Postembryonic development of the posterior lateral line in zebrafish

We examine how the posterior lateral line of the zebrafish grows and evolves from the simple midbody line present at the end of embryogenesis into the complex adult pattern. Our results suggest that secondary neuromasts do not form through budding from the embryonic line, but rather new waves of neuromasts are added anteroposteriorly. We propose that the developmental module that builds the embryonic pattern of neuromasts is used repeatedly during postembryonic development and that additional (secondary) primordia generate the additional neuromasts. We show that differentiated neuromasts migrate ventrally, and eventually generate "stitches" by successive bisections. We also examine the repatterning of the terminal neuromasts, which anticipates the up-bending of the tail leading to the highly asymmetrical caudal fin of the adult (which develops exclusively from the ventral part of the tail). Because terminal repatterning affects all aspects of tail formation, including its sensory development, we speculate that terminal axis bending may have become intimately associated with the terminal Hox genes before the appearance of the tetrapod lineage.     

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.     

Evolution of brain development in amphibians

Principal events in the early embryonic development of the nervous system, from neurulation to primary differentiation, are considered in different amphibian species. Attention is paid to numerous interspecific differences in the structure of neuroepithelium and the patterns of neurulation and embryonic brain segmentation. The data presented indicate that similarity in brain developmental patterns is apparently explained by universality of morphogenetic mechanisms rather than by the common origin of particular species. A hypothesis is proposed that similarity in the shape of the developing amphibian brain is determined by mechanisms of coding positional information necessary for histogenetic differentiation.     

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.     

Development and evolution of lateral line placodes in amphibians I. Development

Lateral line placodes are specialized regions of the ectoderm that give rise to the receptor organs of the lateral line system as well as to the sensory neurons innervating them. The development of lateral line placodes has been studied in amphibians since the early 1900s. This paper reviews these older studies and tries to integrate them with more recent findings. Lateral line placodes are probably induced in a multistep process from a panplacodal area surrounding the neural plate. The time schedule of these inductive processes has begun to be unravelled, but little is known yet about their molecular basis. Subsequent pattern formation, morphogenesis and differentiation of lateral line placodes proceeds in most respects relatively autonomously: Onset and polarity of migration of lateral line primordia, the type, spacing, size and number of receptor organs formed, as well as the patterned differentiation of different cell types occur normally even in ectopic locations. Only the pathways for migration of lateral line primordia depend on external cues. Thus, lateral line placodes act as integrated and relatively context-insensitive developmental modules.     

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.     

Molecular dissection of the migrating posterior lateral line primordium during early development in zebrafish

Background  

Development of the posterior lateral line (PLL) system in zebrafish involves cell migration, proliferation and differentiation of mechanosensory cells. The PLL forms when cranial placodal cells delaminate and become a coherent, migratory primordium that traverses the length of the fish to form this sensory system. As it migrates, the primordium deposits groups of cells called neuromasts, the specialized organs that contain the mechanosensory hair cells. Therefore the primordium provides both a model for studying collective directional cell migration and the differentiation of sensory cells from multipotent progenitor cells.     

Building the posterior lateral line system in zebrafish

The posterior lateral line (pLL) in zebrafish has emerged as an excellent system to study how a sensory organ system develops. Here we review recent studies that illustrate how interactions between multiple signaling pathways coordinate cell fate,morphogenesis, and collective migration of cells in the posterior lateral line primordium. These studies also illustrate how the pLL system is contributing much more broadly to our understanding of mechanisms operating during the growth, regeneration, and self-organization of other organ systems during development and disease.     

Development and evolution of lateral line placodes in amphibians. - II. Evolutionary diversification

The amphibian lateral line system develops from a series of lateral line placodes. The different phases of development from early induction, to pattern formation, differentiation, morphogenesis, and metamorphic fate were summarized in the first part of this review (Schlosser, 2002a). Here, a survey of the diversity of lateral line systems in amphibians is presented indicating that most phases of lateral line development have been subject to evolutionary changes. Several trends suggest important roles for both adaptive changes and internal constraints in amphibian lateral line evolution. Many of these trends involved the coordinated modification of different derivatives of lateral line placodes suggesting that these placodes are not only autonomous developmental modules, but also units of evolutionary variation that tend to be modified in a coherent and largely context-independent fashion.     

Environmental influences on the development of the cardiac system in fish and amphibians

In poikilothermic animals body temperature varies with environmental temperature, and this results in a change in metabolic activity (Q10 of enzymatic reactions typically is around 2-3). Temperature changes also modify gas transport in body fluids. While the diffusion coefficient increases with increasing temperatures, physical solubility and also hemoglobin oxygen affinity decrease. Therefore, an increase in temperature typically requires adjustments in cardiac activity because ventilatory and convectional transport of respiratory gases usually are tightly coupled in adults in order to meet the oxygen demand of body tissues. Hypoxic conditions also provoke adaptations in the central circulatory system, like the hypoxic bradycardia, which has been described for many adult lower vertebrates, combined with an increase in stroke volume and peripheral resistance. In embryos and larvae the situation is much more complicated, because nervous control of the heart is established only late during development, and because the site of gas exchange changes from mainly cutaneous gas exchange during early development to mainly pulmonary or branchial gas exchange in late stages. In addition, recent studies in amphibian and fish embryos and larvae reveal, that at least in very early stages convectional gas transport of the hemoglobin is not essential, which means that in these early stages ventilatory and convectional gas transport are not yet coupled. Accordingly, in early stages of fish and amphibians the central cardiac system often does not respond to hypoxia, although in some species behavioral adaptations indicate that oxygen sensors are functional. If a depression of cardiac activity is observed, it most likely is a direct effect of oxygen deficiency on the cardiac myocytes. Regulated cardiovascular responses to hypoxia appear only in late stages and are similar to those found in adult species.     

