Nacre was previously thought to be primitive in the Mollusca, but no convincing Cambrian examples are known. This aragonitic microstructure with crystal tablets that grow within an organic framework is thought to be the strongest, most fracture-resistant type of shell microstructure. Fossils described herein from the Ordovician of Iowa, Indiana, and Ohio provide supporting evidence for the hypothesis that sometime between the middle Cambrian and late Ordovician, nacre originated in cephalopod, bivalve, and possibly gastropod lineages. The correlation of independent origins of fracture-resistant nacre with increasing shell-crushing abilities of predators during the Cambrian-Ordovician suggests an early pulse in the evolutionary arms race between predators and molluscan prey.
References
[1]
Runnegar, B. Shell microstructures of Cambrian molluscs replicated by phosphate. Alcheringa 1985, 9, 245–257, doi:10.1080/03115518508618971.
[2]
Kouchinsky, A. Shell microstructures in Early Cambrian molluscs. Acta Palaeontol. Pol. 2000, 45, 119–150.
[3]
Vendrasco, M.J.; Porter, S.M.; Kouchinsky, A.; Li, G.; Fernandez, C.Z. New data on molluscs and their shell microstructures from the Middle Cambrian Gowers Formation, Australia. Palaeontology 2010, 53, 97–135, doi:10.1111/j.1475-4983.2009.00922.x.
[4]
Vendrasco, M.J.; Kouchinsky, A.V.; Porter, S.M.; Fernandez, C.Z. Phylogeny and escalation in Mellopegma and other Cambrian molluscs. Palaeontol. Electron. 2011, 14, 11A:1–11A:44.
[5]
Taylor, J.D.; Layman, M. The mechanical properties of bivalve (Mollusca) shell structures. Palaeontology 1972, 15, 73–87.
[6]
Currey, J.D. Shell form and strength. In The Mollusca, Volume 11: Form and Function; Wilbur, K.M., Trueman, E.R., Clarke, M.R., Eds.; Academic Press: San Diego, CA, USA, 1988; pp. 183–210.
[7]
Palmer, A.R. Relative cost of producing skeletal organic matrix versus calcification: Evidence from marine gastropods. Mar. Biol. 1983, 75, 287–292, doi:10.1007/BF00406014.
[8]
Palmer, A.R. Calcification in marine molluscs: How costly is it? Proc. Natl. Acad. Sci. USA 1992, 89, 1379–1382, doi:10.1073/pnas.89.4.1379.
[9]
Vendrasco, M.J.; Checa, A.G.; Kouchinsky, A.V. Shell microstructure of the early bivalve Pojetaia and the independent origin of nacre within the Mollusca. Palaeontology 2011, 54, 825–850, doi:10.1111/j.1475-4983.2011.01056.x.
[10]
Grégoire, C. On organic remains in shells of Paleozoic and Mesozoic cephalopods (Nautiloids and Ammonoids). Bull. Inst. R. Sci. Nat. Belg. 1966, 42, 1–36.
[11]
Mutvei, H. Flexible nacre in the nautiloid Isorthoceras, with remarks on the evolution of cephalopod nacre. Lethaia 1983, 16, 233–240, doi:10.1111/j.1502-3931.1983.tb00660.x.
[12]
Mutvei, H. Ultrastructural evolution of molluscan nacre. In Biomineralization and Biological Metal Accumulation; Westbroek, P., de Jong, E.W., Eds.; D. Reidel Publishing Company: Dordrecht, the Netherlands, 1983; pp. 267–271.
[13]
Carter, J.G.; Lawrence, D.R.; Sanders, H. Shell microstructural data for the Bivalvia. Part II. Orders Nuculoida and Solemyoida. In Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends; Carter, J.G., Ed.; Van Nostrand Reinhold: New York, NY, USA, 1990; Volume 1, pp. 303–319.
[14]
Baptista, B.M. Petrology of the Limestones of the Arnheim Formation (Cincinnatian Series) from Western Butler County, Ohio. Master’s Thesis, Miami University, Oxford, OH, USA, 1969.
[15]
Martin, A.J. A Paleoenvironmental Interpretation of the “Arnheim” Micromorph Fossil Assemblage from the Cincinnatian Series (Upper Ordovician), Southeastern Indiana and Southwestern Ohio. Master’s Thesis, Miami University, Oxford, Ohio, USA, 1986.
