The evolution of the amphibian lateral line system and its bearing on amphibian phylogeny

In modern amphibians that are aquatic the lateral line system is organized, by order, as follows: caecilians have electroreceptive ampullary organs and single rows of mechanoreceptive neuromast organs; generalized anurans have single rows of neuromasts that divide in a transverse plane to form secondary neuromasts or stitches, they do not have ampullary organs; generalized urodeles have ampullary organs, transverse stitches, and double or triple rows of neuromasts. Fossil evidence indicates that early amphibians had both ampullary organs and single rows of neuromasts embedded in bone. With time, receptors became epidermal in all three orders. Modern caecilians have retained the primitive receptor arrangement. I propose that the common ancestor of anurans and urodeles had transverse stitches, and that this character allies these two groups. Subsequent to the anuranurodele split, anurans lost their ampullary organs, perhaps concomitant with developing specializations for herbivory. Urodeles developed orthogonal neuromast couplets und triplets. In modern anurans und urodeles, transverse stitches are correlated with pond dwelling, while ampullary organs are correlated with carnivory, suggesting that the anuran-urodele ancestor(s) was a (were) pond-dwelling carnivore(s).     

中国大鲵侧线器官的研究

本文以光镜和扫描是镜手段研究了中国大鲵幼体，亚成体及成体头部及躯干部表皮中的侧线器官，即电接受壶腹器官，机械接受的表面神经丘和陷器官的分布，形态和发展变化。壶腹器管仅存于幼体头部，变态结束后消失，后两种终生存在，但前者按一定路线和方向排列，后者仅存于头部，陷在表皮中，文章探讨了壶腹器官的原始性，其消失与生活习性以及由水登陆进化的关系；对三种器官的形态及其它有尾类的侧线器官进行了比较。     

The evolution of electroreception and bioelectrogenesis in teleost fish: a phylogenetic perspective

According to current phylogenetic theory, both electroreceptors and electric organs evolved multiple times throughout the evolution of teleosts. Two basic types of electroreceptors have been described: ampullary and tuberous electroreceptors. Ampullary‐type electroreceptors appeared once in the common ancestor of the Siluriformes+Gymnotiformes (within the superorder Ostariophysi), and on two other occasions within the superorder Osteoglossomorpha: in the African Mormyriformes and in the African Notopteriformes. Tuberous receptors are assumed to have evolved three times; all within groups that already possessed ampullary receptors. With the exception of a single catfish species, for which studies are still lacking, all fish with tuberous electroreceptors also have an electric organ. Tuberous electroreceptors are found in the two unrelated electrogenic teleost lineages (orders Gymnotiformes and Mormyriformes) and in one non‐electrogenic South American catfish species (order Siluriformes). Electric organs evolved eight times independently among teleosts: five of them among the ostariophysans (once in the gymnotiform ancestor and in four siluriform lineages), once in the common ancestor of Mormyriformes, and in two uranoscopids. With the exception of two uranoscopid genera, for which no electroreceptive capabilities have been discovered so far, all electric organs evolved as an extension of a pre‐existing electroreceptive (ampullary) condition. It is suggested that plesiomorphic electric organ discharges (EODs) possessed a frequency spectrum that fully transgressed the tuning curve of ampullary receptors, i.e. a signal such as a long lasting monophasic pulse. Complex EOD waveforms appeared as a derived condition among electric fish. EODs are under constant evolutionary pressure to develop an ideal compromise between a function that enhances electrolocation and electrocommunication capabilities, and thereby ensures species identity through sexual and behavioural segregation, and minimizes the risk of predation.     

Pit organs in axolotls: a second class of lateral line neuromasts

The lateral line system of axolotls (Ambystoma mexicanum) consists of mechanoreceptive neuromasts and electroreceptive ampullary organs. All neuromasts in salamanders are located superficially and are organized into lines that are homologous to canal neuromasts in fishes. Ampullary organs are confined to the head and generally are located adjacent to the lines of superficial neuromasts. Axolotls, however, also possess a third class of receptors; these form restricted patches on the head and are possibly homologous to the superficial pit organs in fishes. In order to test this hypothesis the morphology of the suspected pit organs was examined with scanning electron microscopy, and a number of their physiological properties were determined. Pit organs are approximately half the size of neuromasts and have fewer hair cells, although these hair cells do possess kinocilia and stereocilia like those of neuromasts. Pit organs also possess cupulae and exhibit a pattern of innervation identical to that of neuromasts. Pit organs and neuromasts also exhibit similar rates of spontaneous activity, are excited by weak water currents but not weak electric stimuli, and are not inhibited by magnesium ions. Pit organs appear to have slightly lower rates of spontaneous discharge than neuromasts, however, and have slightly lower displacement thresholds to low frequency wave stimuli. These data support the contention that the pit organs of axolotls constitute a second class of neuromasts homologous to the pit organs of fishes.     