Organization and physiology of posterior lateral line afferent neurons in larval zebrafish

The lateral line system of larval zebrafish can translate hydrodynamic signals from the environment to guide body movements. Here, I demonstrate a spatial relationship between the organization of afferent neurons in the lateral line ganglion and the innervation of neuromasts along the body. I developed a whole cell patch clamp recording technique to show that afferents innervate multiple direction-sensitive neuromasts, which are sensitive to low fluid velocities. This work lays the foundation to integrate sensory neuroscience and the hydrodynamics of locomotion in a model genetic system.     

Cryptosporidium in birds, fish and amphibians

Whilst considerable information is available for avian cryptosporidiosis, scant information is available for Cryptosporidium infections in fish and amphibians. The present review details recent studies in avian cryptosporidiosis and our current knowledge of piscine and amphibian infections.     

Role of zebrafish lbx2 in embryonic lateral line development

Background

The zebrafish ladybird homeobox homologous gene 2 (lbx2) has been suggested to play a key role in the regulation of hypaxial myogenic precursor cell migration. Unlike their lbx counterparts in mammals, the function of teleost lbx genes beyond myogenesis during embryonic development remains unexplored.

Principal Findings

Abrogation of lbx2 function using a specific independent morpholino oligonucleotide (MO) or truncated lbx2 mRNA with an engrailed domain deletion (lbx2^eh-) resulted in defective formation of the zebrafish posterior lateral line (PLL). Migration of the PLL primordium was altered and accompanied by increased cell death in the primordium of lbx2-MO-injected embryos. A decreased number of muscle pioneer cells and impaired expression pattern of sdf1a in the horizontal myoseptum was observed in lbx2 morphants.

Significance

Injection of lbx2 MO or lbx2^eh- mRNA resulted in defective PPL formation and altered sdf1a expression, confirming an important function for lbx2 in sdf1a-dependent migration. In addition, the disassociation of PPL nerve extension with PLL primordial migration in some lbx2 morphants suggests that pathfinding of the PLL primordium and the lateral line nerve may be regulated independently.     

Object localization through the lateral line system of fish: theory and experiment

Fish acquire information about their aquatic environment by means of their mechanosensory lateral-line system. This system consists of superficial and canal neuromasts that sense perturbations in the water surrounding them. Based on a hydrodynamic model presented here, we propose a mechanism through which fish can localize the source of these perturbations. In doing so we include the curvature of the fish body, a realistic lateral line canal inter-pore distance for the lateral-line canals, and the surface boundary layer. Using our model to explore receptor behavior based on experimental data of responses to dipole stimuli we suggest that superficial and canal neuromasts employ the same mechanism, hence provide the same type of input to the central nervous system. The analytical predictions agree well with spiking responses recorded experimentally from primary lateral-line nerve fibers. From this, and taking into account the central organization of the lateral-line system, we present a simple biophysical model for determining the distance to a source.     

Types and development pathways of lateral line scales in some teleost species

Voronina, E.P. and Hughes, D.R. 2011. Types and development pathways of lateral line scales in some teleost species. —Acta Zoologica (Stockholm) 00 : 1–13. A comparative study of lateral line scales (lls) in nine teleost species was undertaken to trace their ontogenetic structural changes. Three universal characters were used to describe and classify definitive and developing lls. The four main structural types in teleosts are represented. In adult fish, lls are the same structural type in all parts of lateral line in any one specimen, but number of tubules and their orientation may vary. In juvenile fish, except for one species, the structural type of every lls changes with growth, and this process progresses along the lateral line in the direction of development typical for the species. Definitive structural type of the lls is not determined by common scale type and size, presence or absence of nerve foramen on lls, scale overlapping or time of initiation of scales and trunk canal. Development pathways are proposed in which terminal states correspond to the final development of the most complex lls type in Cyprinus carpio, Carassius carassius, Oncorhynchus mykiss, Diplodus annularis and Mullus barbatus. The intermediate states of these pathways correspond to other types of lls as examples of pedomorphosis in Perca fluviatilis, Sander lucioperca, Symphysodon aequifasciatus and Hippoglossoides platessoides.     

VISION AND SENSORY PHYSIOLOGY The lateral line systems of three deep-sea fish

The distribution and ultrastructure of the lateral line systems in three taxonomically dispersed deep-sea fish are described: Poromitra capito, Melanonus zugmayeri and Phrynichthys wedli. They are meso- to bathpelagic and are thought to feed on small crustaceans and fish. All possess highly developed lateral line systems, a feature associated with life in the deep sea. Poromitra capito and M. zugmayeri exhibit widened head canals which are connected to the outside by large pores and which contain around 60 large neuromasts. Each neuromast consists of a cupula, shield-shaped mantle and a sensory plate containing hundreds to thousands of hair cells. Direction of sensitivity is in the long axis of the canal (perpendicular to the long axis of the mantle). Depending on their position on the sensory plate, the hair cells have different morphologies. They fall into three basic classes which, from comparison with past work, may be tuned to different frequencies. Alternatively, the various hair cell morphologies could be interpreted as being members of a developmental or growth sequence. Phrynichthys wedli has no canal organs, these being replaced secondarily by many superficial neuromasts placed on prominent papillae in rows which cover much of the 'head' and body. Direction of sensitivity is along the axis of the neuromast row. An extreme proliferation of superficial neuromasts are also found on the heads of P. capito and M. zugmayeri and these are of a type not described before. They consist of stitches, raised on papillae in M. zugmayeri and several mm long in P. capito , in which continuous lines of hair cells, two to three cells wide, are embedded. Direction of sensitivity is perpendicular to the long axis of the stitch. Based on the structure and direction of sensitivity, possible functional implications of all the neuromast types described are compared and discussed.