Jacqueline F. Webb

Gross morphology and evolution of the mechanoreceptive lateral-line system in teleost fishes

The morphology and development of the mechanoreceptive lateral-line system in teleost fishes is reviewed, and the systematic distribution of defined types of lateral-line systems is summarized. The importance of an understanding of ontogeny is stressed and the roles of phylogenetic and developmental constraints in the evolution of the lateral-line system are discussed. Four types of head canal systems are identified on the basis of the relative development of the canals and the orientation of the neuromast receptors contained within them. The distribution of these patterns in the four major teleost clades is analyzed. It is suggested that a branched tubule system associated with the head canals is a primitive teleost character, while widened and reduced head canal patterns are convergent functional specializations in many taxa. The trunk canals are contained in a continuous series of lateral-line scales, and eight trunk canal patterns are described in teleosts. Given the correlation of the systematic distribution of the different trunk canal patterns, ecological habit and body shape, it appears that the trunk canals may function as a hydrodynamic monitor in swimming fishes.

The cusp of evolution and development: a model of cichlid tooth shape diversity

Tooth shape is a hallmark of repeated evolutionary radiations among cichlid fishes from East Africa. Cusp shape and number vary both within populations and among closely related species with different feeding behaviors and ecologies. Here, we use histology and scanning electron microscopy to chart the developmental trajectory of tooth shape differences in fishes from Lake Malawi. We demonstrate that species with bi‐ or tricuspid adult (replacement) teeth initially possess a first‐generation unicuspid dentition. Notably, the timing of turnover from first‐generation to replacement teeth differs among species and is correlated with feeding ecology. Next, we use field data for cichlid species with adult unicuspid, bicuspid, and tricuspid teeth to demonstrate a strong and positive relationship between the number of teeth in a row and tooth shape. We discuss cichlid tooth ontogeny in the context of morphogenetic models designed to explain the developmental basis of tooth shape variation in mammals. We suggest that the dramatic differences in cichlid dentitions can be explained by variation in the expression of common activators and inhibitors acting at multiple stages of odontogenesis.

Developmental Constraints and Evolution of the Lateral Line System in Teleost Fishes

Evolution has been described as the result of two independent and sequential processes: the origin of variation and natural selection. The phenotypic variation upon which natural selection acts is, in turn, a result of processes that generate as well as those that limit variation (Alberch 1980, 1982b). The processes that generate variation (mutation, recombination) have been the mainstay of evolutionary thought for the past century (Mayr 1982), but many processes limit and channel variation to produce “morphological gaps” (Alberch 1980,1982b). These gaps or “potential morphospaces” remain unoccupied, not because of the absence of appropriate selection pressures, but because historical (phylogenetic) and ontogenetic constraints on morphological change limit morphological variation (Liem and Wake 1985). Consideration of the contributions of these constraints in morphological evolution (e.g., Gould and Lewontin 1979; Alberch 1980) challenges the adaptationist program that has prevailed in the field of evolutionary biology for the past century.

Postembryonic development of the cranial lateral line canals and neuromasts in zebrafish

The development of the cranial lateral line canals and neuromast organs are described in postembryonic zebrafish (0–80 days postfertilization). Cranial canal development commences several weeks after hatch, is initiated in the vicinity of individual neuromasts, and occurs in four discrete stages that are described histologically. Neuromasts remain in open canal grooves for several weeks during which they dramatically change shape and increase in size by adding hair cells at a rate one‐tenth that in the zebrafish inner ear. Scanning electron microscopy demonstrates that neuromasts elongate perpendicular to the canal axis and the axis of hair cell polarization and that they lack a prominent nonsensory cell population surrounding the hair cells—features that make zebrafish neuromasts unusual among fishes. These results demand a reassessment of neuromast and lateral line canal diversity among fishes and highlight the utility of the lateral line system of postembryonic zebrafish for experimental and genetic studies of the development and growth of hair cell epithelia. Developmental Dynamics, 2003.

