Evolution of posterior lateral line development in fish and amphibians

The lateral line is a sensory system present in fish and amphibians. It is composed of discrete sense organs, the neuromasts, arranged on the head and body in species-specific patterns. The neuromasts are deposited by migrating primordia that originate from pre- and postotic placodes and follow defined pathways on the head and body. Here we examine the formation of the posterior lateral line (PLL), which extends rostrocaudally on the trunk and tail. In amphibians, the PLL neuromasts are deposited as a single wave from the head to the tip of the tail. In the zebrafish, however, the first wave of neuromast deposition forms but a rudimentary PLL, and several additional waves are needed to form the adult pattern. We show that the amphibian mode is also present in the sturgeon and therefore probably represents the primitive mode, whereas the zebrafish mode is highly conserved in several teleost species. A third mode is found in a subgroup of teleosts, the protacanthopterygians, and may represent a synapomorphy of this group. Altogether, the mode of formation of the embryonic PLL appears to have undergone remarkably few changes during the long history of anamniote evolution, even though large differences can be observed in the lateral line morphology of adult fishes.     

Cell migration in the postembryonic development of the fish lateral line

We examine at the cellular level the postembryonic development of the posterior lateral line in the zebrafish. We show that the first wave of secondary neuromasts is laid down by a migrating primordium, primII. This primordium originates from a cephalic region much like the primordium that formed the primary line during embryogenesis. PrimII contributes to both the lateral and the dorsal branches of the posterior lateral line. Once they are deposited by the primordium, the differentiating neuromasts induce the specialisation of overlying epidermal cells into a pore-forming annulus, and the entire structure begins to migrate ventrally across the epithelium. Thus the final two-dimensional pattern depends on the combination of two orthogonal processes: anteroposterior waves of neuromast formation and dorsoventral migration of individual neuromasts. Finally, we examine how general these migratory processes can be by describing two fish species with very different adult patterns, Astyanax fasciatus (Mexican blind cavefish) and Oryzias latipes (medaka). We show that their primary patterns are nearly identical to that observed in zebrafish embryos, and that their postembryonic growth relies on the same combination of migratory processes that we documented in the case of the zebrafish.     

Chemokine and Fgf signalling act as opposing guidance cues in formation of the lateral line primordium

The directional migration of many cell populations occurs as a coherent group. An amenable model is provided by the posterior lateral line in zebrafish, which is formed by a cohesive primordium that migrates from head to tail and deposits future neuromasts at intervals. We found that prior to the onset of migration, the compact state of the primordium is not fully established, as isolated cells with lateral line identity are present caudal to the main primordium. These isolated cells are retained in position such that they fuse with the migrating primordium as it advances, and later contribute to the leading zone and terminal neuromasts. We found that the isolated lateral line cells are positioned by two antagonistic cues: Fgf signalling attracts them towards the primordium, which counteracts Sdf1α/Cxcr4b-mediated caudal attraction. These findings reveal a novel chemotactic role for Fgf signalling in which it enables the coalescence of the lateral line primordium from an initial fuzzy pattern into a compact group of migrating cells.     

Postembryonic development of the posterior lateral line in the zebrafish

SUMMARY The posterior lateral line (PLL) of zebrafish comprises seven to eight sense organs at the end of embryogenesis, arranged in a single antero-posterior line that extends along the horizontal myoseptum from the ear to the tip of the tail. At the end of larval life, four antero-posterior lines extend on the trunk and tail, comprising together around 60 sense organs. The embryonic pattern is largely conserved among teleosts, although adult patterns are very diverse. Here we describe the transition from embryonic to juvenile pattern in the zebrafish, to provide a framework for understanding how the diversity of adult patterns comes about. We show that the four lines that extend over the adult body originate from latent precursors laid down by migrating primordia that arise during embryogenesis. We conclude that, in zebrafish, the entire development of the PLL system up to adulthood can be traced back to events that took place during the first 2 days of life. We also show that the transition from embryonic to adult pattern involves few distinct operations, suggesting that the diversity of patterns among adult teleosts may be due to differential control of these few operations acting upon common embryonic precursors.     

Pattern formation in the lateral line of zebrafish.

The lateral line of fish and amphibians is a sensory system that comprises a number of individual sense organs, the neuromasts, arranged in a defined pattern on the surface of the body. A conspicuous part of the system is a line of organs that extends along each flank (and which gave the system its name). At the end of zebrafish embryogenesis, this line comprises 7-8 neuromasts regularly spaced between the ear and the tip of the tail. The neuromasts are deposited by a migrating primordium that originates from the otic region. Here, we follow the development of this pattern and show that heterogeneities within the migrating primordium prefigure neuromast formation.     

