Functional and Evolutionary Implications of Peripheral Diversity in Lateral Line Systems

Any treatise on the evolution of hearing inevitably raises the possibility that the vertebrate auditory system has evolved from the mechanosensory lateral line system known to exist in the earliest vertebrates. The arguments for (van Bergeijk 1967; Jorgensen 1989) and against (Wever 1976; Northcutt 1981) this “octavolateralis” hypothesis, first proposed by Ayers (1892), have depended primarily on anatomical and developmental comparisons between the two systems. It is questionable whether this issue can or ever will be resolved, but the frequency with which it has been addressed in the past and is currently being addressed in this volume (Popper, Piatt, and Edds, Chapter 4; Fritzsch, Chapter 18) testifies to the fascination it holds for anyone interested in the evolution of ears and hearing.

[1]  M. Lannoo.  Neuromast topography in anuran amphibians , 1987, Journal of morphology.

[2]  J. Gray,et al.  Mechanical Factors in the Excitation of the Lateral Lines of Fishes , 1988 .

[3]  J. Webb,et al.  Developmental Constraints and Evolution of the Lateral Line System in Teleost Fishes , 1989 .

[4]  J. Gray,et al.  Structure and development of the free neuromasts and lateral line system of the herring , 1983, Journal of the Marine Biological Association of the United Kingdom.

[5]  M. A. Ali.  Environmental Physiology of Fishes , 2014, NATO Advanced Study Institutes Series.

[6]  R. Boyle,et al.  Resting discharge and response dynamics of horizontal semicircular canal afferents of the toadfish, Opsanus tau , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Catherine A. McCormick,et al.  Central Lateral Line Mechanosensory Pathways in Bony Fish , 1989 .

[8]  R. Northcutt,et al.  Sensory and Other Neural Traits and the Adaptationist Program: Mackerels of San Marco? , 1988 .

[9]  N. Schellart,et al.  Interrelationship of Acousticolateral and Visual Systems in the Teleost Midbrain , 1989 .

[10]  F. Dercum.  The Lateral Sensory Apparatus of Fishes , 1879 .

[11]  O. Sand,et al.  Field studies of hearing in two species of flatfish Pleuronectes platessa (L.) and limanda limanda (L.) (family pleuronectidae). , 1974, Comparative biochemistry and physiology. A, Comparative physiology.

[12]  W. D. Neff.  Contributions to sensory physiology , 1965 .

[13]  G. Nelson.  Cephalic sensory canals, pitlines, and the classification of esocoid fishes, with notes on galaxiids and other teleosts. American Museum novitates ; no. 2492 , 1972 .

[14]  Peter Görner,et al.  Stimulus Localization in Xenopus: Role of Directional Sensitivity of Lateral Line Stitches , 1989 .

[15]  F. Merkel.  Über die Endigungen der sensiblen Nerven in der Haut der Wirbelthiere , 1880 .

[16]  M. Lannoo.  Neuromast topography in urodele amphibians , 1987, Journal of morphology.

[17]  E. Allis.  The anatomy and development of the lateral line system in amia calva , 1889 .

[18]  P. S. Enger,et al.  An electrophysiological field study of hearing in fish. , 1967, Comparative biochemistry and physiology.

[19]  Bernd Fritzsch.  Diversity and Regression in the Amphibian Lateral Line and Electrosensory System , 1989 .

[20]  K. Kirk.  Water flows produced by Daphnia and Diaptomus: Implications for prey selection by mechanosensory predators , 1985 .

[21]  E. Denton,et al.  Mechanical factors in the excitation of clupeid lateral lines , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[22]  J. Gray,et al.  Some Observations on the Forces Acting on Neuromasts in Fish Lateral Line Canals , 1989 .

[23]  Peripheral Processing by the Lateral Line System of the Mottled Sculpin ( Cottus bairdi ) , 1989 .

[24]  R. Fay.  Coding of information in single auditory-nerve fibers of the goldfish. , 1978, The Journal of the Acoustical Society of America.

[25]  T. Poulson.  Cave Adaptation in Amblyopsid Fishes , 1963 .

