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Direct measurement of age in fossil Gryphaea: the solution to a classic problem in heterochrony

Published online by Cambridge University Press:  20 May 2016

Douglas S. Jones  and
Stephen Jay Gould
Douglas S. Jones
Affiliation:
Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611
Stephen Jay Gould
Affiliation:
Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138
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Abstract

We have known since Trueman's classic work of 1922 that the Lower Jurassic Gryphaea of Britain exhibit phyletic size increase and heterochronic change in shape. Since Hallam's revisionary work in the 1960s, we have recognized that pronounced and generalized juvenilization of form accompanied this increasing size. This extensive literature provides invertebrate paleontology's most famous example of a biometrically documented, continuous anagenetic trend within a discrete lineage. But Gryphaea has also provoked great frustration because a key datum, required for a full solution, had been theoretically recognized but practically unavailable. We could identify the evolution of shape as paedomorphic, but could not specify the mode of heterochrony for this paedomorphic result because we could not standardize samples by common age or developmental stage.

In this paper, we provide sclerochronological data on sizes and shapes at specified ages marked by annual growth bands in two Jurassic sequences of Gryphaea: the classic Lower Jurassic series showing phyletic size increase with paedomorphosis, and an independent Middle–Upper Jurassic series illustrating neither size increase nor heterochrony. We prove that size increase in the classic series occurs entirely by faster growth (larger descendant sizes at the same ages as ancestors), and not by extended age (for descendants lived no longer than ancestors). The well-marked paedomorphosis of form probably arose as a correlated consequence of growing larger by extending and maintaining rapid juvenile growth rates—thus marking the heterochronic mode as a case of neoteny. The independent upper sequence, acting as a different replicate in a natural experiment, shows neither size increase nor heterochrony but does exhibit (in contrast with the classic sequence) evolution toward greater longevity.

Hallam's flow tank experiments indicated a strong adaptive advantage in shell stability for both larger size and paedomorphic form. Neotenous development provides an evolutionary pathway to the simultaneous acquisition of both favored traits—thus showing that “constraints” due to “correlations of growth” (Darwin's own phrase for the phenomenon) may be positive in promoting joint evolutionary advantages, and not only neutral (in carrying spandrels along with primary adaptations), or negative (by imposing inadaptive “baggage” upon trends in form through developmental correlation with selected traits).

Type
Articles
Information
Paleobiology , Volume 25 , Issue 2 , Spring 1999 , pp. 158 - 187
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Anderson, T. F. and Arthur, M. A. 1983. Stable isotopes of oxygen and carbon and their application to sedimentologic and environmental problems. In Arthur, M. A., organizer. Stable isotopes in sedimentary geology. SEPM Short Course 10: 1–151.Google Scholar
Barker, R. M. 1964. Microtextural variation in pelecypod shells. Malacologia 2: 69–86.Google Scholar
Barker, R. M. 1970. Constituency and origins of cyclic growth layers in pelecypod shells. Ph.D. dissertation. University of California, Berkeley.Google Scholar
Bayer, J. J. 1709. Oryktografia norica. W. Michaelis, Nuremberg.Google Scholar
Bertrand, E. 1763. Dictionnaire universel des fossiles propres et des fossiles accidentels. L. Chambeau, Avignon.Google Scholar