The fine structure of the lateral-line organs of larval Ichthyophis (Amphibia: Gymnophiona)

Light and electron microscopic observations of the lateral-line organs of larval Ichthyophis kohtaoensis confirmed earlier reports of the occurrence of two different types of lateral-line organs. One type, the ampullary organ, possesses 15–26 egg-shaped sensory cells. Each sensory cell extends a single kinocilium surrounded by a few microvilli into the ampullary lumen. This is in contrast to the ampullary organs of urodele amphibians that contain only microvilli. The second type of organ, the ordinary neuromast, has 15–24 pear-shaped sensory cells arranged in two to three rows. Each sensory cell shows a kinocilium that is asymmetrically placed with respect to both a basal plate and approximately 60 stereovilli. The sensory cells of ampullary organs are always separated by supporting cells; those of neuromasts are occasionally in contact with one another. Numerous (neuromasts) or few (ampullary organs) mantle cells separate the organs from the epidermal cells. Only afferent synapses are found in the ampullary organs whereas vesicle-filled fibers together with afferent nerve terminals are found in neuromasts. Both organs contain similarly sized presynaptic spheres adjacent to the afferent fibers. It is suggested that the neuromasts have a mechanoreceptive function, whereas the ampullary organs have an electroreceptive one.     

The organization of ampullary sense organs in the electric fish, Gymnarchus niloticus

Three types (A, B, and C) of ampullary sense organs occur in the skin of Gymnarchus niloticus. In type A the ampulla is connected to the surface of the skin by an open duct whereas in B and C organs it is closed, though overlain by specialized epidermal cells. In each case the receptor cell surface in contact with the ampullary lumen bears microvilli; these are more highly developed in B and C organs than in type A. Fine structural observations are consistent with the view that the organs are electric receptors of three different types.     

Fine Structure of the Ampullary Organs of the Bichir Polypterus senegalus Cuvier, 1829 (Pisces: Brachiopterygii) With Some Notes on the Phylogenetic Development of Electroreceptors

The ampullary organs of the bichir were examined by light and electron microscopy. Unlike most other ampullary organs, they are exclusively found in the epidermis and are never sunk into the subepidermal connective tissue. The sensory epithelium consists of sensory cells and supporting cells surrounded by mantle cells. The luminal surface of the sensory cell is provided with a cilium surrounded by several microvilli. In the apical cytoplasm are found numerous mitochondria and microtubules. In the basal part of the cell synaptic sheets or synaptic bodies opposite to afferent nerve endings are frequent.     

Fine structure and immunocytochemistry of a new chemosensory system in the Chiton larva (Mollusca: Polyplacophora).

Combined electron microscopy and immunocytochemistry of the larvae of several polyplacophoran species (Chiton olivaceus, Lepidochitona aff. corrugata, Mopalia muscosa) revealed a sensory system new to science, a so-called "ampullary system." The cells of the "ampullary system" are arranged in four symmetrically situated pairs lying dorsolaterally and ventrolaterally in the pretrochal part of the trochophore-like larva and they send axons into the cerebral commissure. They are lost at metamorphosis. The fine structure of these cells strongly resembles that of so-called "ampullary cells" known from various sensory organs of other molluscs, such as the apical complex of gastropod and bivalve larvae, osphradia of vetigastropods, and olfactory organs of cephalopods, and nuchal organs of certain polychaetes. The ampullary cells and their nerves are densely stained by anti-FMRF-amide fluorescence dyes, whereas antiserotonin staining is only weak. While cytological homology of the ampullary cells with those of other organs is probable, the ampullary system as a whole is regarded as a synapomorphy of the Polyplacophora or Chitonida.     