[26]  Sheryl Coombs,et al.  The Morphology and Evolution of the Ear in Actinopterygian Fishes , 1982 .

[27]  I. Whitfield.  Discharge Patterns of Single Fibers in the Cat's Auditory Nerve , 1966 .

[28]  R. Fettiplace,et al.  The frequency selectivity of auditory nerve fibres and hair cells in the cochlea of the turtle , 1980, The Journal of physiology.

[29]  P. M. Shelton.  The lateral line system at metamorphosis in Xenopus laevis (Daudin). , 1970, Journal of embryology and experimental morphology.

[30]  H. de Vries,et al.  The microphonic activity of the lateral line , 1952, The Journal of physiology.

[31]  Jan Willem Kuiper,et al.  The microphonic effect of the lateral line organ: A study on the biophysics and the function of the lateral line organ of Acernina cernua L. , 1956 .

[32]  Torsten Pehrson.  THE SYSTEM OF PIT ORGAN LINES IN GYMNARCHUS NILOTICUS , 1945 .

[33]  J. Camhi.  Neural mechanisms of behavior , 1993, Current Opinion in Neurobiology.

[34]  Joseph G. Hoffman,et al.  Marine Bio‐Acoustics , 1965 .

[35]  I. J. Russell,et al.  Amphibian Lateral Line Receptors , 1976 .

[36]  C. J. Herrick.  The cranial nerves and cutaneous sense organs of the north american siluroid fishes , 1901 .

[37]  T. H. Bullock,et al.  Evolution of electroreception , 1982, Trends in Neurosciences.

[38]  L. Stone.  The development of lateral‐line sense organs in amphibians observed in living and vital‐stained preparations , 1933 .

[39]  M. Dodd,et al.  Evolutionary Biology of Primitive Fishes , 1985, NATO ASI Series.

[40]  Elke Blübaum-Gronau,et al.  The Lateral Line System of Surface-Feeding Fish: Anatomy, Physiology, and Behavior , 1989 .

[41]  P. J. Miller,et al.  A new goby (Teleostei: Gobiidae) from the South China Sea and its significance for gobioid classification , 1979 .

[42]  Olav Sand,et al.  The Lateral Line and Sound Reception , 1981 .

[43]  S. Gould,et al.  The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[44]  A. L. Megela.  Diversity of adaptation patterns in responses of eighth nerve fibers in the bullfrog, Rana catesbeiana. , 1984, The Journal of the Acoustical Society of America.

[45]  H. Heffner,et al.  Hearing range of the domestic cat , 1985, Hearing Research.

[46]  J. Kelly,et al.  Topography and mechanics of the cupula in the fish lateral line. I. Variation of cupular structure and composition in three dimensions , 1991, Journal of morphology.

[47]  J. M. Jørgensen.  Evolution of Octavolateralis Sensory Cells , 1989 .

[48]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[49]  A. S. Kapoor.  Development of dermal bones related to sensory canals of the head in the fishes Ophicephalus punctatus Bloch (Ophicephalidae) and Wallago attu Bl. & Schn. (Siluridae)* , 1970 .

[50]  N A Schellart,et al.  Velocity- and acceleration-sensitive units in the trunk lateral line of the trout. , 1992, Journal of neurophysiology.

[51]  R. Fay,et al.  Acoustic response and tuning in saccular nerve fibers of the goldfish (Carassius auratus). , 1986, The Journal of the Acoustical Society of America.

[52]  A. S. Kapoor.  Functional Morphology of Latero-sensory Canals in the Notopteridae (Pisces) , 1964 .

[53]  S. Smirnov,et al.  Sensory Organs of the Lateral-Line Canal System in Two Percids and Their Importance in Behavior , 1977 .

[54]  C. Moss,et al.  Behavioral audiograms of the bullfrog (Rana catesbeiana) and the green tree frog (Hyla cinerea). , 1985, The Journal of the Acoustical Society of America.

[55]  Bertil Lekander,et al.  The sensory line system and the canal bones in the head of some Ostariophysi , 1949 .

