and 3. These features have not been described in any gar species, but can be observed in other gar species, and thus represent anatomical structures common to lepisosteiformes. The present work highlights the power and importance of ontogenic studies and provides bases for future evolutionary and morphological investigations on actinopterygians fins. Developmental Dynamics 247:724-740, 2018. © 2018 Wiley Periodicals, Inc.

Bioinspiration From Flexible Propulsors: Organismal Design, Mechanical Properties, Kinematics and Neurobiology of Pectoral Fins in Labrid Fishes

AbstractLabrid fishes use their pectoral fins for efficient high-speed cruising behavior, as well as for precision maneuvering in complex environments, making them good models for biomimicry applications in propulsor technology for aquatic vehicles. Lift-based labriform locomotion is a form of aquatic flight used by many species and is the sole mode of transport across most speeds by some of the largest wrasses and parrotfishes on coral reefs. Although basic and applied research has explored fin design in several species utilizing labriform propulsion, a detailed analysis of fin anatomy, fin mechanical properties, and well-resolved three-dimensional (3D) kinematics in high-performance aquatic flyers has not yet been attained. Here, we present recent research on fin structure, fin flexural stiffness, sensory abilities of fins, and a novel 3D approach to flexible fin kinematics. Our aims are to outline important future directions for this field and to assist engineers attempting biomimicry of maneuverable fin-based locomotion for applications in robotics. First, we illustrate the anatomical structure and branching patterns of the pectoral fin skeleton and the muscles that drive fin motion. Second, we present data on the flexural stiffness of pectoral fins in the parrotfish (Scarus quoyi), setting up a stiffness field that gives the fin propulsor its passive mechanical properties and enables hydrodynamically advantageous fin deformations during swimming. Third, we present 3D reconstructions of the kinematics of high-performanceScarusfins that greatly enhance our ability to reproduce fin motions for engineering applications and also yield insight into the functional role of the fin stiffness field. Lastly, recent work on mechanosensation is illustrated as key to understanding sensorimotor control of labriform locomotion. Research on pectoral fin structure, function, and neural control in large marine species with high-performance wing-like fins is important to the comparative biology of locomotion in fishes, and we suggest it is a productive area of research on fin function for applications in the design of quiet, efficient propulsors.

Dynamics of actinotrichia regeneration in the adult zebrafish fin

The skeleton of adult zebrafish fins comprises lepidotrichia, which are dermal bones of the rays, and actinotrichia, which are non-mineralized spicules at the distal margin of the appendage. Little is known about the regenerative dynamics of the actinotrichia-specific structural proteins called Actinodins. Here, we used immunofluorescence analysis to determine the contribution of two paralogous Actinodin proteins, And1/2, in regenerating fins. Both proteins were detected in the secretory organelles in the mesenchymal cells of the blastema, but only And1 was detected in the epithelial cells of the wound epithelium. The analysis of whole mount fins throughout the entire regenerative process and longitudinal sections revealed that And1-positive fibers are complementary to the lepidotrichia. The analysis of another longfin fish, a gain-of-function mutation in the potassium channel kcnk5b, revealed that the long-fin phenotype is associated with an extended size of actinotrichia during homeostasis and regeneration. Finally, we investigated the role of several signaling pathways in actinotrichia formation and maintenance. This revealed that the pulse-inhibition of either TGFβ/Activin-βA or FGF are sufficient to impair deposition of Actinodin during regeneration. Thus, the dynamic turnover of Actinodin during fin regeneration is regulated by multiple factors, including the osteoblasts, growth rate in a potassium channel mutant, and instructive signaling networks between the epithelium and the blastema of the regenerating fin.

Development of the axial, paired and unpaired fin skeleton in three species of Patagonian zoarcids

Zoarcids are abundant in the intertidal zone of the Argentine Patagonian coast. However, their osteological development has not yet been described. Thus, the aim of this work is to describe the ontogeny of the axial skeleton and that of the paired and unpaired fins of the zoarcids Iluocoetes elongatus, Phucocoetes latitans and Dadyanos insignis. The three species studied showed a high degree of development at hatching and meristic counts coincide with those of the adults. At hatching, most of the structures showed that the appearance of bones was in progress. In the three species studied, this process occurred in a cephalo-caudal direction and, in most of the structures, the appearance of bones is observed from the middle to the rim.

