Symposium Summary: Evolutionary Patterns in Actinopterygian Fishes

SYNOPSIS. The actinopterygian fishes are an exemplary cladefor the study of structural and functional evolutionary patterns.With over half of all vertebrate species, ray-finned fisheshave diversified into a wide variety of habitats, and considerableprogress has been made over the last fifteen years in understandingthe genealogical relationships of actinopterygians. This symposiumhas contributed to our understanding of phylogenetic patternsin actinopterygians and to knowledge of the major structuraland functional patterns in locomotor, auditory, trophic, andneural systems. A number of key areas for future research havebeen identified. (1) The relationships of "palaeonisciform"fishes, (2) the study of trends in feeding and locomotor systemswithin a phylogenetic context, (3) the identification of primitivepatterns of pharyngeal jaw movement and steady and unsteadylocomotor patterns in actinopterygians, (4) the homologies,identification, and functional significance of neural pathwaysin the telencephalon, and (5) the comparative study of form-functionrelations in the auditory system. The study of teleost fishbiology has proceeded at the expense of data on primitive actinopterygians(e.g., Polypterus, Polyodon, Aapenser, Lepisosteus, Amia) whichare especially important in the analysis of structural and functionalpatterns in ray-finned fishes.     

Development of the scales in Lepisosteus as a model for scale formation in fossil fishes

The living holostean fish Lepisosteus and the closely related Atractosteus offer a unique opportunity to study the development and homology of the ganoine-covered scales typical of early groups of actinopterygian fishes. Unlike the living chondrostean Polypterus , the scales of lepisosteids lack dentine and thus the role of the dentine, epidermis and mesodermal mesenchyme can be compared. Formation of the 'preganoine' is shown for the first time in Lepisosteus. Initial results show that in Lepisosteus ganoine is formed on the inner surface of a cell layer, apparently mesenchymal in origin, proliferating deep to the epidermal basement membrane. If this is correct ganoine in Lepisosteus is mesodermal and its formation has changed significantly from the pattern in the closely related fossil Semionotidae where dentine is present and is presumably involved in ganoine formation. The canals of Williamson in early fossil fishes were formed by migrating cells that played a major role in bone morphogenesis. The Lepisosteidae offer a unique opportunity to study these cells in a living vertebrate.     

Scale morphology of greater lizardfish Saurida tumbil (Bloch, 1795) (Pisces: Synodontidae)

A comparative study comprising scale morphology and squamation of Saurida tumbil was conducted to identify the most useful scale and squamation characters within the different body regions and length groups and to clarify their significance for future systematic studies. The presence of the caudal pores is documented for the first time in teleosts. In addition, the presence of crenae and spines formed by posterior orientation and projection of circuli is recorded for the first time in a member of the Synodontidae. Scales of S. tumbil show some characters that are either never seen or they are exceedingly rare in scales of other teleosts. These are: two types of scalar denticles, denticles in the inter-circular area, and twin or Siamese scales. Several other scale characters have shown a consistent variation in different body regions and in fishes from different length groups. These are: focus position; bilobate rostral field edge; presence of three radii; long, narrow and separated crenae; papillae-form, crowded scalar denticles with posterior directed spines; the number of scale rows between anterior end of the dorsal fin and the lateral line.     

