Abstract
Pectinidae, a large group of marine bivalves comprising more than 300 species worldwide, inhabit a diverse array of habitats, enabling an enormous radiation, and yielding many different life forms and adaptations. This apparent diversity led to the distinction of ecotypes based on shell morphology and lifestyle. Eyes in Pectinidae (Bivalvia, Pteriomorphia) have long sparked scientific interest and have been described for various species over the past two centuries. These eyes are morphologically and functionally highly complex. Despite this complexity, studies have focused mostly on functional aspects with only few examining the relationships associated with different environmental or evolutionary traits. Here, the pallial eye structure within the Pectinidae was examined using Masson Goldner Trichrom staining, and ancestral character estimation with BayesTraits was performed to reconstruct macro-evolutionary patterns. To evaluate the connection of substrate type and lifestyle to the evolution of eyes, we compared eyes within the major subgroups of Pectinidae while considering the different lifestyles and substrate types as well as different depth ranges. The results indicate a tendency towards a taxon-/clade-specific evolution in respect to characters such as the cornea and lens while depth specific adaptations occur mainly in the light sensitive compartments of the retina. Successive reduction of eyes seems to occur from shallow to deep water species and ends in a total reduction of all structures in deep sea species.
Similar content being viewed by others
References
Alejandrino, A., Puslednik, L., & Serb, J. M. (2011). Convergent and parallel evolution in life habit of the scallops (Bivalvia: Pectinidae). BMC Evolutionary Biology, 11, 164.
Brand, A. R. (2006). Chapter 12. Scallop Ecology: Distributions and Behavior. In S. E. Shumway & J. Parsons (Eds.), Scallops: Biology (Ecology and Aquaculture, 2nd edn, pp. 651–713). Elsevier: Amsterdam.
Butcher, E. O. (1930). The formation, regeneration, and transplantation of eyes in Pecten (Gibbus borealis). Biological Bulletin, 59(2), 154–164.
Ciocco, N. F. (1998). Anatomía de la "vieira tehuelche", Aequipecten tehuelchus (d'Orbigny, 1846) (=Chlamys tehuelcha). IV, Sistema nervioso y estructuras sensoriales (Bivalvia, Pectinidae). Revista de Biología Marina y Oceanografía, 33(1), 25–42.
Crocetta, F., & Spanu, M. (2008). Molluscs associated with a Sardinian deep water population of Corallium rubrum (Linné, 1758). Mediterranean Marine Science, 9(2), 63–85.
Cronin, T. W. (1986). Photoreception in marine invertebrates. American Zoologist, 26, 403–415.
Dakin, W. J. (1909). Pecten. Series: L.M.B.C. memoirs on typical British marine plants and animals 17 (pp. 1–136). London: Williams & Norgate. plates 1–9.
Dakin, W. J. (1910). The eye of Pecten. The Quarterly Journal of Microscopical Science, 55, 49–112. plates 6-7.
Dakin, W. J. (1928). The eyes of Pecten, Spondylus, Amussium and allied Lamellibranchs, with a short discussion on their evolution. Proceedings of the Royal Society London Series B, Containing Papers of a Biological Character, 103(725), 355–365.
Dijkstra, H. H. (1991). A contribution to the knowledge of the pectinacean Mollusca (Bivalvia: Propeamussiidae, Entoliidae, Pectinidae) from the Indonesian Archipelago. Zoologische Verhandelingen (Leiden), 271, 1–57.
Dijkstra, H. H., Warén, A., & Gudmundsson, G. (2009). Pectinoidea (Mollusca: Bivalvia) from Iceland. Marine Biology Research, 5, 207–243.
Drew, G. A. (1906). The habits anatomy, and embryology of the giant scallop. (Pecten tenuicostatus, Mighels) (pp. 1–71). Maine: Orono.
Freiwald, A., & Schönfeld, J. (1996). Substrate pitting and boring pattern of Hyrrokkin sarcophaga Cedhagen, 1994 (Foraminifera) in a modern deep-water coral reef mound. Marine Micropaleontology, 28, 199–207.