Burnaby, T. P. 1965. Reversed coiling trend in Gryphaea arcuata. Geological Journal 4: 257–278.Google Scholar
Carter, J. G. 1990. Shell microstructural data for the Bivalvia, Part IV. Order Ostreoida. pp. 347–362in Carter, J. G. ed. Skeletal biomineralization: patterns, processes and evolutionary trends, Vol. I. Van Nostrand Reinhold, New York.Google Scholar
Clark, G. R. II. 1974. Growth lines in invertebrate skeletons. Annual Review of Earth and Planetary Sciences 2: 77–99.Google Scholar
Cope, J. C. W. 1995. Introduction to the British Jurassic. pp. 1–7in Taylor, P. D. ed. Field geology of the British Jurassic. Geological Society of London.Google Scholar
Cope, J. C. W., Getty, T. A., Howarth, M. K., Morton, N., and Torrens, H. S. 1980. A correlationof Jurassic rocks in the British Isles, Part 1. Introduction and Lower Jurassic. Geological Society of London Special Report 14.Google Scholar
Cope, J. C. W., Duff, K. L., Parsons, C. F., Torrens, H. S., Wimbledon, W. A., and Wright, J. K. 1980. A correlation of Jurassic rocks in the British Isles, Part 2. Middle and Upper Jurassic. Geological Society of London Special Report 15.Google Scholar
Cox, L. R. and Nuttall, C. P. 1969. Geometry of shell. Pp. N84–N91in Mollusca 6, Vol. 1. Part N ofMoore, R. C. ed. Treatise on invertebrate paleontology. Geological Society of America and University of Kansas, Boulder, Colo.Google Scholar
Duff, K. 1991. Bivalves. pp. 35–77in Martill, D. M., Hudson, J. D. eds. Fossils of the Oxford Clay. Palaeontological Association, London.Google Scholar
Emerson, S. B. 1986. Heterochrony and frogs: the relationship of a life history trait to morphologic form. American Naturalist 127: 167–183.Google Scholar
Epstein, S., Buchsbaum, R., Lowenstam, H., and Urey, H. 1953. Revised carbonate-water isotopic temperature scale. Geological Society of America Bulletin 64: 1315–1326.Google Scholar
Fritts, H. C. 1976. Tree rings and climate. Academic Press, London.Google Scholar
Gallucci, V. F. and Quinn, T. J. II. 1979. Reparameterizing, fitting, and testing a simple growth model. Transactions of the American Fisheries Society 108: 14–25.Google Scholar
Gould, S. J. 1972. Allometric fallacies and the evolution of Gryphaea: a new interpretation based on White's criterion of geometric similarity. In Dobzhansky, T., Hecht, M. K., Steere, W. C. eds. Evolutionary Biology 6: 91–119.Google Scholar
Gould, S. J. 1977. Ontogeny and phylogeny. Belknap Press, Harvard University Press, Cambridge.Google Scholar
Gould, S. J. 1980. The evolution of Gryphaea. Arno, New York.Google Scholar
Gould, S. J. 1988. The uses of heterochrony. pp. 1–13in McKinney 1988a.CrossRefGoogle Scholar
Gould, S. J. 1989. A developmental constraint in Cerion, with comments on the definition and interpretation of constraint in evolution. Evolution 43: 516–539.Google ScholarPubMed
Gould, S. J. 1997a. Theory of the living earth. Natural History Magazine 05 1997: 18–21. 58–64.Google Scholar
Gould, S. J. 1997b. Questioning the millennium. Hamony Books, New York.Google Scholar
Gradstein, F. M., Agterberg, F. P., Ogg, J. G., Hardenbol, J., Veen, P. V., Thierry, J., and Huang, Z. 1995. A Triassic, Jurassic, and Cretaceous time scale. pp. 95–126in Berggren, W. A., Kent, D. V., Aubry, M.-P., Hardenbol, J. eds., Geochronology, time scales and global stratigraphic correlation. SEPM Special Publication 54.Google Scholar
Grizzle, R. E. and Lutz, R. A. 1988. Descriptions of macroscopic banding patterns in sectioned polished shells of Mercenaria mercenaria from southern New Jersey. Journal of Shellfish Research 7: 367–370.Google Scholar
Grossman, E. L. and Ku., T-L. 1986. Oxygen and carbon isotopic fractionation in biogenic aragonite: temperature effects. Chemical Geology (Isotope Geoscience Section) 59: 59–74.Google Scholar
Hallam, A. 1959. On the supposed evolution of Gryphaea in the Lias. Geological Magazine 96: 99–108.Google Scholar