The ultrastructure of the integument of the American eel,Anguilla rostrata

Summary The morphology and ultrastructure of the lateral body integument of the leptocephalus, glass eel, pigmented elver, and adult stages of the American eel, Anguilla rostrata, were examined with light and electron microscopy. The integument consists of an epidermis separated by a basal lamina from the underlying dermis. Three cell types are present in the epidermis in all stages. Filament-containing cells, which are the principal structural cell type, are increasingly numerous at each stage. Mucous cells, which secrete the mucous that compose the mucous surface coat, are also more numerous in each subsequent stage and are more numerous in the anterior lateral body epidermis than in the posterior lateral body epidermis of the adult. Club cells, whose function is unknown, are most numerous in the glass eel and pigmented elver. Chloride cells are common in the leptocephalus which is marine and infrequent in the glass eel. They are not present in the pigmented elver and adult which inhabit estuaries and fresh-water. Lymphocytes and melanocytes are also present in some stages. The dermis comprises two layers: a layer of collagenous lamellae, the stratum compactum, and an underlying layer of loose connective tissue, the stratum spongiosum.There is a progressive increase in epidermal thickness at each stage which is paralleled by an increase in the thickness of the stratum compactum. Rudimentary scales are present in the dermis of the adult. The increase in the number of epidermal filament-containing cells, epidermal thickness and stratum compactum thickness is correlated with an increased need for protection from abrasion and mechanical damage as the eel moves from a pelagic, oceanic habitat to a benthic, freshwater habitat. The increase in mucous cell numbers is likewise correlated with an increased need for the protective and anti-bacterial action of the mucous surface coat in the freshwater environment.This investigation was supported by NIH research grant NS-11276 from National Institute of Neurological Diseases and Stroke to Dr. J.D. McCleave and by N.S.F. Grant GD 38933 to the Bermuda Biological Station, St. Georges West, Bermuda. Bermuda Biological Station Contribution No. 668     

Ausgangsform und Entwicklung der rhombischen Schuppen der Osteichthyes (Pisces)

Ganoid and cosmoid scales, the two types of rhombic scales within the osteichthyans, can be traced back to a primitive scale similar to the scales ofLophosteus. The primitive rhombic scale did not have a peg-and-socket articulation, it is composed of lamellar bone superposed by many layers of spongy bone + dentine. That kind of superposition of layers of spongy bone + dentine (+ enamel) has been retained in the cosmoid scale; in contrast in the ganoid scale the growth of the dentine has become restricted to the lateral surface, the growth of ganoin to the outer surface and the growth of bone to the inner surface of the scale. The scales ofAndreolepis have a position between the primitive rhombic scale and the ganoid scale. — Scales from the Gedinnian (Lower Devonian) of New Sibirian Islands, USSR, are described asDialipina markae n. sp. The morphological features are very typical for the genus, but the histology is different from the type speciesD. salgueiroensis. Within the two Devonian palaeoniscoid generaDialipina andOrvikuina acellular bone with irregular non-vascular canals of Williamson has developed twice from cellular bone.     

Fossils and Strata

Jessen, H. L.: Schultergürtel und Pectoralflosse hci Actinopterygiern. [Shoulder girdle and pectoral fin in actinopterygians.] Fossils and Strata , Number 1, pp. 1–101, Pls. 1–25. Oslo, 5th May 1972.
The anatomy of the shoulder girdle and pectoral fin is investigated in adults and larvae of Asperser, Amia, Lepisosteus, Elops, Salmo , and Polypterus . In comparison with similar structures in other gnathostomian fishes these studies yielded certain conclusions as concerns the interrelationships of the recent actinopterygian groups and the affinities of the hrachiopterygians, the latter by this evidence belonging to an evolutionary line of their own. With regard to actinopterygian phylogeny, a comparison with the shoulder girdle and pectoral fin in fossil forms, including Chondrosteus, Moythomoasia, Palaeoniscus, Pteronisculus, Pachycormus, Catarus, Hypsocormus , and Birzeria , shows that teleosteans presumably are closer to chondrosteans than holosteans, and that holosteans seem to have branched off comparatively early from the actinopterygian stem.     

Scales and Dermal Skeletal Histology of an Early Bony Fish Psarolepis romeri and Their Bearing on the Evolution of Rhombic Scales and Hard Tissues