[16]
Meyer, D.L.; Davis, R.A. A Sea Without Fish; Indiana University Press: Bloomington, IN, USA, 2009.
[17]
Caster, K.E.; Dalve, E.A.; Pope, J.K. Elementary Guide to the Fossils and Strata of the Ordovician in the Vicinity of Cincinnati, Ohio; Cincinnati Museum of Natural History: Cincinnati, OH, USA, 1961.
[18]
Davis, R.A. Cincinnati Fossils, an Elementary Guide to the Ordovician Rocks and Fossils of the Cincinnati, Ohio, Region; Cincinnati Museum Center: Cincinnati, OH, USA, 1998.
[19]
Martin, A.J.; Martin, W.D.; Pope, J.K. Genesis of phosphatic sediments in Cincinnatian Series (Upper Ordovician), southeastern Indiana and southwestern Ohio. AAPG Bull. 1985, 69, 1441.
[20]
Martin, A.J.; Pope, J.K. Paleoenvironmental interpretation of a micromorph fossil assemblage from the Cincinnatian Series (Upper Ordovician), Indiana and Ohio. GSA Abstr. Programs 1985, 17, 653–654.
[21]
Holland, S.M. The type Cincinnatian Series: An overview. In Stratigraphic Renaissance in the Cincinnati Arch; McLaughlin, P.I., Brett, C.E., Holland, S.M., Storrs, G.W., Eds.; Cincinnati Museum Center: Cincinnati, OH, USA, 2008; pp. 173–184.
[22]
Holland, S.M. Department of Geology, The University of Georgia, Athens, GA, USA.
[23]
Baumann, S.D.J. Rock Outcrop of the Maquoketa Graf Section and Highway D-17 Section, Iowa, Lower Scales and Neda Formations; No. G-032009-1A; Midwest Institute of Geosciences and Engineering: Chicago, IL, USA, 2009. Available online: http://www.migeweb.org/ (accessed on 2 September 2012).
[24]
Miller, A.K.; Youngquist, W. The Maquoketa coquina of cephalopods. J. Paleontol. 1949, 23, 199–204.
[25]
Tasch, P. Paleoecologic observations on the orthoceratid coquina beds of the Maquoketa at Graf, Iowa. J. Paleontol. 1955, 29, 510–518.
[26]
Hay, H.B.; Cuffey, R.J. The “Brookville Formation” (“Excello,” Waynesville, and Liberty Members) at Bon Well Hill near Brookville (Upper Ordovician, southeastern Indiana). In Sampling the Layer Cake That Isn’t: The Stratigraphy and Paleontology of the Type-Cincinnatian; Ohio Division of Geological Survey Guidebook No. 13; Davis, R.A., Cuffey, R.J., Eds.; Ohio Division of Geological Survey: Columbus, OH, USA, 1998; pp. 79–83.
[27]
Hay, H.B.; Kirchner, B.; Cuffey, R.J. “Excello” (Arnheim) to basal Saluda strata on Indiana Route 1 at South Gate Hill (Upper Ordovician, southeastern Indiana). In Sampling the Layer Cake That Isn’t: The Stratigraphy and Paleontology of the Type-Cincinnatian; Ohio Division of Geological Survey Guidebook No. 13; Davis, R.A., Cuffey, R.J., Eds.; Ohio Division of Geological Survey: Columbus, OH, USA, 1998; pp. 89–94.
[28]
Grandjean, J.; Grégoire, Ch.; Lutts, A. On the mineral components and the remnants of organic structures in shells of fossil molluscs. Bull. Acad. R. Sci. Nat. Belg. 1964, 50, 562–595.
[29]
Prév？t, L.; Lucas, J. Microstructure of apatite-replacing carbonate in synthesized and natural samples. J. Sediment. Pet. 1986, 56, 153–159.
[30]
Balthasar, U. Mummpikia gen. nov. and the origin of Calcitic-shelled Brachiopods. Palaeontology 2008, 51, 263–279, doi:10.1111/j.1475-4983.2008.00754.x.
[31]
Carter, J.G.; Bandel, K.; de Buffrénil, V.; Carlson, S.J.; Castanet, J.; Crenshaw, M.A.; Dalingwater, J.E.; Francillon-Vieillot, H.; Géraudie, J.; Meunier, F.J.; et al. Glossary of skeletal biomineralization. In Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends; Carter, J.G., Ed.; Van Nostrand Reinhold: New York, NY, USA, 1990; Volume 1, pp. 609–671.