The amphibian octavo-lateralis system and its regressive and progressive evolution

The phylogenetic and ontogenetic changes in the octavolateralis system of sarcopterygian fish and tetrapods, presumed to be important for the formation of an amphibian auditory system, are reviewed. The lateral line system shows rudimentation of lines and loss of ampullary electroreceptors in many amphibians; in some amphibians it never develops. The metamorphic changes of the lateral-line system show different patterns in the different amphibian lineages with metamorphic retention in most urodeles and metamorphic loss in most anurans. The multitude of both ontogenetic and phylogenetic changes of the lateral line system among amphibians do exclude any prediction as to how this system might have changed in ancestral amniotes. The most important auditory epithelium of the tetrapod inner ear, the basilar papilla, seems to be primitively present in all tetrapods and Latimeria. In two amphibian lineages there is a trend towards rudimentation and loss of the basilar papilla. Only in the third order, the anurans, a tympanic ear develops and the inner ear shows a progressive evolution of the auditory epithelia. Together with the known differences in the periotic labyrinth of amphibians and amniotes, this scenario suggests a parallel evolution of the amniotic and anuran auditory periphery. All mechanoreceptive hair cells of the lateral line system and the inner ear appear to receive a common and bilateral efferent innervation. Among amphibians this pattern is represented only in some urodeles, whereas anurans show a derived pattern with loss of a bilateral component and presumably also of a common neuromast/inner ear component. Changes in the rhombencephalic nuclei which receive octavo-lateralis afferent fibers show a trend towards development of auditory nuclei only in the anuran lineage. The phylogenetic appearance of an auditory nucleus in this lineage coincides with the complete absence of formation of ampullary electroreceptors. In contrast, the earlier claim of a correlation between a metamorphic loss of the lateral line system and the formation of an auditory nucleus is not supported by more recent data: an auditory nucleus develops in anurans already prior to metamorphosis and is present in all anurans even when they retain the neuromast system. In anurans with a metamorphic loss of the neuromasts, the second order neurons degenerate as well. This independence of the auditory and the second order lateral line nuclei is further substantiated by their separate projection to other brain areas, like the torus semicircularis of the midbrain, and their functional properties.(ABSTRACT TRUNCATED AT 400 WORDS)     

On the ampullary organs of the South-American paddle-fish Sorubim lima (Siluroidea,Pimelodidae)

Summary Ampullary organs were found in the epidermis of the paddle-fish Sorubim lima; they are distributed all over the skin surface of the fish but are particularly densely grouped in the head region and on the dorsal surface of the paddle. Histological and electron microscopical observations show that their structure is similar to the type of cutaneous ampullary organs characteristic of other Siluroidea. Composed of a relatively large mucus-filled ampulla, the organ possesses a short and narrow canal which leads to the outer epidermal surface. The wall of the ampulla is formed of several layers of flat epidermal cells. In general four sensory cells, each one surrounded by supporting cells, compose the sensory epithelium at the bottom of the ampulla. The inner surface of the sensory cells in contact with the ampullary mucus bears only microvilli. The contact between the nerve endings and the sensory cells show the characteristic structure of an afferent neuro-sensory junction. Two ampullae are innervated in some cases by the same afferent nerve fibre.The author expresses her gratitude to Dr. Szabo for his scientific advice during her stay in Gif sur Yvette     

Morphological comparison of the ampullae of Lorenzini of three sympatric benthic rays

This study investigated and compared the morphology of the electrosensory system of three species of benthic rays. Neotrygon trigonoides, Hemitrygon fluviorum and Maculabatis toshi inhabit similar habitats within Moreton Bay, Queensland, Australia. Like all elasmobranchs, they possess the ability to detect weak electrical fields using their ampullae of Lorenzini. Macroscopically, the ampullary organs of all three species are aggregated in three bilaterally paired clusters: the mandibular, hyoid and superficial ophthalmic clusters. The hyoid and superficial ophthalmic clusters of ampullae arise from both dorsal and ventral ampullary pores. The dorsal pores are typically larger than the ventral pores in all three species, except for the posterior ventral pores of the hyoid grouping. Ampullary canals arising from the hyoid cluster possessed a quasi‐sinusoidal shape, but otherwise appeared similar to the canals described for other elasmobranchs. Ultrastructure of the ampullae of Lorenzini of the three species was studied using a combination of light, confocal and electron microscopy. All possess ampullae of the alveolar type. In N. trigonoides and M. toshi, each ampullary canal terminates in three to five sensory chambers, each comprising several alveoli lined with receptor and supportive cells and eight to 11 sensory chambers in H. fluviorum. Receptor cells of all three species possess a similar organization to those of other elasmobranchs and were enveloped by large, apically nucleated supportive cells protruding well into the alveolar sacs. The luminally extended chassis of supportive cells protruding dramatically into the ampullary lumen had not previously been documented for any elasmobranch species.     