Recent discoveries of early bony fishes from the Silurian and earliest Devonian of South China (e.g. Psarolepis, Achoania, Meemannia, Styloichthys and Guiyu) have been crucial in understanding the origin and early diversification of the osteichthyans (bony fishes and tetrapods). All these early fishes, except Guiyu, have their dermal skeletal surface punctured by relatively large pore openings. However, among these early fishes little is known about scale morphology and dermal skeletal histology. Here we report new data about the scales and dermal skeletal histology of Psarolepis romeri, a taxon with important implications for studying the phylogeny of early gnathostomes and early osteichthyans. Seven subtypes of rhombic scales with similar histological composition and surface sculpture are referred to Psarolepis romeri. They are generally thick and show a faint antero-dorsal process and a broad peg-and-socket structure. In contrast to previously reported rhombic scales of osteichthyans, these scales bear a neck between crown and base as in acanthodian scales. Histologically, the crown is composed of several generations of odontodes and an irregular canal system connecting cylindrical pore cavities. Younger odontodes are deposited on older ones both superpositionally and areally. The bony tissues forming the keel of the scale are shown to be lamellar bone with plywood-like structure, whereas the other parts of the base are composed of pseudo-lamellar bone with parallel collagen fibers. The unique tissue combination in the keel (i.e., extrinsic Sharpey''s fibers orthogonal to the intrinsic orthogonal sets of collagen fibers) has rarely been reported in the keel of other rhombic scales. The new data provide insights into the early evolution of rhombic (ganoid and cosmoid) scales in osteichthyans, and add to our knowledge of hard tissues of early vertebrates.     

Mechanical design of polypterid fish integument for energy storage during recoil aspiration

Polypterid fishes ventilate their lungs by recoil aspiration. Active exhalation compresses the bony scale jacket; inhalation occurs when the scale jacket recoils to its original shape. Exhalation and loading of the integument are powered by contraction of striated muscle in the lung walls. The integument of polypterid fishes consists of interlocking rhomboid scales held together by collagen fibre strands. The scales imbricate with bevelled edges, so that when the fish is at rest, its integument is circular in cross-section and the overlapping scale edges are parallel. During exhalation, the hemicircular shape of the ventral integument is deformed, and the scales rotate slightly. As the overlapping scale edges become non parallel, the scales act as tiny levers to stretch the collagen fibres between them. When the fish opens its glottis to inhale, the stretched collagen fibres return to their rest lengths and pull the scale jacket back into a circular shape, sucking air into the lungs. Thus, despite the deformation of the integument as a whole in compression, strain energy is stored in tensile elements.     

Functional aspects of the integument in polypterid fishes

The integument and the axial musculoskeletal system of fishes belonging to the family Polypteridae (Osteichthyes, Actinopterygii) are re-examined with the purpose of clarifying the mechanical functions of the squamation. The major integumentary axes of bone and collagen are laid down in such a pattern as to resist that deformation of the skin resulting from axial body torsion. This resistance will have the effect of reducing or preventing such torsion and maintaining the strictly transverse plane of locomotory undulations.     

Scales in young Polypterus senegalus are elasmoid: new phylogenetic implications

A component of the basal plate which has a plywood-like organization similar to that of the elasmoid scales of teleosts is described in the scales of Polypterus senegalus for the first time. The origin and development of this structure is studied in young (50-117 mm, standard length) and adult (225 and 240 mm) specimens using light and electron microscopy. In 50 mm fish, the scales are imbricated and composed mainly of a succession of orthogonal collagen layers forming a plywood-like structure, the isopedin. The outer surface of the scale is ornamented locally by irregular patches of collagenous material. The layers are not mineralized, whereas the superficial patches are well calcified. The isopedin thickens until it has 12-15 layers and then stops growing (88 mm fish). It mineralizes irregularly from its upper part, and two vascular regions, surrounded by woven-fibered osseous material, form on the outer and deeper surfaces of the isopedin. These regions thicken while the vascular canals close by centripetal deposition of parallel-fibered osseous tissue. The outer region is the superficial part of the mature scale (called here osteodentin), which is covered by the ganoine deposited by the epidermal cells. The deeper part constitutes the definitive basal plate, composed of parallel-fibered osseous tissue. The results show 1) that the young ganoid scales of Polypterus senegalus have a structure similar to that of typical elasmoid scales; and 2) that the isopedin structure does not change during ontogeny and so represents a permanent record of the first ontogenetic stages. The phylogenetic implication of these results is that the elasmoid scales of teleosts arose by a process of paedomorphosis.     