Hallam, A. 1968. Morphology, palaeoecology and evolution of the genus Gryphaea in the British Lias. Philosophical Transactions of the Royal Society of London B 254: 91–128.Google Scholar
Hallam, A. 1982. Patterns of speciation in Jurassic Gryphaea. Paleobiology 8: 354–366.Google Scholar
Hallam, A. and Gould, S. J. 1975. The evolution of British and American Middle and Upper Jurassic Gryphaea: a biometrical study. Proceedings of the Royal Society of London B 189: 511–542.Google Scholar
Haskin, H. H. 1954. Age determination in mollusks. Transactions of the New York Academy of Sciences 16: 300–304.Google Scholar
Heller, J. 1990. Longevity in molluscs. Malacologia 31: 259–295.Google Scholar
Hudson, J. H., Shinn, E., Halley, R., and Lidz, B. 1976. Sclerochronology: a new tool for interpreting past environments. Geology 4: 361–364.Google Scholar
Johnson, A. L. A. 1993. Punctuated equilibria vs. phyletic gradualism in European Jurassic Gryphaea evolution. Proceedings of the Geologists' Association 104: 209–222.Google Scholar
Johnson, A. L. A. 1994. Evolution of European Lower Jurassic Gryphaea (Gryphaea) and contemporaneous bivalves. Historical Biology 7: 167–186.Google Scholar
Jones, C. E., Jenkyns, H. C., and Hesselbo, S. P. 1994. Strontium isotopes in Early Jurassic seawater. Geochimica et Cosmochimica Acta 58: 1285–1301.Google Scholar
Jones, D. S. 1980. Annual cycle of shell growth increment formation in two continental shelf bivalves and its paleobiological significance. Paleobiology 6: 331–340.Google Scholar
Jones, D. S. 1983. Sclerochronology: reading the record of the molluscan shell. American Scientist 71: 384–391.Google Scholar
Jones, D. S. 1988. Sclerochronology and the size versus age problem. pp. 93–108in McKinney, 1988a.Google Scholar
Jones, D. S. and Quitmyer, I. R. 1996. Marking time with bivalve shells: oxygen isotopes and season of annual increment formation. Palaios 11: 340–346.Google Scholar
Jones, D. S., Thompson, I., and Ambrose, W. G. 1978. Age and growth rate determinations for the Atlantic surf clam Spisula solidissima based on internal growth lines in shell cross-sections. Marine Biology 47: 63–70.CrossRefGoogle Scholar
Jones, D. S., Williams, D. F., and Arthur, M. A. 1983. Growth history and ecology of the Atlantic surf clam, Spisula solidissima (Dillwyn), as revealed by stable isotopes and annual shell increments. Journal of Experimental Marine Biology and Ecology 73: 225–242.Google Scholar
Jones, D. S., Quitmyer, I. R., Arnold, W. S., and Marelli, D. C. 1990. Annual shell banding, age, and growth rate of hard clams (Mercenaria spp.) from Florida. Journal of Shellfish Research 9: 215–225.Google Scholar
Jones, J. 1865. On Gryphaea incurva and its varieties. Proceedings of the Cotteswold Naturalists' Field Club 3: 81–95.Google Scholar
Joysey, K. A. 1959. The evolution of the Liassic oysters Ostrea-Gryphaea. Biological Review 34: 297–332.Google Scholar
Kaufmann, K. W. 1981. Fitting and using growth curves. Oecologia 49: 293–299.Google Scholar
Krantz, D. E., Jones, D. S., and Williams, D. F. 1984. Growth rates of the sea scallop, Placopecten magellanicus, determined from the 18O/16O record in shell calcite. Biological Bulletin 167: 186–199.Google Scholar
Krantz, D. E., Williams, D. F., and Jones, D. S. 1987. Ecological and paleoenvironmental information using stable isotope profiles from living and fossil molluscs. Palaeogeography, Palaeoclimatology, Palaeoecology 58: 249–266.Google Scholar
Lamarck, J. B. P. 1801. Histoire naturelle des animaux sans vertèbres. Verdière, Paris.Google Scholar
Lancisi, J. M. 1719. Metallotheca Vaticana Michaelis Mercati. J. M. Salvioni, Rome.Google Scholar
Lochner, J. H. 1716. Rariora musei Besleriani. Academy Leopold Carol, Nuremburg.Google Scholar