Comparative osteology of the family Tripterygiidae (Teleostei: Blenniiformes)

This paper presents the results of a comparative study of five osteological complexes, the infraorbital bones, branchial arches, urohyal bone, interdigitation of the median fins, and the caudal fin skeleton, of some members of the fish family Tripterygiidae. Osteological characters that may prove valuable for taxonomic purposes are described, and on the basis of the material handled, their use to separate species within the family is discussed. Several formulae were developed for the distribution of the osteological complexes of the dorsal fin, dorsal and ventral caudal procurrent ray distribution, and caudal fin in the different tripterygiid species studied.

Structure and mechanical implications of the pectoral fin skeleton in the Longnose Skate (Chondrichthyes, Batoidea).

Batoid fishes have very light cartilaginous skeletons that facilitate their elegant swimming by applying their enlarged wing-like pectoral fins. Previous studies have shown structural features and mechanical properties of the mineralized cartilage skeleton in various batoid fishes. However, the details of the pectoral fin structure at different length scales, as well as the relationship between the mechanical properties and structural design remains unknown. The present work illustrates the hierarchical structure of the pectoral fin of the Longnose Skate (a representative batoid fish) and verifies the materials configuration and structural design increases the stiffness of fin skeleton without a loss in flexibility. These results have implications for the design of strong but flexible materials and bio-inspired autonomous underwater vehicles (AUVs).

An integrative approach to reappraising species validity in Pseudexostoma (Teleostei: Sisoridae).

The catfish genus Pseudexostoma (Sisoridae) currently contains three species: P. yunnanensis from the upper Irrawaddy River (Dayingjiang), and P. brachysoma and P. longipterus from the upper Salween River (Nujiang). We adopted an integrative approach combining both morphology-based (traditional measurements, truss-based and geometric morphometrics, fin skeleton examination and X-ray photography) and molecular approaches (genetic distances, haplotype network, phylogenetic relationships) to reappraise species validity in Pseudexostoma. Our results showed that P. longipterus cannot be distinguished from P. brachysoma from either morphological or molecular analyses, and that the former name should thus be considered a junior synonym of the latter. The two remaining geographically isolated species, P. yunnanensis and P. brachysoma, showed a distinct genetic distance equated to the typical 2% sequence divergence threshold delineating different species of fishes, and with a divergence time dated to approximately 1.22-2.14 million years ago. Although P. yunnanensis and P. brachysoma share some morphological characters that appear gradually diverging (body depth at anus and interorbital distance), some degree of overlap still exists, we suggest the two species are distinct based on the total evidence.

Digits and fin rays share common developmental histories.

Understanding the evolutionary transformation of fish fins into tetrapod limbs is a fundamental problem in biology. The search for antecedents of tetrapod digits in fish has remained controversial because the distal skeletons of limbs and fins differ structurally, developmentally, and histologically. Moreover, comparisons of fins with limbs have been limited by a relative paucity of data on the cellular and molecular processes underlying the development of the fin skeleton. Here, we provide a functional analysis, using CRISPR/Cas9 and fate mapping, of 5' hox genes and enhancers in zebrafish that are indispensable for the development of the wrists and digits of tetrapods. We show that cells marked by the activity of an autopodial hoxa13 enhancer exclusively form elements of the fin fold, including the osteoblasts of the dermal rays. In hox13 knockout fish, we find that a marked reduction and loss of fin rays is associated with an increased number of endochondral distal radials. These discoveries reveal a cellular and genetic connection between the fin rays of fish and the digits of tetrapods and suggest that digits originated via the transition of distal cellular fates.

Postembryonic staging of wild-type goldfish, with brief reference to skeletal systems.