Comparative squamation of the lateral line canal pores in sharks

The current study collected the first quantitative data on lateral line pore squamation patterns in sharks and assessed whether divergent squamation patterns are similar to experimental models that cause reduction in boundary layer turbulence. In addition, the hypothesis that divergent orientation angles are exclusively found in fast‐swimming shark species was tested. The posterior lateral line and supraorbital lateral line pore squamation of the fast‐swimming pelagic shortfin mako shark Isurus oxyrinchus and the slow‐swimming epi‐benthic spiny dogfish shark Squalus acanthias was examined. Pore scale morphology and pore coverage were qualitatively analysed and compared. In addition, pore squamation orientation patterns were quantified for four regions along the posterior lateral line and compared for both species. Isurus oxyrinchus possessed consistent pore scale coverage among sampled regions and had a divergent squamation pattern with multiple scale rows directed dorsally and ventrally away from the anterior margin of the pore with an average divergent angle of 13° for the first row of scales. Squalus acanthias possessed variable amounts of scale coverage among the sampled regions and had a divergent squamation pattern with multiple scale rows directed ventrally away from the anterior margin of the pore with an average angle of 19° for the first row of scales. Overall, the squamation pattern measured in I. oxyrinchus fell within the parameters used in the fluid flow analysis, which suggests that this pattern may reduce boundary layer turbulence and affect lateral line sensitivity. The exclusively ventral oriented scale pattern seen in S. acanthias possessed a high degree of divergence but the pattern did not match that of the fluid flow models. Given current knowledge, it is unclear how this would affect boundary layer flow. By studying the relationship between squamation patterns and the lateral line, new insights are provided into sensory biology that warrant future investigation due to the implications for the ecology, morphology and sensory evolution of sharks.     

The musculotendinous system of an anguilliform swimmer: Muscles, myosepta, dermis, and their interconnections in Anguilla rostrata

Eel locomotion is considered typical of the anguilliform swimming mode of elongate fishes and has received substantial attention from various perspectives such as swimming kinematics, hydrodynamics, muscle physiology, and computational modeling. In contrast to the extensive knowledge of swimming mechanics, there is limited knowledge of the internal body morphology, including the body components that contribute to this function. In this study, we conduct a morphological analysis of the collagenous connective tissue system, i.e., the myosepta and skin, and of the red muscle fibers that sustain steady swimming, focusing on the interconnections between these systems, such as the muscle-tendon and myosepta-skin connections. Our aim is twofold: (1) to identify the morphological features that distinguish this anguilliform swimmer from subcarangiform and carangiform swimmers, and (2) to reveal possible pathways of muscular force transmission by the connective tissue in eels. To detect gradual morphological changes along the trunk we investigated anterior (0.4L), midbody (0.6L), and posterior body positions (0.75L) using microdissections, histology, and three-dimensional reconstructions. We find that eel myosepta have a mediolaterally oriented tendon in each the epaxial and hypaxial regions (epineural or epipleural tendon) and two longitudinally oriented tendons (myorhabdoid and lateral). The latter two are relatively short (4.5-5% of body length) and remain uniform along a rostrocaudal gradient. The skin and its connections were additionally analyzed using scanning electron microscopy (SEM). The stratum compactum of the dermis consists of approximately 30 layers of highly ordered collagen fibers of alternating caudodorsal and caudoventral direction, with fiber angles of 60.51 +/- 7.05 degrees (n = 30) and 57.58 +/- 6.92 degrees (n = 30), respectively. Myosepta insert into the collagenous dermis via fiber bundles that pass through the loose connective tissue of the stratum spongiosum of the dermis and either weave into the layers of the stratum compactum (weaving fiber bundles) or traverse the stratum compactum (transverse fiber bundles). These fiber bundles are evenly distributed along the insertion line of the myoseptum. Red muscles insert into lateral and myorhabdoid myoseptal tendons but not into the horizontal septum or dermis. Thus, red muscle forces might be distributed along these tendons but will only be delivered indirectly into the dermis and horizontal septum. The myosepta-dermis connections, however, appear to be too slack for efficient force transmission and collagenous connections between the myosepta and the horizontal septum are at obtuse angles, a morphology that appears inadequate for efficient force transmission. Though the main modes of undulatory locomotion (anguilliform, subcarangiform, and carangiform) have recently been shown to be very similar with respect to their midline kinematics, we are able to distinguish two morphological classes with respect to the shape and tendon architecture of myosepta. Eels are similar to subcarangiform swimmers (e.g., trout) but are substantially different from carangiform swimmers (e.g., mackerel). This information, in addition to data from kinematic and hydrodynamic studies of swimming, shows that features other than midline kinematics (e.g., wake patterns, muscle activation patterns, and morphology) might be better for describing the different swimming modes of fishes.     