Feeding in the dark: lateral-line-mediated prey detection in the peacock cichlid Aulonocara stuartgranti

SUMMARY The cranial lateral line canal system of teleost fishes is morphologically diverse and is characterized by four patterns. One of these, widened lateral line canals, has evolved convergently in a wide range of teleosts, including the Lake Malawi peacock cichlids (Aulonocara), and has been attributed to its role in prey detection. The ability to study Aulonocara in the laboratory provides an opportunity to test the hypothesis that their reported ability to feed on invertebrate prey living in sandy substrates in their natural habitat is the result of lateral-line-mediated prey detection. The goal of this study was to determine whether Aulonocara stuartgranti could detect hydrodynamic stimuli generated by tethered brine shrimp (visualized using digital particle image velocimetry) under light and dark conditions, with and without treatment with cobalt chloride, which is known to temporarily inactivate the lateral line system. Fish were presented with six pairs of tethered live and dead adult brine shrimp and feeding behavior was recorded with HD digital video. Results demonstrate that A. stuartgranti: (1) uses the same swimming/feeding strategy as they do in the field; (2) detects and consumes invertebrate prey in the dark using its lateral line system; (3) alters prey detection behavior when feeding on the same prey under light and dark conditions, suggesting the involvement of multiple sensory modalities; and (4) after treatment with cobalt chloride, exhibits a reduction in their ability to detect hydrodynamic stimuli produced by prey, especially in the dark, thus demonstrating the role of the lateral line system in prey detection.

Larvae in Fish Development and Evolution

Publisher Summary This chapter focuses on the development and evolution of fish larvae. The development of fishes from fertilization to sexual maturity is a continuum that is punctuated by developmental events and transitions, which may be either gradual and unremarkable or abrupt and quite dramatic. Freshwater teleost fishes are generally characterized by unspecialized larvae with a gradual transition to the juvenile stage. Some marine teleost fishes develop from demersal eggs and larvae, and these also tend to be unremarkable and have a gradual transition to the juvenile stage. In contrast, the majority of marine teleost fishes have planktonic eggs and larvae, which may have extensive specializations and whose transition to the juvenile stage generally is dramatic. The presence of distinctive features in marine fish larvae (or any group of organisms) would lead one to expect that they are functionally important, that they are the result of natural selection, and that they are thus adaptive. However, unique or unusual features in larvae must be interpreted in the context of the comparative development of the larval, juvenile, and adult stages in order to be considered properly. Further, the adaptive significance of such specializations cannot be determined until structure–function relationships are better understood.

Morphology and Distribution of Pit Organs and Canal Neuromasts in Non-Teleost Bony Fishes

The morphology of the pit organs and canal neuromasts of the actinopterygian Polypterus and the lungfishes Lepidosiren, Neoceratodus and Protopterus are described using light microscopy, scanning electron microscopy and transmission electron microscopy. Pit organs resemble canal neuromasts in their hair cell polarization, but they differ in size, shape, hair cell density and in the length of the kinocilia. Pit line neuromasts in Lepidosiren, Polypterus and Protopterus are arranged in dense lines, with numerous neuromasts between pores in the canal, and are an order of magnitude smaller than canal neuromasts in Polypterus. We suggest that the evolutionary transformation of canal neuromasts into superficial neuromasts occurred through the evolutionary reduction of the lateral line canals, either as the result of selection for changes in neuromast function, or as the result of non-adaptive reduction of dermal bone around the lateral line canals and their neuromasts. Protopterus (a lepidosirenid lungfish) is apparently unique among bony fishes in that it has multiple neuromasts between adjacent pores in lateral line canals on the head. An analysis of the distribution of this character among major gnathostome clades indicates that multiple canal neuromasts between pore positions is a primitive gnathostome character. Latimeria, Neoceratodus and actinopterygian fishes are characterized by an alternative character state, the presence of one canal neuromast between adjacent pores.