Background: Artificial selection of postembryonic features is known to have established morphological variation in goldfish (Carassius auratus). Although previous studies have suggested that goldfish and zebrafish are almost directly comparable at the embryonic level, little is known at the postembryonic level. Results: Here, we categorized the postembryonic developmental process in the wild‐type goldfish into 11 different stages. We also report certain differences between the postembryonic developmental processes of goldfish and zebrafish, especially in the skeletal systems (scales and median fin skeletons), suggesting that postembryonic development underwent evolutionary divergence in these two teleost species. Conclusions: Our postembryonic staging system of wild‐type goldfish paves the way for careful and appropriate comparison with other teleost species. The staging system will also facilitate comparative ontogenic analyses between wild‐type and mutant goldfish strains, allowing us to closely study the relationship between artificial selection and molecular developmental mechanisms in vertebrates. Developmental Dynamics 244:1485–1518, 2015. © 2015 Wiley Periodicals, Inc.

Collagen duplicate genes of bone and cartilage participate during regeneration of zebrafish fin skeleton

The zebrafish fin is widely used as a model for skeleton regeneration. For years, the nature of the fin skeleton has been controversial as its extracellular matrix shows hybrid characteristics of both bone and cartilage. The presence of co-orthologs genes also increases the complexity of these tissues. In this article, we have identified and described the expression of fibrillar collagens in zebrafish fin skeleton. We found that genes coding for types I, II, V, XI and XXVII collagens are duplicated, showing in several cases, different expression domains. We also identified specific genomic features, such as the presence of type XXIV collagen and the absence of type III collagen in the zebrafish genome. Our study showed that actinotrichia-forming cells and osteoblasts synthesize a wide variety of these fibrillar collagens during fin regeneration. An intertrichial domain expressing most of the collagens was located in the transition between the mesenchyme condensations of actinotrichia and lepidotrichia and may determine an important niche associated with fin skeleton morphogenesis. We also confirmed the hybrid nature of the fin exoskeleton and provided a complete description of those fibrillar collagens expressed during the formation of the fin skeleton.

The origin of a new fin skeleton through tinkering.

Adipose fins are positioned between the dorsal and caudal fins of many teleost fishes and primitively lack skeleton. In at least four lineages, adipose fins have evolved lepidotrichia (bony fin rays), co-opting the developmental programme for the dermal skeleton of other fins into this new territory. Here I provide, to my knowledge, the first description of lepidotrichia development in an adipose fin, characterizing the ontogeny of the redtail catfish, Phractocephalus hemioliopterus. Development of these fin rays differs from canonical lepidotrich development in the following four ways: skeleton begins developing in adults, not in larvae; rays begin developing at the fin's distal tip, not proximally; the order in which rays ossify is variable, not fixed; and lepidotrichia appear to grow both proximally and distally, not exclusively proximodistally. Lepidotrichia are often wavy, of irregular thickness and exhibit no regular pattern of segmentation or branching. This skeleton is among the most variable observed in a vertebrate appendage, offering a unique opportunity to explore the basis of hypervariation, which is generally assumed to reflect an absence of function. I argue that this variation reflects a lack of canalization as compared with other, more ancient lepidotrichs and suggest developmental context can affect the morphology of serial homologues.

The Hapln1a‐ECM Influences Sema3d Signal Transduction During Fin Regeneration

The zebrafish regenerating fin is an important model system to understand skeletal morphogenesis, the process of how the skeleton achieves its appropriate size and shape. The fin skeleton is comprised of multiple bony fin rays where each fin ray is comprised of bony segments separated by joints. Our research on the short fin (sof) mutant revealed that the gap junction protein Connexin43 (Cx43) coordinates bone growth and skeletal patterning. Downstream mediators of Cx43 function include the secreted signaling molecule Semaphorin3d (Sema3d) and the link protein Hyaluronan and Proteoglycan Link Protein 1a (Hapln1a). Hapln1a stabilizes the hyaluronan (HA) and proteoglycan network in the extracellular matrix (ECM). We suggest that components of the Hapln1a ECM, including HA and the proteoglycan Aggrecan (Acan), influence the ability of Sema3d to interact with its cell surface receptors to mediate cell proliferation and joint formation. Indeed, knockdown of Hapln1a destabilizes HA, Acan, and strikingly, Sema3d. Thus, HA and/or Acan may be required for the presentation of Sema3d to its receptors. Moreover, we find that hapln1a and sema3d interact genetically, suggesting that the Hapln1a and Sema3d gene products function in common pathways to coordinate skeletal growth and patterning. These findings provide the first evidence that the Hapln1a-ECM regulates Sema3d signal transduction in vivo. Moreover, these findings reveal tangible connections between the Hapln1a-ECM, signal transduction, and skeletal morphogenesis. This research was supported by the NSF.