Lateral line scale types and review of their taxonomic distribution

The trunk canal of fishes is contained within a series of lateral line (LL) scales. To categorise LL scale structural types, and determine their distribution, an analysis of original data was undertaken using light and scanning electron microscopy in combination with a literature survey from over 1,000 species representative of most orders of bony fishes. Our categorisation of LL scales is based on the relationship between the tube, or ossified trunk canal segment, and associated scale. Tubular‐Scalar LL scales consist of a distinguishable tube and elasmoid scale in scale pockets. Four types occur only in species with elasmoid scales. Integrated LL scales do not develop in scale pockets, and their tube is enclosed or extended by a non‐elasmoid scale or spines. Integrated 1 and 2 LL scales co‐occur with ganoid and calcidermoid scales, and Integrated 3 LL scales occur when common scales are absent or elasmoid. Tubular LL scales are tubes only, occurring mainly in scaleless species or with calcidermoid and elasmoid scales. Non‐Tubular LL scales are composed only of a scale, co‐occurring mainly with cycloid scales. There is consistency of LL scale type in many orders, families and genera and the presence of different types within taxa can be meaningful.     

Ontogenetic causes and mechanisms for formation of differences in number of fish scales

Fish squamation is developed in late ontogeny. Therefore, the conditions of development significantly affect its characteristics (number of scales). This study is aimed at considering the influence of external and internal factors on variation of the number of scales in fish. Acceleration of development results in decrease of the number of scales, while it increases with retardation. Experiments on regulation of thyroid status of fish showed that the certain mechanism of alteration of the number of scales is related with heterochrony, such as a shift of the timing of squamation. Accelerated development is caused by early scale development at smaller body length, while retarded development is characterized with later scale development and at greater body length. Data considering heterochrony as the possible reason for differences in the number of scales in related fish species are represented. Moreover, alterations of the distance between scales (morphogenetic count) can serve as another alteration mechanism of the number of scales in fish (especially phyletically distant species).     

Proprioceptive endings in the myotomes of the pickerel (Teleostei: Esocidae)

Simple spray nerve endings of axons with a large diameter (15 μm) were located in the stratum compactum overlying the myotomal muscles in the pickerels, Esox niger and E. americanus . Based on the location of these nerve endings within the interwoven collagenous fibre matrix comprising the stratum compactum, and on the lack of reactivity to cholinesterase treatment, it is suggested that the endings are sensory in function and may be used as proprioceptors. These putative proprioceptors may aid the pickerel in monitoring the position of the body, (1) during ambush prey capture where the pickerel must lie motionless with as little disturbance in the water column as possible, and (2) in counteracting unwanted hydrodynamic forces such as pitch or roll brought about by sudden stopping of forward movement immediately following prey capture. This is the first report of proprioceptive endings associated with locomotor musculature in teleost fishes.     

