Electroreception in early vertebrates: survey,evidence and new information

Electroreception is widespread in living vertebrates, and is often considered to be a primitive vertebrate character. However, the early evolution of electroreception remains unclear. A variety of structures in early vertebrate fossils have been put forward as potential electroreceptors, but these need to be reassessed in light of the now substantial literature on electroreceptors in living vertebrates. Here we review the evidence for all putative electroreceptors in early vertebrates, and provide new information from CT scans. In the jawless osteostracans, the pore canal system in the dermal skeleton and the lateral and dorsal fields do not resemble electroreceptors in living species. Nevertheless, the presence of a recurrent ramus of the anterior lateral line nerve in osteostracans suggests that electroreceptors were present, by comparison with lampreys. In placoderms, cutaneous sense organs on arthrodire cheek plates are possible electroreceptors. CT data shows that the orientation of these pits is anomalous for electroreceptors, and intimately associated with bone growth. A newly identified type of cheek pit, for which the term ‘Young's apparatus’ is introduced, is known from only two arthrodire specimens. It is closely associated with the underlying jaw joint, but its precise function is unknown. In osteichthyans, the ‘pore group’ clusters of early sarcopterygians may have housed electroreceptors. CT data from Devonian lungfish support this interpretation, showing internal morphology consistent with electroreceptors, and innervation via the rostral tubuli underlying the dermal bone of the snout. The early osteichthyan Ligulalepis has pit structures which may be electroreceptors, and were possibly innervated by lateral line nerves. Specialized electroreceptor systems, including elaborated ‘pore group’ pits in Devonian lungfish and rostral organs in the earliest coelacanths, show that electroreception may have had an important role in niche specialization in early vertebrates. Finally, fossil data does not support the hypothesis that vertebrate hard tissues initially evolved to shield electroreceptors.     

Skin structure in the snout of the Australian lungfish,Neoceratodus forsteri (Osteichthyes: Dipnoi)

Many fossil lungfish have a system of mineralised tubules in the dermis of the snout, branching extensively and radiating towards the epidermis. The tubules anastomose in the superficial layer of the dermis, forming a plexus consisting of two layers of vessels, with branches that expand into pore canals and flask organs, flanked by cosmine nodules where these are present. Traces of this system are found in the Australian lungfish, Neoceratodus forsteri, consisting of branching tubules in the dermis, a double plexus below the epidermis and dermal papillae entering the epidermis without reaching the surface. In N. forsteri, the tubules, the plexus and the dermal papillae consist of thick, unmineralised connective tissue, enclosing fine blood vessels packed with lymphocytes. Tissues in the epidermis and the dermis of N. forsteri are not associated with deposits of calcium, which is below detectable limits in the skin of the snout at all stages of the life cycle. Canals of the sensory line system, with mechanoreceptors, are separate from the tubules, the plexus and the dermal papillae, as are the electroreceptors in the epidermis. The system of tubules, plexus, dermal papillae and lymphatic capillaries may function to protect the tissues of the snout from infection.     

The Latero-sensory Component of the Dermal Skeleton in Lower Vertebrates and Its Phyletic Significance

Ørvig, T. (Section of Palaeozoology, Swedish Museum of Natural History, Stockholm, Sweden.) The latero-sensory component of the dermal skeleton in lower vertebrates and its phyletic significance. Zool. Scripta 1(3–4): 139–155, 1972.–A latero-sensory component of the dermal skeleton is met with not only in teleostomian fishes, but also in arthrodires, holocephalians (the lateral line canal “rings”), some fossil selachians, bradyodonts and acanthodians, and a few, at least, of the Osteostraci. Although not yet traceable with certainty in the Heterostraci, such a component probably existed even in early stages of vertebrate history. The persistence in the adult of this component as separate ossicles embracing the lateral line canals is surely the result of regression or other modifications of the dermal skeleton in fishes like arthrodires, coelacanthids and actinopterygians, but is apparently a primitive feature in e.g. acanthodians. In discussing the phyletic relations between the latero-sensory and membranous components of the dermal skeleton, it is concluded that these probably were separate formations from the very beginning. A condition (exemplified by certain acanthodians) where separate latero-sensory ossicles of the lateral line canals are surrounded by a mosaic of small scales of membranous origin is presumably that from which the various dermal bone-patterns in lower vertebrates are all derived. A discussion is also included in this paper of the scales and otoliths in acanthodians.     