Asymmetric cell convergence-driven zebrafish fin bud initiation and pre-pattern requires Tbx5a control of a mesenchymal Fgf signal.

Tbx5 plays a pivotal role in vertebrate forelimb initiation, and loss-of-function experiments result in deformed or absent forelimbs in all taxa studied to date. Combining single-cell fate mapping and three-dimensional cell tracking in the zebrafish, we describe a Tbx5a-dependent cell convergence pattern that is both asymmetric and topological within the fin-field lateral plate mesoderm during early fin bud initiation. We further demonstrate that a mesodermal Fgf24 convergence cue controlled by Tbx5a underlies this asymmetric convergent motility. Partial reduction in Tbx5a or Fgf24 levels disrupts the normal fin-field cell motility gradient and results in anteriorly biased perturbations of fin-field cell convergence and truncations in the pectoral fin skeleton, resembling aspects of the forelimb skeletal defects that define individuals with Holt-Oram syndrome. This study provides a quantitative reference model for fin-field cell motility during vertebrate fin bud initiation and suggests that a pre-pattern of anteroposterior fate specification is already present in the fin-field before or during migration because perturbations to these early cell movements result in the alteration of specific fates.

Early Development of the Caudal Fin Skeleton of Capelin,Mallotus villosus(Osmeridae)

Development of the caudal fin skeleton of capelin, Mallotus villosus, is described based on observations of cleared-and-stained specimens from a wild caught growth series ranging in size from 4.2 mm notochord length (NL) to 144 mm standard length (SL). The sequence of chondrification and ossification for each element is described and compared with that of related salmonoid and esocoid fishes. Caudal fin elements are first chondrified in specimens that are 8.9 mm NL and all elements are ossified by 52 mm SL. In general, hypaxial elements (e.g., parhypural, hypurals, hemal arches and spines of preural vertebrae) develop before epaxial elements (e.g., epurals, uroneurals, neural arches and spines of preural vertebrae). Preural centra are among the last elements to form in the caudal skeleton of M. villosus. Interestingly, preural centrum 1 does not form. The caudal fin skeleton morphology of adult M. villosus is nearly identical to that of other osmerid species, and the developmental sequence of the caudal s...

The humerus of Eusthenopteron: a puzzling organization presaging the establishment of tetrapod limb bone marrow.

Because of its close relationship to tetrapods, Eusthenopteron is an important taxon for understanding the establishment of the tetrapod body plan. Notably, it is one of the earliest sarcopterygians in which the humerus of the pectoral fin skeleton is preserved. The microanatomical and histological organization of this humerus provides important data for understanding the evolutionary steps that built up the distinctive architecture of tetrapod limb bones. Previous histological studies showed that Eusthenopteron's long-bone organization was established through typical tetrapod ossification modalities. Based on a three-dimensional reconstruction of the inner microstructure of Eusthenopteron's humerus, obtained from propagation phase-contrast X-ray synchrotron microtomography, we are now able to show that, despite ossification mechanisms and growth patterns similar to those of tetrapods, it also retains plesiomorphic characters such as a large medullary cavity, partly resulting from the perichondral ossification around a large cartilaginous bud as in actinopterygians. It also exhibits a distinctive tubular organization of bone-marrow processes. The connection between these processes and epiphyseal structures highlights their close functional relationship, suggesting that either bone marrow played a crucial role in the long-bone elongation processes or that trabecular bone resulting from the erosion of hypertrophied cartilage created a microenvironment for haematopoietic stem cell niches.