[32]
Carter, J.G. Evolutionary significance of shell microstructure in the Palaeotaxodonta, Pteriomorphia and Isofilibranchia (Bivalvia: Mollusca). In Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends; Carter, J.G., Ed.; Van Nostrand Reinhold: New York, NY, USA, 1990; Volume 1, pp. 135–296.
[33]
Carter, J.G. Shell and ligament microstructure of selected Silurian and Recent palaeotaxodonts (Mollusca: Bivalvia). Am. Malacol. Bull. 2001, 16, 217–238.
[34]
Checa, A.; Ramírez, J.; González-Segura, A.; Sánchez-Navas, A. Nacre and false nacre (foliated aragonite) in extant monoplacophorans (=Triblidiida: Mollusca). Naturwissenschaften 2009, 96, 111–122, doi:10.1007/s00114-008-0461-1.
[35]
Checa, A.; Sánchez-Navas, A.; Rodríguez-Navarro, A. Crystal growth in the foliated aragonite of monoplacophorans (Mollusca). Cryst. Growth Des. 2009, 9, 4574–4580, doi:10.1021/cg9005949.
Feng, W.; Sun, W. Phosphate replicated and replaced microstructure of molluscan shells from the earliest Cambrian of China. Acta Palaeontol. Pol. 2003, 48, 21–30.
[38]
Qian, Y.; Bengtson, S. Palaeontology and Biostratigraphy of the Early Cambrian Meishucunian Stage in Yunnan Province, South China; Fossils and strata series; Universitetsforlaget: Oslo, Norway, 1989; pp. 1–156.
[39]
Kouchinsky, A. Shell microstructures of the Early Cambrian Anabarella and Watsonella as new evidence on the origin of the Rostroconchia. Lethaia 1999, 32, 173–180, doi:10.1111/j.1502-3931.1999.tb00537.x.
[40]
Runnegar, B.; Pojeta, J., Jr. The earliest bivalves and their Ordovician descendents. Am. Malacol. Bull. 1992, 9, 117–122.
[41]
Vendrasco, M.J.; Li, G.; Porter, S.M.; Fernandez, C.Z. New data on the enigmatic Ocruranus-Eohalobia group of early Cambrian small skeletal fossils. Palaeontology 2009, 52, 1373–1396, doi:10.1111/j.1475-4983.2009.00913.x.
[42]
Porter, S.M. Seawater chemistry and early carbonate biomineralization. Science 2007, 316, 1302, doi:10.1126/science.1137284.
Carter, J.G.; Barrera, E.; Tevesz, M.J.S. Thermal potentiation and mineralogical evolution in the Bivalvia (Mollusca). J. Paleontol. 1998, 72, 991–1010.
[45]
Carter, J.G.; Seed, R. Thermal potentiation and mineralogical evolution in Mytilus (Mollusca: Bivalvia). In Bivalves: An Eon of Evolution—Paleobiological Studies Honouring Norman D. Newell; Johnston, P.A., Haggart, J.W., Eds.; University of Calgary Press: Calgary, Canada, 1998; pp. 87–117.
[46]
Carter, J.G.; Clark, G.R., II. Classification and phylogenetic significance of molluscan shell microstructure. In Mollusks, Notes for a Short Course; Broadhead, T.W., Ed.; University of Tennessee: Knoxville, TN, USA, 1985; pp. 50–71.
[47]
Marie, B.; Marin, F.; Marie, A.; Bédouet, L.; Dubost, L.; Alcaraz, G.; Milet, C.; Luquet, G. Evolution of nacre: Biochemistry and proteomics of the shell organic matrix of the cephalopod Nautilus macromphalus. ChemBioChem 2009, 10, 1495–1506, doi:10.1002/cbic.200900009.
[48]
Jackson, D.J.; McDougall, C.; Woodcroft, B.; Moase, P.; Rose, R.A.; Kube, M.; Reinhardt, R.; Rokhsar, D.S.; Montagnani, C.; Joubert, C.; et al. Marallel evolution of nacre building gene sets in molluscs. Mol. Biol. Evol. 2010, 27, 591–608, doi:10.1093/molbev/msp278.