Development of the supraorbital and mandibular lateral line canals in the cichlid,Archocentrus nigrofasciatus

The development of two of the cranial lateral line canals is described in the cichlid, Archocentrus nigrofasciatus. Four stages of canal morphogenesis are defined based on histological analysis of the supraorbital and mandibular canals. "Canal enclosure" and "canal ossification" are defined as two discrete stages in lateral line canal development, which differ in duration, an observation that has interesting implications for the ontogeny of lateral line function. Canal diameter in the vicinity of individual neuromasts begins to increase before ossification of the canal roof in each canal segment; this increase in canal diameter is accompanied by an increase in canal neuromast size. The mandibular canal generally develops later than the supraorbital canal in this species, but in both of these canals development of the different canal segments contained within a single dermal bone is asynchronous. These observations suggest that a dynamic process requiring integration and interaction among different tissues, in both space and time, underlies the development of the cranial lateral line canal system. The supraorbital and mandibular canals appear to demonstrate a "one-component" pattern of development in Archocentrus nigrofasciatus, where the walls of each canal segment grow up from the underlying dermal bone and then fuse to form the bony canal roof. This is contrary to numerous published reports that describe a "two-component" pattern of development in teleosts where the bony canal ossifies separately and then fuses with an underlying dermal bone. A survey of the literature in which lateral line canal development is described using histological analysis suggests that the occurrence of two different patterns of canal morphogenesis ("one-component" and "two-component") may be due to phylogenetic variation in the pattern of the development of the lateral line canals.     

Morphology of the mechanosensory lateral line system in the Atlantic Stingray,Dasyatissabina: The mechanotactile hypothesis

The biological function of anatomical specializations in the mechanosensory lateral line of elasmobranch fishes is essentially unknown. The gross and histological features of the lateral line in the Atlantic stingray, Dasyatis sabina, were examined with special reference to its role in the localization and capture of natural invertebrate prey. Superficial neuromasts are arranged in bilateral rows near the dorsal midline from the spiracle to the posterior body disk and in a lateral position along the entire length of the tail. All dorsal lateral line canals are pored, contain sensory neuromasts, and have accessory lateral tubules that most likely function to increase their receptive field. The pored ventral canal system consists of the lateral hyomandibular canal along the disk margin and the short, separate mandibular canal on the lower jaw. The extensive nonpored and relatively compliant ventral infraorbital, supraorbital, and medial hyomandibular canals form a continuous complex on the snout, around the mouth, and along the abdomen. Vesicles of Savi are small mechanosensory subdermal pouches that occur in bilateral rows only along the ventral midline of the rostrum. Superficial neuromasts are best positioned to detect water movements along the transverse body axis such as those produced by tidal currents, conspecifics, or predators. The pored dorsal canal system is positioned to detect water movements created by conspecifics, predators, or possibly distortions in the flow field during swimming. Based upon the stingray lateral line morphology and feeding behavior, we propose the Mechanotactile Hypothesis, which states that the ventral nonpored canals and vesicles of Savi function as specialized tactile mechanoreceptors that facilitate the detection and capture of small benthic invertebrate prey. J. Morphol. 238:1–22, 1998. © 1998 Wiley-Liss, Inc.     

The origin of novel features by changes in developmental mechanisms: ontogeny and three‐dimensional microanatomy of polyodontode scales of two early osteichthyans

Recent advances in synchrotron imaging allow us to study the three‐dimensional (3D) histology of vertebrate fossils, including microfossils (e.g. teeth and scales) of early jawed vertebrates. These microfossils can often be scanned at submicron resolution (<1 µm) because of their small size. The resulting voxel (3D pixel) stacks can be processed into virtual thin sections revealing almost every internal detail of the samples, comparable to traditional thin sections. In addition, 3D models of the internal microanatomical structures, such as embedded odontodes and vasculature, can be assembled and examined in situ. Scales of two early osteichthyans, Psarolepis romeri from the Early Devonian of China and Andreolepis hedei from the Late Silurian of Sweden, were scanned using propagation phase‐contrast synchrotron X‐ray microtomography (PPC‐SRµCT), and 3D models of internal canal systems and buried odontodes were created from the scans. Based on these new data, we review the evolutionary origin of cosmine and its associated pore‐canal system, which has been long recognized as a synapomorphy of sarcopterygians. The first odontode that appeared during growth shows almost identical morphology in the two scales, but the second odontode of the Psarolepis scale shows a distinctive morphology with several pores on the surface. It is suggested that a shift from ridge‐like odontode to pore‐bearing odontode was the key step in the origin of cosmine, which was then elaborated further in more‐derived sarcopterygians. We perform a detailed comparison between the two scales and propose a primary homology framework to generate microanatomical characters, which can be used in the phylogenetic analysis of early osteichthyans when more 3D data become available. Our results highlight the importance of 3D data for the study of histology and ontogeny of the dermal skeleton of early jawed vertebrates, especially scales of the polyodontode type. The traditional microvertebrate collection is not only useful for biostratigraphic studies, but also preserves invaluable biological information about the growth of vertebrate hard tissues. Today, we are only beginning to understand the biological meaning of the new 3D data. The increasing availability of such data will enable, and indeed require, a complete revision of traditional palaeohistological studies on early vertebrates.     

