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The Science of Nature

, 102:65 | Cite as

Denticle-embedded ampullary organs in a Cretaceous shark provide unique insight into the evolution of elasmobranch electroreceptors

  • Romain Vullo
  • Guillaume Guinot
Original Paper

Abstract

Here, we report a novel type of dermal denticle (or placoid scale), unknown among both living and fossil chondrichthyan fishes, in a Cretaceous lamniform shark. By their morphology and location, these dermal denticles, grouped into clusters in the cephalic region, appear to have been directly associated with the electrosensory ampullary system. These denticles have a relatively enlarged (∼350 μm in diameter), ornamented crown with a small (∼100 μm) asterisk- or cross-shaped central perforation connected to a multi-alveolate internal cavity. The formation of such a complex structure can be explained by the annular coalescence and fusion, around an ampullary vesicle, of several developmental units still at papillary stage (i.e. before mineralization), leading to a single denticle embedding an alveolar ampulla devoid of canal. This differs from larger typical ampullae of Lorenzini with a well-developed canal opening in a pore of the skin and may represent another adaptive response to low skin resistance. Since it has been recently demonstrated that ampullary organs arise from lateral line placodes in chondrichthyans, this highly specialized type of dermal denticle (most likely non-deciduous) may be derived from the modified placoid scales covering the superficial neuromasts (pit organs) of the mechanosensory lateral line system of many modern sharks.

Keywords

Chondrichthyes Lamniformes Cretaceous Dermal denticle Electrosensory ampullary system 

Notes

Acknowledgments

We are extremely grateful to G. Barbe for donating the specimen to the UM collections. We thank A.-M. Damiano for the documentation, P. Janvier for the discussion, V. Perrichot for the technical assistance and A. Piuz for the SEM imaging. We also thank the three anonymous reviewers for their constructive comments. G.G. was funded by the Swiss National Science Foundation (200021-140827).