Apically administered cytochalasin B and D decreases sensitivity of electroreceptor organs in the North-American catfish,Ictalurus nebulosus

The receptor cells of the ampullary electroreceptor organs of Ictalurus nebulosus bear microvilli on the apical membrane. Whereas microvilli in mechanoreceptive hair cells and in chemoreceptor cells have a transduction function, the function of these membrane specializations in electroreceptor cells is not fully understood. To study the role of the microvilli of the electroreceptor cells, the ampullary electroreceptor organs were apically exposed to the microfilament-disrupting agents cytochalasin B and D. Electrophysiological measurements showed that cytochalasin caused a high decrease in sensitivity and a slight decrease in spontaneous activity. Exposure to cytochalasin B resulted in a striking disorganization of the microvilli on the apical membrane of the electroreceptor cells. The most plausible explanation for the results is that treatment with cytochalasin mainly affects the actin filaments of the microvilli causing an increase of the resistance of the apical membrane. A high apical resistance results in a decrease of the voltage over the basal membrane, which in turn reduces the sensitivity. The conclusion is that intact apical microvilli are necessary for proper functioning of ampullary electroreceptor organs. Alterations in microvillar properties, like surface area and ion channel conductancy might play a considerable role in the regulation of the sensitivity.     

Comparative features of the surface morphology of the basilar papilla in five families of salamanders (Amphibia; Caudata)

The surface morphology of the basilar recess and papilla was examined in 14 species of newts and salamanders selected from the five families of urodeles (Ambystomatidae, Salamandridae, Hynobiidae, Cryptobranchidae, and Amphiumidae) known to have this end-organ. In this sampling, the general organization of basilar structures is essentially similar across species investigated. The recess forms a tubular diverticulum of the proximal part of the lagena. One wall of the recess is associated with a diverticulum of the intracapsular periotic sac, and an adjacent wall is occupied by the basilar papilla. The papilla contained from as few as five hair cells in specimens of Taricha torosa to over 200 hair cells in Cryptobranchus allegheniensis. In most species, the papilla showed a morphological continuum between tall centrally or distally placed ciliary bundles and short ciliary bundles near the papillar margins. In certain species examined, tall bundles had kinocilia with swellings near their tips. Most forms showed a tendency to have groups of ciliary bundles morphologically polarized either toward or away from the saccule. In Cryptobranchus and Dicamptodon, many bundles had a random orientation. The gross and fine structural features of the basilar complex are compared in urodeles and anurans, and "generalized" features for the amphibian basilar complex are suggested. The basilar complex of Cryptobranchus is interpreted as being most generalized, representing a structural form from which most features of the basilar complex in other urodeles and anurans can be derived.     

中国大鲵机械感受器的超微结构

首次以透射电镜研究了大鲵成体（实验材料共两条）皮肤侧线器官中机械受器即表面神经丘和陷器官的超微结构,并在这两种感受器官之间进行了比较。它们都由三种细胞组成：周围的套细胞,底部的支持细胞以及中央的感觉细胞;且感觉细胞的游离面均有一根动纤毛和几十根静纤毛。但这两种器官在大小、各种细胞的数量、形状和排列上下不同,尤其是表面神经丘感觉细胞游离面纤毛具有双向极性,而陷器官体现为多向极性;表面神经丘的突触球集中分布于一个特殊的感觉细胞,而陷器官的每个感觉细胞基部都有一个突触球。     

西伯利亚鲟仔鱼侧线系统的发育

鲟鱼属软骨硬鳞鱼,在电感受器的进化中占据着极为重要的地位。该文以光镜和扫描电镜手段研究了西伯利亚鲟侧线系统早期发育,包括侧线基板发育及感觉嵴的形成、侧线感受器的发育和侧线管道的形成。1日龄,听囊前后外胚层增厚区域出现6对侧线基板;除后侧线基板细胞向躯干侧面迁移外,其他侧线基板均形成感觉嵴结构;每一侧线基板中均有神经丘原基形成。7日龄,壶腹器官在吻部腹面两侧出现,壶腹器官的发育比神经丘晚一周左右。9日龄,神经丘下的表皮略有凹陷,侧线管道开始形成。29日龄,在吻部腹面两侧可见少数个别的壶腹器官表皮细胞覆盖壶腹器官中央区域留下3～4个小的开口;壶腹管内可见大量的微绒毛存在,在其他鲟形目鱼类、软骨鱼类中也存在类似的结构。57日龄,躯干侧线管道已完全埋于侧骨板中;壶腹器官主要分布在吻部腹面,3～4个聚集在一起,呈"梅花状",分布紧密,并且该部分皮肤表面凹陷,形成花朵状凹穴;侧线系统发育完善。     