杨氏鱼(Youngolepis)吻部网状骨质管的研究

本文描述了我国云南曲靖早泥盆世总鳍鱼——杨氏鱼(Youngolepis sp.)吻部网状骨质小管管壁电镜结构、元素成分、整个系统的分支状况以及它与膜质骨、侧线系统的关系,推测其功能是为吻部神经和血管提供通道.文中认为杨氏鱼与肺鱼共同具有 rostral tubuli 这一特征;将杨氏鱼吻部神经分支与骨鳞鱼、孔鳞鱼、肺鱼及两栖类进行了比较,指出杨氏鱼的眼浅支分支进入鼻囊这一特点.     

Morphology and development of the multiple lateral line canals on the trunk in two species of Hexagrammos (Scorpaeniformes,Hexagrammidae)

The morphology and development of the multiple lateral line canals (canals 1–5 in dorsal to ventral sequence) on the trunk of two representative hexagrammids, Hexagrammos decagrammus and H. stelleri, were studied using histological and cleared and stained material. The morphology of the lateral line scales of which the lateral line canals are composed and the distribution of canal neuromasts within them were described quantitatively. We hypothesized that 1) one neuromast is contained in each lateral line scale and all five canals contain neuromasts, 2) all five canals develop similarly, and 3) the multiple trunk canals are an adaptation for the alteration of lateral line function. Lateral line scale morphology was found to be similar among the five canals in Hexagrammos decagrammus and H. stelleri. However, canal 3 is significantly wider than the other four canals. It is the only one of the five canals connected to the canals on the head, and more significantly, it is the only one of the five canals that contains neuromasts. The lateral line scales that comprise all five lateral line canals show the same pattern of development whether or not they contain neuromasts. The five canals develop asynchronously, and each of the canals develops either rostro-caudally or caudo-rostrally. Canal 3 is the homologue of a single trunk canal in other teleosts; canals 1, 2, 4, and 5 are apomorphic features of the two species of Hexagrammos. Canals 1, 2, 4, and 5 cannot be functional components of the lateral line system because they do not contain neuromasts and thus cannot be adaptations for the alteration of lateral line function. The occurrence of lateral line canals lacking neuromasts demands a direct assessment of neuromast distributions in the lateral line canals among fishes. Finally, our data suggest that the putative role of neuromasts in the morphogenesis of lateral line canals and the nature of neuromast-bone relationships need to be critically reevaluated. J. Morphol. 233:195–214, 1997. © 1997 Wiley-Liss, Inc.     

Osteocranial development in the viviparous surfperch Amphistichus argenteus (pisces: Embiotocidae)

The development of the cranial and branchial skeleton of the surfperch Amphistichus argenteus, a member of the family Embiotocidae, is described, and phylogenetic and functional aspects of the skull development of this species are discussed. The earliest bones to appear are those dermal elements of the branchial skeleton involved with feeding, and the bones, both dermal and endochondral, located in the basicranial region of the neurocranium. These are followed by dermal bones associated with the lateral line system and finally by the remainder of the bones of the branchial skeleton and the cartilaginous bones of the otic capsules. The last bone to develop is the ethmoid.     