Lutz, R. A. and Rhoads, D. C. 1980. Growth patterns within the molluscan shell: an overview. pp. 203–254in Rhoads, D. C., Lutz, R. A. eds. Skeletal growth of aquatic organisms: biological records of environmental change. Plenum, New York.Google Scholar
Maclennan, R. M. and Trueman, A. E. 1942. Variation in Gryphaea incurva (Sow.) from the Lower Lias of Loch Aline, Argyll. Proceedings of the Royal Society of Edinburgh B 61: 211–232.Google Scholar
McKinney, M.L ed. 1988a. Heterochrony in evolution: a multidisciplinary approach. Plenum, New York.Google Scholar
McKinney, M. L. 1988b. Classifying heterochrony: allometry, size and time. pp. 17–34in McKinney, M. L. 1988a.CrossRefGoogle Scholar
McKinney, M. L. and McNamara, K. J. 1991. Heterochrony: the evolution of ontogeny. Plenum, New York.Google Scholar
Orton, J. H. 1923. On the significance of “rings” on the shells of Cardium and other molluscs. Nature 112: 10.Google Scholar
Pannella, G. and MacClintock, C. 1968. Biological and environmental rhythms reflected in molluscan shell growth. in Macurda, D. B. Jr. ed. Paleobiological aspects of growth and development—a symposium. Journal of Paleontology Memoir 2, 42 (Suppl. to No. 5). 64-80.Google Scholar
Plot, R. 1677. The natural history of Oxfordshire. S. Millers, London.Google Scholar
Rhoads, D. C., Lutz, R. A. eds. 1980. Skeletal growth of aquatic organisms: biological records of environmental change. Plenum, New York.Google Scholar
Rhoads, D. C. and Pannella, G. 1970. The use of molluscan shell growth patterns in ecology and paleoecology. Lethaia 3: 143–161.Google Scholar
Rosenberg, G. D. 1980. An ontogenetic approach to the environmental significance of bivalve shell chemistry. pp. 133–168in Rhoads, D. C., Lutz, R. A. eds. Skeletal growth of aquatic organisms: biological records of environmental change. Plenum, New York.Google Scholar
Rosenberg, G. D., Runcorn, S. K. eds. 1975. Growth rhythms and the history of the earth's rotation. Wiley, London.Google Scholar
SAS Institute Inc. 1988. SAS/STAT user's guide: release 6.03 ed. SAS Institute Inc., Cary, N.C.Google Scholar
Scheuchzer, J. J. 1737. Physique sacrée ou histoire-naturelle de la Bible. P. Schenk, Amsterdam.Google Scholar
Shea, B. T. 1983. Allometry and heterochrony in the African apes. American Journal of Physical Anthropology 62: 275–289.Google Scholar
Stenzel, H. B. 1971. Oysters. Pp. N953–N1224in Mollusca 6, Vol. 3. Part N ofMoore, R. C. ed. Treatise on invertebrate paleontology. Geological Society of America and University of Kansas, Boulder, Colo.Google Scholar
Swinnerton, H. H. 1932. Unit characters in fossils. Biological Reviews 7: 321–335.Google Scholar
Swinnerton, H. H. 1940. The study of variation in fossils. Quarterly Journal of the Geological Society of London 96: 77–118.Google Scholar
Tanabe, K. 1988. Age and growth rate determinations of an intertidal bivalve, Phacosoma japonicum, using internal shell increments. Lethaia 21: 231–241.Google Scholar
Thompson, D'A. W. 1917. On growth and form. Cambridge University Press, Cambridge.Google Scholar
Trueman, A. E. 1922. The use of Gryphaea in the correlation of the Lower Lias. Geological Magazine 59: 256–268.Google Scholar
Walton, A. and Hammond, J. 1938. The maternal effects on growth and conformation in shire horse-Shetland pony crosses. Proceedings of the Royal Society London B 125: 311–335.Google Scholar
Wefer, G. and Berger, W. H. 1991. Isotope paleontology: growth and composition of extant calcareous species. Marine Geology 100: 207–248.Google Scholar
Weymouth, F. W. 1923. The life history and growth of the Pismo clam (Tivela stultorum Mawe). California Fish and Game Commission, Fish Bulletin 7.Google Scholar
Worm, O. 1655. Museum Wormianum, seu historia rerum rariorum. Elsevier, Leiden.Google Scholar
Zolotarev, V. N. 1980. The life span of bivalves from the Sea of Japan and Sea of Okhotsk. Soviet Journal of Marine Biology 6: 301–308.Google Scholar