The pattern of lateral-line afferents in urodeles

Summary The organization of posterior and anterior afferents of the lateralline system was studied in several species of urodeles by means of transganglionic transport of horseradish peroxidase. The afferents of each lateral-line nerve form distinct fascicles in the medullary alar plate. Each of the two branches of the anterior lateral-line nerve is organized in two long and one short fascicles. The posterior lateral-line afferents form only two long fascicles. Each ordinary neuromast is supplied by only two afferents, which run in the two ventral medullary fiber bundles. It is suggested that afferents to hair cells displaying one type of polarity form together one bundle, but those contacting hair cells polarized in the opposite way form the second ventral bundle of one lateral-line branch. Thus, the lateral-line afferents may be organized in a directotopic fashion.The short dorsal fascicle formed only by the anterior lateral-line afferents receives fibers exclusively from small pit organs. Each pit organ is supplied by only one afferent. Anatomically, these pit organs resemble in many respects the electroreceptive ampullary organs of certain fish.Neurons labeled retrogradely via the anterior lateral-line nerve afferents have been attributed to the nervus trigeminus or facialis. In addition to the posterior lateral-line afferents, only few centrifugally projecting neurons were labeled. These neurons are discussed as efferents to the posterior lateral-line neuromasts.     

Morphology of the ampullae of Lorenzini in juvenile freshwater Carcharhinus leucas

Ampullae of Lorenzini were examined from juvenile Carcharhinus leucas (831–1,045 mm total length) captured from freshwater regions of the Brisbane River. The ampullary organ structure differs from all other previously described ampullae in the canal wall structure, the general shape of the ampullary canal, and the apically nucleated supportive cells. Ampullary pores of 140–205 µm in diameter are distributed over the surface of the head region with 2,681 and 2,913 pores present in two sharks that were studied in detail. The primary variation of the ampullary organs appears in the canal epithelial cells which occur as either flattened squamous epithelial cells or a second form of pseudostratified contour‐ridged epithelial cells; both cell types appear to release material into the ampullary lumen. Secondarily, this ampullary canal varies due to involuted walls that form a clover‐like canal wall structure. At the proximal end of the canal, contour‐ridged cells abut a narrow region of cuboidal epithelial cells that verge on the constant, six alveolar sacs of the ampulla. The alveolar sacs contain numerous receptor and supportive cells bound by tight junctions and desmosomes. Pear‐shaped receptor cells that possess a single apical kinocilium are connected basally by unmyelinated neural boutons. Opposed to previously described ampullae of Lorenzini, the supportive cells have an apical nucleus, possess a low number of microvilli, and form a unique, jagged alveolar wall. A centrally positioned centrum cap of cuboidal epithelial cells overlies a primary afferent lateral line nerve. J. Morphol. 276:481–493, 2015. © 2014 Wiley Periodicals, Inc.     

Ultrastructural Investigation of the Integument of Tubiluchus philippinensis (Priapulida, Tubiluchidae)

The integument of Tubiluchus philippinensis van der Land, 1984 has been investigated by means of scanning and transmission electron microscopy. The ultrastructure of the cuticle corresponds principally to what has been found in Priapulidae. The tumuli are mere cuticular thickenings. Setae, tubuli, flosculi and scalids are receptor organs. Tubuli additionally serve a second function: they produce a secretion. The male genital area is equipped with various receptor organs, the internal morphology of which has been described. All receptor cells are characterized by apical cilia, which may be surrounded by a circlet of microvilli. They sometimes bear a rather complicated rootlet apparatus.     

Ampullary organ morphology of freshwater salmontail catfish, Arius graeffei

Two types of ampullary organs are present in the skin of the freshwater salmontail catfish, Arius graeffei, each consisting of a short canal (0.2-0.5 mm) oriented perpendicular to the basement membrane and ending in an ampulla. Histochemical staining techniques (Alcian blue and Lillie's allochrome) indicate that the ampullary canals contain an acidic mucopolysaccharide gel, which is uniform in its staining properties along the canals. Type II ampullary organs consist of a canal, the wall of which is lined with cuboidal epithelial cells. The canal opens into an ampulla with 50-60 receptor cells. Electron microscopy reveals that the pear-shaped receptor cells bear microvilli on their luminal surface and lie adjacent to an unmyelinated neuron. Type III ampullary organs differ from Type II in that the canal wall consists of cells that possess a protein-rich sac at the luminal apex and have a polymorphic nucleus. The canals of Type III ampullary organs open to an ampulla with 8-30 receptor cells similar in both staining properties and structure to those of the Type II organ. In both types of ampullary organs, supportive cells surround each receptor cell except at the apex of the receptor cell.