[49]
Druschchits, V.V.; Doguzhayeva, L.A.; Korinevskiy, V.G. Shell microstructure of the Ordovician monoplacophoran Romaniella Doguzhaeva, 1972. Dokl. Akad. Nauk SSR 1979, 245, 458–461.
[50]
West, K.; Cohen, A. Shell microstructure of gastropods from Lake Tanganyika. Evolution 1996, 50, 672–681, doi:10.2307/2410840.
[51]
Stanley, S.M. Influence of seawater chemistry on biomineralization throughout Phanerozoic time: Paleontological and experimental evidence. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2006, 232, 214–236, doi:10.1016/j.palaeo.2005.12.010.
[52]
Vermeij, G.J. Evolution and Escalation; Princeton University Press: Princeton, NJ, USA, 1987.
[53]
Bengtson, S. Origins and early evolution of predation. In The Fossil Record of Predation, Paleontological Society Papers; Kowalewski, M., Kelley, P.H., Eds.; The Paleontological Society: Boulder, CO, USA, 2002; Volume 8, pp. 289–317.
[54]
Alexander, R.R. Resistance to and repair of shell breakage induced by durophages in Late Ordovician brachiopods. J. Paleontol. 1986, 60, 273–285.
[55]
Blake, D.B.; Guensburg, T.E. Predation by the Ordovician asteroid Promopalaeaster on a pelecypod. Lethaia 1994, 27, 235–239.
[56]
Ausich, W.I.; Baumiller, T.K. Column regeneration in an Ordovician crinoid (Echinodermata): paleobiologic implications. J. Paleontol. 1993, 67, 1068–1070.
[57]
Donovan, S.K.; Schmidt, D.A. Survival of crinoid stems following decapitation: Evidence from the Ordovician and palaeobiological implications. Lethaia 2001, 34, 263–270, doi:10.1080/002411601753293015.
[58]
Baumiller, T.K.; Gahn, F.J. Fossil record of parasitism on marine invertebrates with special emphasis on the platyceratid-crinoid interaction. In The Fossil Record of Predation, Paleontological Society Papers; Kowalewski, M., Kelley, P.H., Eds.; The Paleontological Society: Boulder, CO, USA, 2002; Volume 8, pp. 195–209.
[59]
Babcock, L.E. Trilobites in Paleozoic predator-prey systems, and their role in reorganization of Early Paleozoic ecosystems. In Predator-Prey Interactions in the Fossil Record; Kelley, P.H., Kowalewski, M., Eds.; Kluwer/Plenum: New York, NY, USA, 2003; pp. 55–92.
[60]
Bruton, D.L. The arthropod Sidneyia inexpectans, Middle Cambrian, Burgess Shale, British Columbia. Phil. Trans. R. Soc. Lond. B 1981, 295, 619–653, doi:10.1098/rstb.1981.0164.
[61]
Signor, P.W.; Vermeij, G.J. The plankton and the benthos: Origins and early history of an evolving relationship. Paleobiology 1994, 20, 297–319.
[62]
Ebbestad, J.O.; Peel, J.S. Attempted predation and shell repair in Middle and Upper Ordovician gastropods from Sweden. J. Paleont. 1997, 71, 1007–1019.
[63]
Brett, C.E. Durophagous predation in Paleozoic marine benthic assemblages. In Predator-Prey Interactions in the Fossil Record; Kelley, P.H., Kowalewski, M., Eds.; Kluwer/Plenum: New York, NY, USA, 2003; pp. 401–432.
[64]
Kr？ger, B. Large shell injuries in Middle Ordovician Orthocerida (Nautiloidea, Cephalopoda). GFF 2004, 126, 311–316, doi:10.1080/11035890401263311.
[65]
Skovsted, C.B.; Brock, G.A.; Lindstr？m, A.; Peel, J.S.; Paterson, J.R.; Fuller, M.K. Early Cambrian record of failed durophage and shell repair in an epibenthic mollusc. Biol. Lett. 2007, 3, 314–317, doi:10.1098/rsbl.2007.0006.
[66]
Kr？ger, B.; Landing, E. Cephalopods and paleoenvironments of the Fort Cassin Formation (Upper Lower Ordovician), eastern New York and adjacent Vermont. J. Paleont. 2009, 83, 664–693, doi:10.1666/08-181.1.