References

  1. Andres KH, von Düring M (1988) Comparative anatomy of vertebrate electroreceptors. In: Hamann W, Iggo A (eds) Transduction and cellular mechanisms in sensory receptors. Progress in Brain Research 74 113–131Google Scholar
  2. Baker CVH, Modrell MS, Gillis JA (2013) The evolution and development of vertebrate lateral line electroreceptors. J Exp Biol 216:2515–2522CrossRefPubMedGoogle Scholar
  3. Budker P (1938) Les cryptes sensorielles et les denticules cutanés des plagiostomes. Ann Inst Oceanogr 18:207–288Google Scholar
  4. Camilieri-Asch V, Kempster RM, Collin SP, Johnstone RW, Theiss SM (2013) A comparison of the electrosensory morphology of a euryhaline and a marine stingray. Zoology 116:270–276CrossRefPubMedGoogle Scholar
  5. Cappetta H, Case GR (1975) Sélaciens nouveaux du Crétacé du Texas. Geobios 8:303–307CrossRefGoogle Scholar
  6. Cavin L, Tong H, Boudad L, Meister C, Piuz A, Tabouelle J, Aarab M, Amiot R, Buffetaut E, Dyke G, Hua S, Le Lœuff J (2010) Vertebrate assemblages from the early Late Cretaceous of southeastern Morocco: an overview. J Afr Earth Sci 57:391–412CrossRefGoogle Scholar
  7. Donoghue PC (2002) Evolution of development of the vertebrate dermal and oral skeletons: unraveling concepts, regulatory theories, and homologies. Paleobiology 28:474–507CrossRefGoogle Scholar
  8. Freitas R, Zhang G, Albert JS, Evans DH, Cohn MJ (2006) Developmental origin of shark electrosensory organs. Evol Dev 8:74–80CrossRefPubMedGoogle Scholar
  9. Gillis JA, Modrell MS, Northcutt RG, Catania KC, Luer CA, Baker CVH (2012) Electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes. Development 139:3142–3146CrossRefPubMedGoogle Scholar
  10. Green SA, Simoes-Costa M, Bronner ME (2015) Evolution of vertebrates as viewed from the crest. Nature 520:474–482CrossRefPubMedGoogle Scholar
  11. Hueter RE, Mann DA, Maruska KP, Sisneros JA, Demski LS (2004) Sensory biology of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 325–368Google Scholar
  12. Jørgensen JM (2005) Morphology of electroreceptive sensory organs. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer Handbook of Auditory Research, vol 21. New York, pp 47–67CrossRefGoogle Scholar
  13. Kajiura SM (2001) Head morphology and electrosensory pore distribution of carcharhinid and sphyrnid sharks. Environ Biol Fish 61:125–133CrossRefGoogle Scholar
  14. Kajiura SM, Cornett AD, Yopak KE (2010) Sensory adaptations to the environments: electroreceptors as a case study. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives II—biodiversity, adaptive physiology, and conservation. CRC Press, Boca Raton, pp 393–433CrossRefGoogle Scholar
  15. Kitamura N (2013) “Carchariasamonensis (Chondrichthyes, Odontaspididae) from the Upper Cretaceous Mifune group in Kumamoto, Japan. Paleontol Res 17:230–235CrossRefGoogle Scholar
  16. Lee RTH, Thiery JP, Carney TJ (2013) Dermal fin rays and scales derive from mesoderm, not neural crest. Curr Biol 23:R336–R337CrossRefPubMedGoogle Scholar
  17. Martill DM, Ibrahim N, Brito PM, Baider L, Zhouri S, Loveridge R, Naish D, Hing R (2011) A new Plattenkalk Konservat Lagerstätte in the Upper Cretaceous of Gara Sbaa, south-eastern Morocco. Cretac Res 32:433–446CrossRefGoogle Scholar
  18. McKenzie RW, Motta PJ, Rohr JR (2014) Comparative squamation of the lateral line canal pores in sharks. J Fish Biol 84:1300–1311CrossRefPubMedGoogle Scholar
  19. Meyer W, Seegers U (2012) Basics of skin structure and function in elasmobranchs: a review. J Fish Biol 80:1940–1967CrossRefPubMedGoogle Scholar
  20. Mongera A, Nüsslein-Volhard C (2013) Scales of fish arise from mesoderm. Curr Biol 23:R338–R339CrossRefPubMedGoogle Scholar
  21. Néraudeau D, Allain R, Perrichot V, Videt B, Lapparent de Broin F de, Guillocheau F, Philippe M, Rage J-C, Vullo R (2003) Découverte d’un dépôt paralique à bois fossiles, ambre insectifère et restes d’Iguanodontidae (Dinosauria, Ornithopoda) dans le Cénomanien inférieur de Fouras (Charente-Maritime, Sud-Ouest de la France). C R Palevol 2:221–230Google Scholar
  22. Ørvig T (1972) The latero-sensory component of the dermal skeleton in lower vertebrates and its phyletic significance. Zool Scr 1:139–155CrossRefGoogle Scholar
  23. Peach MB, Marshall NJ (2009) The comparative morphology of pit organs in elasmobranchs. J Morphol 270:688–701CrossRefPubMedGoogle Scholar
  24. Peach MB, Rouse GW (2004) Phylogenetic trends in the abundance and distribution of pit organs of elasmobranchs. Acta Zool 85:233–244CrossRefGoogle Scholar