Four new basal acanthomorph fishes from the Late Cretaceous of Morocco

ABSTRACT Four new species of acanthomorph fishes are described, and three are named, from the Agoult locality of Morocco, which samples early Late Cretaceous marine deposits of the Akrabou Formation. Of the three new named species, two represent members of the subfamily Aipichthyoidea, based on possession of a caudal fin skeleton with a short, broad, neural spine on the second preural centrum, 19 principal caudal fin rays, and three supraneurals positioned close together in front of the first neural spine. The third named species is placed in the Polymixiiformes based on having a caudal fin with a long, full neural spine on the second preural centrum, and 18 principal caudal fin rays. The fourth species is too poorly preserved to name, but we describe the few details that are visible, and it remains incertae sedis within Acanthomorpha. These new taxa add to the diversity of morphologies seen in both the aipichthyoids and the polymixiiforms during the Cenomanian and Turonian throughout the Tethys Sea.

Morphogenetic effects of vitamin A on the regenerating tail fin of the teleost fish, Oreochromis niloticus

The present study was performed to investigate the effects of vitamin A (VA) on tail fin regeneration of the teleost fish, Oreochromis niloticus. Following amputation, the tail fin undergoes a regenerative process which leads to an apparently faithful replacement, both in shape and size of the missing part. However, analysis of the fin skeleton of whole mount preparations of normal (unamputated), control, and treated tail fins revealed that, fin regenerates were not perfect copies of the missing part, and that the distance and the number of ray segments between the amputation plane and the first dichotomy were higher in treated tail fins than in control and unamputated fins. This suggests that VA can affect patterning formation of the regenerating tail fin. Vitamin A has morphogenetic effects on the regenerating fin by increasing the number of ray segments as well as it exhibits a marked reduction in the amount of tissue between rays that leads to fusion of adjacent rays.

The Medaka zic1/zic4 Mutant Provides Molecular Insights into Teleost Caudal Fin Evolution

Teleosts have an asymmetrical caudal fin skeleton formed by the upward bending of the caudal-most portion of the body axis, the ural region. This homocercal type of caudal fin ensures powerful and complex locomotion and is regarded as one of the most important innovations for teleosts during adaptive radiation in an aquatic environment. However, the mechanisms that create asymmetric caudal fin remain largely unknown. The spontaneous medaka (teleost fish) mutant, Double anal fin (Da), exhibits a unique symmetrical caudal skeleton that resembles the diphycercal type seen in Polypterus and Coelacanth. We performed a detailed analysis of the Da mutant to obtain molecular insight into caudal fin morphogenesis. We first demonstrate that a large transposon, inserted into the enhancer region of the zic1 and zic4 genes (zic1/zic4) in Da, is associated with the mesoderm-specific loss of their transcription. We then show that zic1/zic4 are strongly expressed in the dorsal part of the ural mesenchyme and thereby induce asymmetric caudal fin development in wild-type embryos, whereas their expression is lost in Da. Comparative analysis further indicates that the dorsal mesoderm expression of zic1/zic4 is conserved in teleosts, highlighting the crucial role of zic1/zic4 in caudal fin morphogenesis.

The mechanism of cartilage subdivision in the reorganization of the zebrafish pectoral fin endoskeleton

A cartilaginous pectoral fin endoskeleton in zebrafish (Danio rerio) develops early, after which the cartilage of the larval fin endoskeleton undergoes a complete transformation into the adult morphology. This transformation includes multiple subdivisions of a single cartilaginous disk. The type of cartilage subdivision is unique to teleost fish. In this study, we present the timing and the developmental features of these subdivisions and we discuss variation in this process, caused by differences in growth rate. We establish that the cartilage subdivisions are developmentally linked to the formation of lepidotrichia in the fin fold. At the cellular level, we show that neither apoptosis nor resorption by chondroclasts and/or macrophages contributes to the cartilage subdivision. Ultrastructural observations show dedifferentiation of chondrocytes in subdivision zones. Different from forelimb development in other vertebrates, dedifferentiation is an important mechanism in the development of the adult pectoral fin skeleton. We here provide further support for the idea that the phenotype of skeletal tissues is not terminal and that plasticity of differentiated connective tissues can play an important role in various developmental and homeostatic processes.