[56]  H. Norris.  Observations upon the peripheral distribution of the cranial nerves of certain ganoid fishes (amia Lepidosteus, Polyodon, Scaphirhynchus and Acipenser) , 1925 .

[57]  H. Ayers.  Vertebrate cephalogenesis. II. A contribution to the morphology of the vertebrate ear, with a reconsideration of its functions , 1892 .

[58]  Ad. J. Kalmijn,et al.  Behavioral Investigations on the Functions of the Lateral Line and Inner Ear in Predation , 1989 .

[59]  R. Fay.  Coding of Acoustic Information in the Eighth Nerve , 1981 .

[60]  G. A. Moore,et al.  Description of the Lateral-line System of the Pirate Perch, Aphredoderus sayanus' , 1956 .

[61]  R. Winklbauer,et al.  Development of the lateral line system in Xenopus laevis. I. Normal development and cell movement in the supraorbital system. , 1983, Journal of embryology and experimental morphology.

[62]  R. Winklbauer,et al.  Development of the lateral line system in Xenopus laevis. II. Cell multiplication and organ formation in the supraorbital system. , 1983, Journal of embryology and experimental morphology.

[63]  E. Allis.  The cranial muscles and cranial and first spinal nerves in amia calva , 1897 .

[64]  J. Gray,et al.  Interaction of sound pressure and particle acceleration in the excitation of the lateral-line neuromasts of sprats , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[65]  J. Gray,et al.  Acousticolateralis System in Clupeid Fishes , 1981 .

[66]  H. E. Karlsen,et al.  Detection of infrasound by the Atlantic cod. , 1986, The Journal of experimental biology.

[67]  Alfon B. A. Kroese,et al.  Sensory Transduction in Lateral Line Hair cells , 1989 .

[68]  R L Puzdrowski,et al.  Peripheral distribution and central projections of the lateral-line nerves in goldfish, Carassius auratus. , 1989, Brain, behavior and evolution.

[69]  F. Schulze.  Ueber die Sinnesorgane der Seitenlinie bei Fischen und Amphibien , 1870 .

[70]  C. A. Mccormick.  The organization of the octavolateralis area in actinopterygian fishes: A new interpretation , 1982, Journal of morphology.

[71]  Torsten Pehrson.  Some new interpretations of the skull in Polypterus , 1947 .

[72]  J. Cooper,et al.  Speoplatyrhinus poulsoni, A New Genus and Species of Subterranean Fish from Alabama , 1974 .

[73]  Sietse M. van Netten,et al.  Laser interferometric measurements on the dynamic behaviour of the cupula in the fish lateral line , 1987, Hearing Research.

[74]  S. Dijkgraaf.  THE FUNCTIONING and SIGNIFICANCE OF THE LATERAL‐LINE ORGANS , 1963, Biological reviews of the Cambridge Philosophical Society.

[75]  N. Disler.  Lateral line sense organs and their importance in fish behavior , 1971 .

[76]  E. Crossman,et al.  Surface pits in the family esocidae. II. Epidermal dermal interaction and evidence for aplasia of the lateral line sensory system , 1973, Journal of morphology.

[77]  Jelle Atema,et al.  Sensory Biology of Aquatic Animals , 1988, Springer New York.

[78]  W. K. Metcalfe.  Organization and Development of the Zebrafish Posterior Lateral Line , 1989 .

[79]  R. Fay,et al.  Hearing in Vertebrates: A Psychophysics Databook , 1988 .

[80]  N. B. Marshall.  Explorations in the life of fishes , 1965 .

[81]  Ad. J. Kalmijn,et al.  Hydrodynamic and Acoustic Field Detection , 1988 .

[82]  J F Webb,et al.  Gross morphology and evolution of the mechanoreceptive lateral-line system in teleost fishes. , 1989, Brain, behavior and evolution.

[83]  Richard R. Fay,et al.  Hearing and Sound Communication in Fishes , 1981, Proceedings in Life Sciences.