Gilkinson, K. D., & Gagnon, J. M. (1991). Substratum associations of natural populations of Iceland scallops, Chlamys islandica Müller 1776, on the northeastern Grand Bank of Newfoundland. American Malacological Bulletin, 9, 59–67.
Hautmann, M. (2010). The first scallop. Palaeontologische Zeitschrift, 84, 317–322.
Horváth, G., & Varjú, D. (1993). Theoretical study of the optimal shape of the front profile of the lens in the scallop, Pecten. Bulletin of Mathematical Biology, 55(1), 155–174.
Hrs-Brenko, M., & Legac, M. (2006). Inter- and intra-species relationships of sessile bivalves on the eastern coast of the Adriatic Sea. Natura Croatica, 15(4), 203–230.
Huber, M. (2010). Compendium of Bivalves (pp. 1–901). Hackenheim: Conchbooks.
Johnsen, S., & Sosik, H. (2004). Shedding Light on Light in the Ocean—new research is illuminating an optically complex environment. Oceanus Magazine, 43(2), 1–5.
Jonasova, K., & Kozmik, Z. (2008). Eye evolution: lens and cornea as an upgrade of animal visual system. Seminars in Cell & Developmental Biology, 19, 71–81.
Kosaka, Y., & Ito, H. (2006). Chapter 22. Japan. In S. E. Shumway & J. Parsons (Eds.), Scallops: Biology, Ecology and Aquaculture (2nd ed.). Amsterdam: Elsevier.
Küpfer, M. (1916). Entwicklungsgeschichtliche und neuro-histologische Beiträge zur Kenntnis der Sehorgane am Mantelrande der Pecten-Arten: mit anschliessenden vergleichend-anatomischen Betrachtungen (pp. 1–312). Jena: Fischer.
Land, M. F. (1965). Image formation by a concave reflector in the eye of the scallop, Pecten maximus. The Journal of Physiology, 179, 138–153.
Malkowsky, Y., & Klussmann-Kolb, A. (2012). Phylogeny and spatio-temporal distribution of European Pectinidae (Mollusca: Bivalvia). Systematics and Biodiversity, 10(2), 233–242.
Minchin, D. (2003). Introductions: some biological and ecological characteristics of scallops. Aquatic Living Resources, 16, 521–532.
Morton, B. (1980). Swimming in Amusium pleuronectes (Bivalvia: Pectinidae). Journal of Zoology, 190(3), 375–404.
Morton, B. (2000a). The pallial eyes of Ctenoides floridanus (Bivalvia: Limoidea). Journal of Molluscan Studies, 66, 449–455.
Morton, B. (2000b). The function of pallial eyes within the Pectinidae, with a description of those present in Patinopecten yessoensis. In E. M. Harper, J. D. Taylor, & J. A. Crame (Eds.), The Evolutionary Biology of the Bivalvia (pp. 247–255). London: Geological Society. Special Publications, 177.
Morton, B. (2001). The evolution of eyes in the Bivalvia. Oceanography and Marine Biology. An Annual Review, 39, 165–205.
Morton, B. (2008). The evolution of eyes in the Bivalvia: New Insights. American Malacological Bulletin, 26(1/2), 35–45.
Morton, B., & Thurston, M. H. (1989). The functional morphology of Propeamussium lucidum (Bivalvia: Pectinacea), a deep-sea predatory scallop. Journal of Zoology, 218(3), 471–496.
Otten, E. (1982). Vision in some percoid fishes: a study in functional morphology. In S. Peters (Ed.), Organismus und Anpassung. Aufsätze und Reden der Senckenbergischen Naturforschenden Gesellschaft (pp. 81–87). Frankfurt am Main: Kramer.
Pagel, M. (1994). Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society B, 255, 37–45.
Pagel, M., Meade, A., & Barker, D. (2004). Bayesian estimation of ancestral character states on phylogenies. Systematic Biology, 53, 673–684.
Patten, W. (1887). Eyes of Molluscs and Arthropods. Journal of Morphology, 1(1), 67–92. plate 3.