  25. Petit G, Budker P (1935) Sur la différenciation de dents cutanées, liée à la présence de cryptes sensorielles, chez quelques sélaciens. C R Hebd Séances Acad Sci 201:737–740Google Scholar
  26. Pradel A, Tafforeau P, Maisey JG, Janvier P (2011) A new Paleozoic Symmoriiformes (Chondrichthyes) from the Late Carboniferous of Kansas (USA) and cladistic analysis of early chondrichthyans. PLoS ONE 6:e24938PubMedCentralCrossRefPubMedGoogle Scholar
  27. Raschi W (1986) A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces, Rajoidei). J Morphol 189:225–247CrossRefGoogle Scholar
  28. Raschi W, Mackanos LA (1989) The structure of the ampullae of Lorenzini in Dasyatis garouaensis and its implications on the evolution of the freshwater electroreceptive systems. J Exp Zool 252(Suppl 2):101–111CrossRefGoogle Scholar
  29. Raschi W, Keithan ED, Rhee WCH (1997) Anatomy of the ampullary electroreceptor in the freshwater stingray, Himantura signifer. Copeia 1997:101–107CrossRefGoogle Scholar
  30. Reif W-E (1978) Type of morphogenesis of the dermal skeleton in fossil sharks. Paläeontol Z 52:110–128CrossRefGoogle Scholar
  31. Reif W-E (1985) Squamation and ecology of sharks. Cour Forsch Inst Senckenberg 78:1–255Google Scholar
  32. Reif W-E, Richter M (2001) Revisiting the lepidomorial and the odontode regulation theories of dermo-skeletal morphogenesis. N Jb Geol Paläont (Abh) 219:285–304Google Scholar
  33. Sallan LC, Coates MI (2014) The long-rostrumed elasmobranch Bandringa Zangerl, 1969, and taphonomy within a Carboniferous shark nursery. J Vertebr Paleontol 34:22–33CrossRefGoogle Scholar
  34. Shimada A, Kawanishi T, Kaneko T, Yoshihara H, Yano T, Inohaya K, Kinoshita M, Kamei Y, Tamura K, Takeda H (2013) Trunk exoskeleton in teleosts is mesodermal in origin. Nat Commun 4:1639PubMedCentralCrossRefPubMedGoogle Scholar
  35. Szabo T, Kalmijn AJ, Enger PS, Bullock TH (1972) Microampullary organs and a submandibular sense organ in the fresh water ray, Potamotrygon. J Comp Physiol 79:15–27CrossRefGoogle Scholar
  36. Theiss SM, Collin SP, Hart NS (2011) Morphology and distribution of the ampullary electroreceptors in wobbegong sharks: implications for feeding behaviour. Mar Biol 158:723–735CrossRefGoogle Scholar
  37. Tricas TC (2001) The neuroecology of the elasmobranch electrosensory world: why peripheral morphology shapes behavior. Environ Biol Fish 60:77–92CrossRefGoogle Scholar
  38. Vullo R, Guinot G, Barbe G (2014) A case of parallelism between a mid-Cretaceous lamniform and modern carcharhiniform sharks. J Vertebr Paleontol Program Abstr 2014:250–251Google Scholar
  39. Wada H, Iwasaki M, Kawakami K (2014) Development of the lateral line canal system through a bone remodeling process in zebrafish. Dev Biol 392:1–14CrossRefPubMedGoogle Scholar
  40. Webb JF (2014) Morphological diversity, development, and evolution of the mechanosensory lateral line system. In: Coombs S, Bleckmann H, Fay RR, Popper AN (eds) The lateral line system. Springer Handbook of Auditory Research, vol 48. New York, pp 17–72CrossRefGoogle Scholar
  41. Whitehead DL (2002) Ampullary organs and electroreception in freshwater Carcharhinus leucas. J Physiol Paris 96:391–395CrossRefPubMedGoogle Scholar
  42. Whitehead DL, Gauthier ARG, Mu EWH, Bennett MB, Tibbetts IR (2015) Morphology of the ampullae of Lorenzini in juvenile freshwater Carcharhinus leucas. J Morphol 276:481–493CrossRefPubMedGoogle Scholar
  43. Wonsettler AL, Webb JF (1997) Morphology and development of the multiple lateral line canals on the trunk in two species of Hexagrammos (Scorpaeniformes, Hexagrammidae). J Morphol 233:195–214CrossRefGoogle Scholar
  44. Wueringer BE (2012) Electroreception in elasmobranchs: sawfish as a case study. Brain Behav Evol 80:97–107CrossRefPubMedGoogle Scholar
  45. Yano K, Goto M, Yabumoto Y (1997) Dermal and mucous denticles of a female megamouth shark, Megachasma pelagios, from Hakata Bay, Japan. In: Yano K, Morrissey JF, Yabumoto Y, Nakaya K (eds) Biology of the megamouth shark. Tokai University Press, Tokyo, pp 77–91Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Géosciences Rennes, UMR CNRS 6118Université de Rennes 1RennesFrance
  2. 2.Département de Géologie et PaléontologieMuséum d’Histoire Naturelle de GenèveGeneva 6Switzerland
  3. 3.Institut des Sciences de l’Evolution, UMR CNRS 5554Université de MontpellierMontpellierFrance

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