[84]  Ȧ. Larsson,et al.  Fluids and jellies of the acusticolateralis system in relation to body fluids in Coryphaenoides rupestris and other fishes , 1972, Marine Biology.

[85]  C. S. Bartheld.  Development and Innervation of the Paratympanic Organ (Vitali Organ) in Chick Embryos , 1990 .

[86]  P. S. Enger.  Acoustic threshold in goldfish and its relation to the sound source distance. , 1966, Comparative biochemistry and physiology.

[87]  R. Winklbauer,et al.  Development of the lateral line system in Xenopus laevis. IV. Pattern formation in the supraorbital system. , 1985, Journal of embryology and experimental morphology.

[88]  Van Bergeijk Wa.  The evolution of vertebrate hearing. , 1967 .

[89]  J. Montgomery.  Lateral Line Detection of Planktonic Prey , 1989 .

[90]  J. Gray,et al.  Nerve Fibre and Receptor Counts in the Sprat Utriculus and Lateral Line , 1982, Journal of the Marine Biological Association of the United Kingdom.

[91]  Accepted September,et al.  Single unit activity in the peripheral lateral line system of the cichlid fish Sarotherodon niloticus L. , 1985 .

[92]  H. Vischer.  The development of lateral-line receptors in Eigenmannia (Teleostei, Gymnotiformes). I. The mechanoreceptive lateral-line system. , 1989, Brain, behavior and evolution.

[93]  S. Appelbaum,et al.  Dermal sense organs and their significance in the feeding behaviour of the common sole Solea vulgaris , 1983 .

[94]  J. Gray,et al.  The rigidity of fish and patterns of lateral line stimulation , 1982, Nature.

[95]  R. Northcutt.  The Phylogenetic Distribution and Innervation of Craniate Mechanoreceptive Lateral Lines , 1989 .

[96]  S. V. Netten,et al.  Dynamic Behavior and Micromechanical Properties of the Cupula , 1989 .

[97]  Ad. J. Kalmijn,et al.  Functional Evolution of Lateral Line and Inner Ear Sensory Systems , 1989 .

[98]  H. Münz,et al.  Functional Organization of the Lateral Line Periphery , 1989 .

[99]  J. Montgomery,et al.  Sensory Tuning of Lateral Line Receptors in Antarctic Fish to the Movements of Planktonic Prey , 1987, Science.

[100]  B. Fernholm.  The Lateral Line System of Cyclostomes , 1985 .

[101]  N. B. Marshall.  Systematic and biological studies of the Macrourid fishes (Anacanthini-Teleostii)☆ , 1965 .

[102]  S. Coombs,et al.  Diversity of Lateral Line Systems: Evolutionary and Functional Considerations , 1988 .

[103]  Sheryl Coombs,et al.  Acoustic Detection by Fishes , 1980 .

[104]  R. Northcutt,et al.  Morphology, distribution and innervation of the lateral-line receptors of the Florida gar, Lepisosteus platyrhincus. , 1991, Brain, behavior and evolution.

[105]  W. Graham-Smith.  On the Lateral Lines and Dermal Bones in the Parietal Region of Some Crossopterygian and Dipnoan Fishes , 1978 .

[106]  T. H. Bullock,et al.  The phylogenetic distribution of electroreception: Evidence for convergent evolution of a primitive vertebrate sense modality , 1983, Brain Research Reviews.

[107]  R. Northcutt,et al.  Audition and the Central Nervous System of Fishes , 1981 .

[108]  M. V. Bennett,et al.  Specialized Lateral Line Receptor Systems in Elasmobranchs: The Spiracular Organs and Vesicles of Savi , 1989 .

[109]  N. Marshall.  Structure and general distribution of free neuromasts in the black goby, Gobius niger , 1986, Journal of the Marine Biological Association of the United Kingdom.

[110]  H. Garland,et al.  Altered renal function in chronically hyperprolactinaemic rats. , 1987, The Journal of physiology.

[111]  William Siler.  Near‐ and Farfields in a Marine Environment , 1969 .

[112]  Andreas Elepfandt,et al.  Wave Analysis by Amphibians , 1989 .