Developmental origin of a major difference in sensory patterning between zebrafish and bluefin tuna

The posterior lateral line system (PLL) of teleost fish comprises a number of mechanosensory organs arranged in defined patterns on the body surface. Embryonic patterns are largely conserved among teleosts, yet adult patterns are highly diverse. Although changes in pattern modify the perceptual abilities of the system, their developmental origin remains unknown. Here we compare the processes that underlie the formation of the juvenile PLL pattern in Thunnus thynnus, the bluefin tuna, to the processes that were elucidated in Danio rerio, the zebrafish. In both cases, the embryonic PLL comprises five neuromasts regularly spaced along the horizontal myoseptum, but the juvenile PLL comprises four roughly parallel anteroposterior lines in zebrafish, whereas it is a simple dorsally arched line in tuna fish. We examined whether this difference involves evolutionary novelties, and show that the same mechanisms mediate the transition from embryonic to juvenile patterns in both species. We conclude that the marked difference in juveniles depends on a single change (dorsal vs. ventral migration of neuromasts) in the first days of larval life.     

Development of the lateral line canal system through a bone remodeling process in zebrafish

The lateral line system of teleost fish is composed of mechanosensory receptors (neuromasts), comprising superficial receptors and others embedded in canals running under the skin. Canal diameter and size of the canal neuromasts are correlated with increasing body size, thus providing a very simple system to investigate mechanisms underlying the coordination between organ growth and body size. Here, we examine the development of the trunk lateral line canal system in zebrafish. We demonstrated that trunk canals originate from scales through a bone remodeling process, which we suggest is essential for the normal growth of canals and canal neuromasts. Moreover, we found that lateral line cells are required for the formation of canals, suggesting the existence of mutual interactions between the sensory system and surrounding connective tissues.     

Dermal morphogenesis controls lateral line patterning during postembryonic development of teleost fish

The lateral line system displays highly divergent patterns in adult teleost fish. The mechanisms underlying this variability are poorly understood. Here, we demonstrate that the lateral line mechanoreceptor, the neuromast, gives rise to a series of accessory neuromasts by a serial budding process during postembryonic development in zebrafish. We also show that accessory neuromast formation is highly correlated to the development of underlying dermal structures such as bones and scales. Abnormalities in opercular bone morphogenesis, in endothelin 1-knockdown embryos, are accompanied by stereotypic errors in neuromast budding and positioning, further demonstrating the tight correlation between the patterning of neuromasts and of the underlying dermal bones. In medaka, where scales form between peridermis and opercular bones, the lateral line displays a scale-specific pattern which is never observed in zebrafish. These results strongly suggest a control of postembryonic neuromast patterns by underlying dermal structures. This dermal control may explain some aspects of the evolution of lateral line patterns.     

Post‐embryonic development of canal and superficial neuromasts and the generation of two cranial lateral line phenotypes

The relatively simple structural organization of the cranial lateral line system of bony fishes provides a valuable context in which to explore the ways in which variation in post‐embryonic development results in functionally distinct phenotypes, thus providing a link between development, evolution, and behavior. Vital fluorescent staining, histology, and scanning electron microscopy were used to describe the distribution, morphology, and ontogeny of the canal and superficial neuromasts on the head of two Lake Malawi cichlids with contrasting lateral line canal phenotypes (Tramitichromis sp. [narrow‐simple, well‐ossified canals with small pores] and Aulonocara stuartgranti [widened, more weakly ossified canals with large pores]). This work showed that: 1) the patterning (number, distribution) of canal neuromasts, and the process of canal morphogenesis typical of bony fishes was the same in the two species, 2) two sub‐populations of neuromasts (presumptive canal neuromasts and superficial neuromasts) are already distinguishable in small larvae and demonstrate distinctive ontogenetic trajectories in both species, 3) canal neuromasts differ with respect to ontogenetic trends in size and proportions between canals and between species, 4) the size, shape, configuration, physiological orientation, and overall rate of proliferation varies among the nine series of superficial neuromasts, which are found in both species, and 5) in Aulonocara, in particular, a consistent number of canal neuromasts accompanied by variability in the formation of canal pores during canal morphogenesis demonstrates independence of early and late phases of lateral line development. This work provides a new perspective on the contributions of post‐embryonic phases of lateral line development and to the generation of distinct phenotypes in the lateral line system of bony fishes. J. Morphol. 277:1273–1291, 2016. © 2016 Wiley Periodicals, Inc.     