Ultrastructure of free neuromasts of Bathygobius fuscus (gobiidae) and canal neuromasts of Apogon cyanosoma (apogonidae)

Light and electron microscopic observations were made on the lateral line organs of the free neuromasts of the goby Bathygobius fuscus and the canal neuromasts of the cardinal fish Apogon cyanosoma. As in other lateral line systems, each neuromast consists of hair cells, supporting cells and mantle supporting cells, the whole being covered by a cupula. In B. fuscus the free neuromasts are mounted on papillae and have hair cells with stereocilia up to 2.5 μm long and a single kinocilium at least 25 μm long. Each neuromast is covered by a vane-like cupula that can be divided into two regions. The central region over the sensory area contains columns of myelin-like figures. These figures are absent from the outer region covering the mantle. The canal neuromasts of A. cyanosoma are diamond-shaped with up to 1,500 hair cells. The cupula is unusual in having a channel that lies over the sensory region. The hair cells have up to 45 stereocilia, the tallest reaching 2.5 μm, and a kinocilium at least 5 μm long. Tip links are shown for the first time between rows of stereocilia of the hair cells of lateral line neuromasts. The presence of tip links has now been demonstrated for all acousticolateral hair cell systems.     

Morphology of the teleost ampullary organs in marine salmontail catfish Neoarius graeffei (Pisces: Ariidae) with comparative analysis to freshwater and estuarine conspecifics

We hypothesized that due to the relative conductivity of the environment, and to maintain sensory function, ampullary organs of marine Neoarius graeffei would differ morphologically from those described previously for estuarine and freshwater conspecifics. Unlike the ampullary systems of N. graeffei from freshwater and estuarine habitats, the ampullary pores of marine specimens occur in two distinct patterns; numerous pores seemingly randomly scattered on the head and ventro‐lateral regions of the body, and pores arranged in distinctive vertical lines above the lateral line on the dorso‐lateral body of the fish. Light and electron microscopy revealed that the ampullary organs also differed morphologically from estuarine and freshwater specimens in the presence of longer ampullary canals, a hitherto unreported canal wall composition, and in the collagen sheath surrounding both the canal and the ampulla proper within dermal connective tissues. Ampullary pores were wider in marine individuals and opened to the longest ampullary canals reported for this species. The canal wall was lined by cuboidal and squamous epithelial cells. Each ampullary canal opened into a single ampulla proper containing significantly more receptor cells than estuarine and freshwater conspecifics. The distribution of ampullary pores as well as the microstructure of the ampullary organs indicates that the electrosensory system of marine N. graeffei differs from those of estuarine and freshwater specimens in ways that would be expected to maintain the functionality of the system in a highly conductive, fully marine environment, and reveals the remarkable plasticity of this species’ ampullary system in response to habitat conductivity. J. Morphol. 276:1047–1054, 2015. © 2015 Wiley Periodicals, Inc.     

A new species of the genus Mekongina Fowler, 1937 (Cypriniformes: Cyprinidae) from South China

A new species of cyprinid fish, Mekongina lancangensis, is described from the upper Mekong River drainage in Southern Yunnan, China. The new species is distinguished from the other species of Mekongina occurring in the lower Mekong River drainage by possessing the following combination of characters: one pair of rostral barbels; two rows of tubercles irregularly scattered on the snout and cheeks, with two enlarged tubercles present at each side of anterior of the snout; 19–27 rostral marginal lappets; lateral line with 38–41 scales; 5·5 or 6·5 scales in transverse series from dorsal‐fin origin to lateral line; 18–20 circumpeduncular scales; snout length 31·9–36·9% head length; tip of depressed anal‐fin rays extending to the caudal‐fin base.     

Morphology and ontogeny of multiple lateral‐line canals in the rock prickleback,Xiphister mucosus (Cottiformes: Zoarcoidei: Stichaeidae)

The structure and ontogeny of lateral‐line canals in the Rock Prickleback, Xiphister mucosus, were studied using cleared‐and‐stained specimens, and the distribution and morphology of neuromasts within lateral‐line canals were examined using histology. X. mucosus has seven cephalic canals in a pattern that, aside from four branches of the infraorbital canals, is similar to that of most teleostean fishes. Unlike most other teleosts, however, X. mucosus features multiple trunk lateral‐line canals. These include a short median posterior extension of the supratemporal canal and three paired, branching canals located on the dorsolateral, mediolateral, and ventrolateral surfaces. The ventrolateral canal (VLC) includes a loop across the ventral surface of the abdomen. All trunk canals, as well as the branches of the infraorbitals, are supported by small, dermal, ring‐like ossifications that develop independently from scales. Trunk canals develop asynchronously with the mediodorsal and dorsolateral canals (DLC) developing earliest, followed by the VLC, and, finally, by the mediolateral canal (MLC). Only the mediodorsal and DLC connect to the cephalic sensory canals. Fractal analysis shows that the complexity of the trunk lateral‐line canals stabilizes when all trunk canals develop and begin to branch. Histological sections show that neuromasts are present in all cephalic canals and in the DLC and MLC of the trunk. However, no neuromasts were identified in the VLC or its abdominal loop. The VLC cannot, therefore, directly function as a part of the mechanosensory system in X. mucosus. The evolution and functional role of multiple lateral‐line canals are discussed. J. Morphol. 276:1218–1229, 2015. © 2015 Wiley Periodicals, Inc.     