The evolution of the laterophysic connection with a revised phylogeny and taxonomy of butterflyfishes (Teleostei: Chaetodontidae)

The higher‐level relationships of butterflyfishes were examined using 37 morphological characters. This analysis combines characters derived from a histological study describing variation in the morphology of the laterophysic connection (an association between the swim bladder and the lateral‐line canals) with previously described morphological characters. The phylogenetic analysis resulted in four equally parsimonious trees that only differed in the placement of two of the 11 chaetodontid genera (Amphichaetodon and Forcipiger). We compare our analysis with previous hypotheses, present a new taxonomy consistent with the proposed cladistic relationships, and diagnose Chaetodon with five unreversed synapomorphies, including the evolution of characters composing the laterophysic connection. A new character‐based diagnosis of Chaetodon is provided and species are allocated accordingly; Chaetodon now includes the former Parachaetodon ocellatus and excludes the former subgenera Prognathodes and Roa. The evolution of the laterophysic connection is examined by optimizing character‐state transformations on the new hypothesis of relationships.

The laterophysic connection and swim bladder of butterflyfishes in the genus Chaetodon (Perciformes: Chaetodontidae).

The laterophysic connection (LC) is an association between bilaterally paired, anterior swim bladder extensions (horns) and medial openings in the supracleithral lateral line canals that diagnoses butterflyfishes in the genus Chaetodon. It has been hypothesized that the LC makes the lateral line system sensitive to sound pressure stimuli that are transmitted by the swim bladder horns and converted to fluid flow into the lateral line system via a laterophysic tympanum. The purpose of this study was to define variation in the morphology of the LC, swim bladder and swim bladder horns among 41 Chaetodon species from all 11 Chaetodon subgenera and a species from each of four non‐Chaetodon genera using gross dissection, histological analysis as well as 2D or 3D CT (computed tomographic) imaging of live, anesthetized fishes. Our results demonstrate that the lateral line system appears rather unspecialized with well‐ossified narrow canals in all species examined. Two LC types (direct and indirect), defined by whether or not the paired anterior swim bladder horns are in direct contact with a medial opening in the supracleithral lateral line canal, are found among species examined. Two variants on a direct LC and four variants of an indirect LC are defined by combinations of soft tissue anatomy (horn length [long/short] and width [wide/narrow], number of swim bladder chambers [one/two], and presence/absence of mucoid connective tissue in the medial opening in the supracleithrum). The combination of features defining each LC variant is predicted to have functional consequences for the bioacoustics of the system. These findings are consistent with the recent discovery that Chaetodon produce sounds during social interactions. The data presented here provide the comparative morphological context for the functional analysis of this novel swim bladder‐lateral line connection. J. Morphol., 2006.

Morphological Diversity, Development, and Evolution of the Mechanosensory Lateral Line System

Morphological, physiological, behavioral, and developmental studies of the mechanosensory lateral line system are used to define sources of morphological and functional variation in the system among fishes (and briefly in amphibians), review patterns and mechanisms of embryonic and postembryonic development, discuss how interspecific variation in morphology is explained by developmental patterns, and place the morphology of the lateral line system in model species for neurophysiological and neuroethological studies into a broader comparative context. The presence of both canal and superficial neuromasts defines two sensory submodalities in jawed fishes. The number and spatial distribution of superficial neuromasts appear to demonstrate more variation among species when compared to that of the canal neuromasts, whose distribution is limited by their association with the lateral line canals. Morphological diversity of the lateral line canal system is defined by (1) variation in the morphology and extent of development of the cranial lateral line canals; (2) the number, placement, and extent of development of the trunk canals; and (3) the distribution of superficial neuromasts on the skin of the head, trunk, and tail. An understanding of the pattern and timing of lateral line development is essential for an appreciation of changes in lateral line function and thus its behavioral roles through a fish’s life history. The evolution of the lateral line system and structure–function relationships among species are best appreciated when patterns and underlying mechanisms of development are considered. Conversely, an appreciation for morphological diversity among species is likely to assist in the interpretation of developmental patterns.