Ontogeny and phylogeny of the trunk lateral line system in cichlid fishes

An examination of the ontogeny of the lateral line trunk canal and the diversity of adult trunk canal patterns among cichlids indicates that bidirectional canal formation is a general ontogenetic pattern in the Cichlidae with the exception of Cichla and those few species with a complete trunk canal pattern. In addition to the tubed scales which make up the trunk canal, some lateral line scales have pits containing superficial neuromasts. These are recognized as components of the lateral line system of the trunk in adult cichlids for the first time. Eight trunk canal patterns that are variations on a simple disjunct pattern are defined among the 17 cichlid genera examined. Using bidirectional canal formation as a developmental model, these patterns can be placed along an ontogenetic spectrum. This suggests that heterochrony (alterations in the timing of development) is an important mechanism of evolutionary change in the lateral line system of the trunk in cichlid fishes.     

Organization of the superficial neuromast system in goldfish, Carassius auratus

Distribution, morphology, and orientation of superficial neuromasts and polarization of the hair cells within superficial neuromasts of the goldfish (Carassius auratus) were examined using fluorescence labeling and scanning electron microscopy. On each body side, goldfish have 1,800-2,000 superficial neuromasts distributed across the head, trunk and tail fin. Each superficial neuromast had about 14-32 hair cells that were arranged in the sensory epithelium with the axis of best sensitivity aligned perpendicular to the long axis of the neuromast. Hair cell polarization was rostro-caudal in most superficial neuromasts on trunk scales (with the exception of those on the lateral line scales), or on the tail fin. On lateral line scales, the most frequent hair cell polarization was dorso-ventral in 45% and rostro-caudal in 20% of the superficial neuromasts. On individual trunk scales, superficial neuromasts were organized in rows which in most scales showed similar orientations with angle deviations smaller than 45 degrees . In about 16% of all trunk scales, groups of superficial neuromasts in the dorsal and ventral half of the scale were oriented orthogonal to each other. On the head, most superficial neuromasts were arranged in rows or groups of similar orientation with angle deviations smaller than 45 degrees . Neighboring groups of superficial neuromasts could differ with respect to their orientation. The most frequent hair cell polarization was dorso-ventral in front of the eyes and on the ventral mandible and rostro-caudal below the eye and on the operculum.     

Zebrafish larvae exhibit rheotaxis and can escape a continuous suction source using their lateral line

Zebrafish larvae show a robust behavior called rheotaxis, whereby they use their lateral line system to orient upstream in the presence of a steady current. At 5 days post fertilization, rheotactic larvae can detect and initiate a swimming burst away from a continuous point-source of suction. Burst distance and velocity increase when fish initiate bursts closer to the suction source where flow velocity is higher. We suggest that either the magnitude of the burst reflects the initial flow stimulus, or fish may continually sense flow during the burst to determine where to stop. By removing specific neuromasts of the posterior lateral line along the body, we show how the location and number of flow sensors play a role in detecting a continuous suction source. We show that the burst response critically depends on the presence of neuromasts on the tail. Flow information relayed by neuromasts appears to be involved in the selection of appropriate behavioral responses. We hypothesize that caudally located neuromasts may be preferentially connected to fast swimming spinal motor networks while rostrally located neuromasts are connected to slow swimming motor networks at an early age.     

Regulation of latent sensory hair cell precursors by glia in the zebrafish lateral line

The lateral line is a placodally derived mechanosensory organ in anamniotes that detects the movement of water. In zebrafish embryos, a migrating primordium deposits seven to nine clusters of sensory hair cells, or neuromasts, at intervals along the trunk. Postembryonically, neuromasts continue to be added. We show that some secondary neuromasts arise from a pool of latent precursors that are deposited by the primordium between primary neuromasts. Interneuromast cells lie adjacent to the lateral line nerve and associated glia. These cells remain quiescent while they are juxtaposed with the glia; however, when they move away from the nerve they increase proliferation and form neuromasts. If glia are manually removed or genetically ablated by mutations in cls/sox10, hypersensitive (hps), or rowgain (rog), neuromasts precociously differentiate. Transplantation of wt glia into mutants rescues the appropriate temporal differentiation of interneuromast cells. Our studies reveal a role for glia in regulating sensory hair cell precursors.     