Cephalic lateral line systems in the Far Eastern species of the genus Phoxinus (Cyprinidae)

The cephalic lateral line systems of seven Far Eastern Phoxinus species (P. phoxinus, P. kumgangensis, P. semotilus, P. lagowskii, P. oxycephalus, P. perenurus, and P. czekanowskii) were investigated. In this genus, the infraorbital canal is not connected with either the supraorbital canal or the preoperculomandibular canal. Phoxinus phoxinus is unique for having an underdeveloped condition, such as canal formation or remaining as uncovered. A unified supraorbital canal was observed in all species, but the infraorbital canal of both P. perenurus and P. czekanowskii was not unified into a single canal throughout their development. Unification between both sides of the supratemporal canal occurred in larger individuals of P. lagowskii, P. oxycephalus, and P. czekanowskii. The preoperculomandibular canal of P. kumgangensis, large P. lagowskii, and large P. oxycephalus was unified. The pore number of each part of the canal system also varied depending on the species. Intraspecific variations were observed between Korean and Japanese specimens of P. lagowskii in the unification of the supratemporal canal and the preoperculomandibular canal, and the number of pores of the supratemporal canal. It was inferred that the specific characteristic patterns of their cephalic lateral line systems reflected the following two factors: different environmental requirement for their microhabitat and different maximum body size.     

The trigeminofacial innervation of the cephalic lateral line organs and photophores of the lantern fish Tarletonbeania crenularis (Myctophidae)

The trigeminofacial innervation of the cephalic photophores and lateral line organs of Tarletonbeania crenularis has been studied from gross dissections. The facial and trigeminal roots leave the brainstem separately, but later intermingle forming a trigemino‐facial complex. The seventh nerve gives rise to the hyomandibular trunk and sends a branch rostrad to join the trigeminal forming the supra‐ and infraorbital trunks. The supraorbital trunk innervates the Dn photophore, the snout, the iris, the supraorbital lateral line organs and part of the olfactory sacs. The infraorbital trunk supplies the infraorbital lateral line organs, the Vn photophore and the tissues surrounding the premaxillaries. The hyomandibular trunk passes to the opercular photophores and lateral line organs, and together with a branch from the infraorbital trunk supplies the branchiostegal photophores and lateral line organs of the mandible.     

The lateral line system in larvalIchthyophis (Amphibia: Gymnophiona)

Summary The lateral line systems of larval caecilians of the genusIchthyophis possess two types of elements, free neuromasts and ampullary organs. Free mechanoreceptive neuromasts are typical of those found in other vertebrates, and are arranged in series roughly homologous to neuromast groups in many other fishes and amphibians. In contrast to other amphibians,Ichthyophis larvae possess only one paired, dorsal body series of neuromasts. Regional specialization of neuromasts is evident inIchthyophis. Premaxillary and anterior head neuromasts are the largest in size and total cell number. Overall, size and total cell numbers are correlated with depth of epidermis. Neuromasts on the anterior sides of the head occur in slight grooves and have apical tips situated farther below the level of the epidermis and with greater apical indentation. These features probably provide increased protection against abrasion. Apparently abnormal neuromasts are frequently found among the neuromast series. Such neuromasts contain fewer cells that lack normal apical extension, producing a sunken effect similar to that of the ampullary organ elements. The ampullary organs ofIchthyophis are morphologically similar to those found in various freshwater fishes and known to function as electroreceptors. These organs are not observed in the lateral line systems of members of other amphibian orders (Urodela and Anura), and we suggest that they function as electroreceptors. The sunken neuromasts of theIchthyophis lateral line system may parallel the possible evolutionary development of pit organs from normal neuromasts.