Biosynthesis of ascorbic acid by extant actinopterygians

Polypterus senegalus , the longnose gar Lepisosteus osseus and the bowfin Amia calva had gulonolactone oxidase activity in the kidney and thus can synthesize ascorbic acid de novo . The enzyme activity was associated with the microsomal fraction. The common carp Cyprinus carpio and the goldfish Carassius auratus had no gulonolactone oxidase activity. Antibodies directed against white sturgeon gulonolactone oxidase showed cross-reactivity with lake sturgeon, bowfin and longnose gar kidney enzymes, but not with enzymes from Polypterus , sea lamprey, and tadpole kidney or pig liver. Given cross-reactivity, gulonolactone oxidase relatedness matched actinopterygian phylogeny, and suggested homology of the character throughout fishes. Modern teleosts may have lost the ability to synthesize ascorbic acid since the late Triassic as a result of a single reversal in the founding population. Wild bowfin and longnose gar exhibited high ascorbate concentrations in liver and spleen when compared with the teleosts rainbow trout Oncorhynchus mykiss and common carp fed vitamin C-supplemented diets.     

Unusual intraindividual variation of the nuclear 18S rRNA gene is widespread within the Acipenseridae

Significant intraindividual variation in the sequence of the 18S rRNA gene is unusual in animal genomes. In a previous study, multiple 18S rRNA gene sequences were observed within individuals of eight species of sturgeon from North America but not in the North American paddlefish, Polyodon spathula, in two species of Polypterus (Polypterus delhezi and Polypterus senegalus), in other primitive fishes (Erpetoichthys calabaricus, Lepisosteus osseus, Amia calva) or in a lungfish (Protopterus sp.). These observations led to the hypothesis that this unusual genetic characteristic arose within the Acipenseriformes after the presumed divergence of the sturgeon and paddlefish families. In the present study, a survey of nearly all Eurasian acipenseriform species was conducted to examine 18S rDNA variation. Intraindividual variation was not found in the polyodontid species, the Chinese paddlefish, Psephurus gladius, but variation was detected in all Eurasian acipenserid species. The comparison of sequences from two major segments of the 18S rRNA gene and identification of sites where insertion/deletion events have occurred are placed in the context of evolutionary relationships within the Acipenseriformes and the evolution of rDNA variation in this group.     

Development of the paired fins in the paddlefish, Polyodon spathula

In Polyodon spathula, the pectoral fin radials, with the exception of the metapterygium, are derived from the decomposition of a single continuous cartilage fin plate that is continuous with the scapulocoracoid. This cartilage sheet develops two interior splits to form three precursor pieces, and these decompose in a predictable way to generate the propterygium and radials. The metapterygium is an extension of the scapulocoracoid that segments off of it during early development. To our knowledge, this has not been reported for acipenserids or other basal actinopterygians. In teleosts, the proximal radials also develop from the "break up" of an initially continuous paddle-like sheet of cartilage along the posterior edge of the scapulocoracoid, and in Polypterus and sharks a similar pattern holds. Thus, the pattern observed in Polyodon may represent the basal developmental condition for the gnathostome pectoral fin. The process underlying development of the superficially similar cartilages of the pelvic and pectoral fins is different. In the pectoral fin, the metapterygium is segmented off of the scapulocoracoid and other radials form from the decomposition of the cartilage plate. In contrast, individual rod-like basipterygial elements form in a close one-to-one correspondence with the middle radials of the pelvic fin, but later fuse to form an anterior element that is branched in appearance. To evaluate further claims of similarity among the pectoral and pelvic fin elements of various fishes, the course of the development of these structures must be observed. The pectoral fin and girdle in Polyodon ossifies in a different sequence than that proposed as ancestral (and highly conserved) for actinopterygians: the supracleithrum ossifies significantly before the cleithrum. The later ossification of the cleithrum in Polyodon may be related to the primary use of the caudal fin vs. the pectoral fins in their locomotion.     

Preliminary molecular phylogeny of the fishes based on sequence analysis of 28S ribosomal RNA

"Fish" phylogeny has been studied using partial 28 S ribosomal RNA sequences of 14 species among which 12 are "fish" ranging from lamprey to perciforms. Our results are in good agreement with generally accepted cladograms based on anatomical and paleontological data. Two interesting conclusions emerged: a) Polypterus is the sister-group of all other actinopterygians; b) the divergences of the Clasdistia, Tetrapoda and Chondrichthyes seem to have occurred during a relatively short period of time.