Postembryonic lineages of the Drosophila brain: II. Identification of lineage projection patterns based on MARCM clones

The Drosophila central brain is largely composed of lineages, units of sibling neurons derived from a single progenitor cell or neuroblast. During the early embryonic period, neuroblasts generate the primary neurons that constitute the larval brain. Neuroblasts reactivate in the larva, adding to their lineages a large number of secondary neurons which, according to previous studies in which selected lineages were labeled by stably expressed markers, differentiate during metamorphosis, sending terminal axonal and dendritic branches into defined volumes of the brain neuropil. We call the overall projection pattern of neurons forming a given lineage the “projection envelope” of that lineage. By inducing MARCM clones at the early larval stage, we labeled the secondary progeny of each neuroblast. For the supraesophageal ganglion excluding mushroom body (the part of the brain investigated in the present work) we obtained 81 different types of clones. Based on the trajectory of their secondary axon tracts (described in the accompanying paper, Lovick et al., 2013), we assigned these clones to specific lineages defined in the larva. Since a labeled clone reveals all aspects (cell bodies, axon tracts, terminal arborization) of a lineage, we were able to describe projection envelopes for all secondary lineages of the supraesophageal ganglion. This work provides a framework by which the secondary neurons (forming the vast majority of adult brain neurons) can be assigned to genetically and developmentally defined groups. It also represents a step towards the goal to establish, for each lineage, the link between its mature anatomical and functional phenotype, and the genetic make-up of the neuroblast it descends from.     

The lateral line of zebrafish: a model system for the analysis of morphogenesis and neural development in vertebrates

The lateral line of the zebrafish has many of the advantages that made the sensory organs of Drosophila a very productive model system: 1) it comprises a set of discrete sense organs (neuromasts) arranged in a defined, species-specific pattern, such that each organ can be individually recognized; 2) the neuromasts are superficial and easy to visualize, and the innervating neurons are easy to label; 3) the sensory projection is simple yet reproducibly organized. Here we describe some of the tools that can be used to investigate the development of this system, and we illustrate their usefulness with specific examples. We conclude that the lateral line is uniquely suited among vertebrate sensory systems for a molecular, cellular and genetic analysis of pattern formation and of neural development.     

Distributional Pattern of Neuromasts in Goby,Gobius striatus Day (Gobiidae)

Distributional pattern of the neuromasts has been described for Gobius striatus Day. The neuromasts are arranged in several lines. Canal formation, like many gobiids, is suppressed to varying extent. The supraorbital line presents interesting variations. The supraorbital lines of the two sides are separate from each other even in the so-called common ‘interorbital chamber’. An outstanding feature of the neuromast system of the fish is the great development of the supramaxillary line which is perhaps best developed in this case.     

发育重塑与生物多样性

多细胞生物的成熟个体都是由单细胞的受精卵发育而来的。如果把成熟个体的表型看成生命存在的式样或模式(pattern), 那么发育就是形成和产生这种式样或模式的过程, 即塑造(patterning)或发育塑造(developmental patterning)。相应地, 对原来发育过程进行修饰或改变而产生新表型的过程就是发育重塑(developmental repatterning)。已有的研究结果表明, 发育重塑在多细胞生物的进化过程中非常普遍, 也非常重要。根据突变的类型和后果, 发育重塑既包括对相同基因在表达的时、空和量上的改变, 分别为异时(heterochrony)、异位(heterotopy)和异量(heterometry), 又包括对基因类型的改变, 即异型(heterotypy)。本文通过对一些经典案例的介绍, 揭示了发育重塑与表型变化的关系, 探讨发育重塑对生物多样性的贡献。     

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.     

Neuromast formation in the prehatching embryos of the Japanese flounder (Paralichthys olivaceus)

The present paper clarifies the initial development of the lateral line organs in the embryonic Japanese flounder, Paralichthys olivaceus. The first appearances of lateral line primordia, and the proliferation, distribution and morphological development of the free neuromasts, including nerve ending formation: establishment of hair cell innervations via the formation of synapses, were examined by light microscopy, scanning and transmission electron microscopy. The first pair of neuromast primordia appeared in the otic region ≈ 30 h prior to hatching and subsequently differentiated into free neuromasts, otic neuromasts, after ≈ 8 h. At hatching, a pair of free neuromasts and three pairs of neuromast primordia were present on the head, and three pairs of neuromast primordia were present on the trunk. The hair cell polarity of the otic neuromast until just prior to hatching was radial, but not bi‐directional. The typical afferent and efferent nerve endings in the otic neuromasts had formed by the time of hatching, suggesting that the otic neuromasts are functional prior to hatching. The three neuromast primordia located on each side of the trunk were derived from a long, narrow ectodermal cell cluster and erupted through the epidermis after hatching.