Piatigorsky, J. (2001). Enigma of the abundant water-soluble cytoplasmic proteins of the cornea—the “Refracton” Hypothesis. Cornea, 20(8), 853–858.
Poppe, G.T. & Goto, Y. (1993). European seashells Volume II. Verlag Christa Hemmen Wiesbaden, 1-221.
Puslednik, L., & Serb, J. M. (2008). Molecular phylogenetics of the Pectinidae (Mollusca: Bivalvia) and effect of increased taxon sampling and outgroup selection on tree topology. Molecular Phylogenetics and Evolution, 48, 1178–1188.
Raines, B. K., & Poppe, G. T. (2006). The Family Pectinidae. In G. T. Poppe & K. Groh (Eds.), A Conchological Iconography (pp. 1–722). Hackenheim: Conch Books.
Salvini-Plawen, L. V. (2008). Photoreception and the polyphyletic evolution of photoreceptors (with special reference to Mollusca). American Malacological Bulletin, 26(1/2), 83–100.
Speiser, D. I., & Johnsen, S. (2008a). Comparative morphology of the concave mirror eyes of scallops (Pectinoidea). American Malacological Bulletin, 26(1/2), 27–33.
Speiser, D. I., & Johnsen, S. (2008b). Scallops visually respond to the size and speed of virtual particles. The Journal of Experimental Biology, 211, 2066–2070.
Speiser, D. I., Loew, E. R., & Johnsen, S. (2011). Spectral sensitivity of the concave mirror eyes of scallops: potential influences of habitat, self-screening and longitudinal chromatic aberration. The Journal of Experimental Biology, 214, 422–431.
Stanley, S. M. (1970). Relation of shell form to life habits of the Bivalvia (Mollusca). Geological Society of America Memoir, 125, 1–296.
Stanley, S. M. (1972). Functional morphology and evolution of byssally attached bivalve mollusk. Journal of Paleontology, 46(2), 165–212.
Trigg, C., & Moore, C. G. (2009). Recovery of the biogenic nest habitat of Limaria hians (Mollusca: Limacea) following anthropogenic disturbance. Estuarine, Coastal and Shelf Science, 82, 351–356.
Viana, M. G., & Rocha-Barreira, C. A. (2007). The sensorial structures of Spondylus americanus Hermann, 1781 (Mollusca: Bivalvia, Spondylidae). Brazilian Archives of Biology and Technology, 50(5), 815–819.
Waller, T.R. (2006). Phylogeny of families in the Pectinoidea (Mollusca: Bivalvia): importance of the fossil record. In Bieler R (ed) Bivalvia—a look at the Branches. Zoological Journal of the Linnean Society, 148, 313–342.
Wilkens, L. A. (2008). Primary inhibition by light: A unique property of bivalve photoreceptors. American Malacological Bulletin, 26(1/2), 101–109.
Acknowledgements
We are very grateful to the following colleagues for the generous loan of material and hospitality in their laboratories: Dr. Bernhard Hausdorf (HH), Dr. Ronald Janssen (SMN), Dr. Kennet Lundin (Göteborg), and Dr. Anders Warén (SMNH). The following people and institutions assisted with collection of material: Dr. Michael Türkay (SMN) Observatoire Océanologique de Banyuls sur mer and Station Biologique Roscoff. Thanks also to Dipl. Biol. Juliane Vehof for her assistance with sectioning and staining and Dr. Eugenia Zarza-Franco and Dr. Jan Schnitzler for their introduction to BayesTraits. Thanks also go to Annette Klussmann-Kolb and the four anonymous reviewers for their unwavering efforts and most helpful comments on the manuscript. This research was funded by the Hessian initiative for the development of scientific and economic excellence (LOEWE) at the Biodiversity and Climate Research Centre (BiK-F), Frankfurt/Main.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Malkowsky, Y., Götze, MC. Impact of habitat and life trait on character evolution of pallial eyes in Pectinidae (Mollusca: bivalvia). Org Divers Evol 14, 173–185 (2014). https://doi.org/10.1007/s13127-013-0165-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13127-013-0165-z