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A plastic boomerang: speciation and intraspecific evolution in the Cretaceous bivalve Actinoceramus

Published online by Cambridge University Press:  08 April 2016

James S. Crampton
Affiliation:
Institute of Geological and Nuclear Sciences, Post Office Box 30-368, Lower Hutt, New Zealand. E-mail: j.crampton@gns.cri.nz
Andy S. Gale
Affiliation:
Department of Earth and Environmental Sciences, University of Greenwich, Chatham Maritime, Kent, ME4 4TB, United Kingdom, and Department of Palaeontology, Natural History Museum, Cromwell Road, London SW7 5DB, United Kingdom

Abstract

The late Albian (Early Cretaceous) lineage of Actinoceramus sulcatus (Parkinson 1819) is a remarkable example of macro- and microevolution within the Bivalvia. Immediately following cladogenesis from ancestral A. concentricus, the lineage displays a conspicuous, short-term excursion through morphospace followed by a return to the ancestral form. This excursion is marked by the acquisition, and subsequent loss, of large radial folds affecting some part or all of the shell. The pattern is noteworthy because of the gross scale and rate of morphological evolution, the relatively short life span of an “extreme” morphology, an apparent evolutionary reversal, the presence of phenotypic clines through time, the extent of phenotypic variation within populations and abundance of morphological intermediates between disparate end-member types, the wide geographic distributions of phenotypic clines and variants, and the subtle asymmetry of morphological transitions bounding the evolutionary excursion.

From census and biometric analyses of stratigraphically constrained samples, we conclude that morphological change was not focused at speciation and the pattern of evolution does not conform to the classical paradigm of punctuated equilibrium. Instead, we infer that observed patterns are best explained by phyletic evolution, at widely varying rates, combined with ecophenotypic plasticity. Evolution targeted the potential to form radial folds; the expression of those in any individual was determined, in part at least, by environmental cues. Ecophenotypic plasticity in A. sulcatus was itself probably an evolutionary response favored by the presence of long-lived planktotrophic larvae and wide dispersal of the species. In A. sulcatus, there is a continuum of pattern between intrapopulational, ecophenotypic variation that can be observed on bedding planes, interregional variation, and phyletic change through time. We argue that this continuity of pattern is most easily explained by continuity of process: in the case of the visually striking radial folds in A. sulcatus, there is no reason to invoke distinct hierarchies of macro- and microevolution; instead, these seem to be parts of a continuum.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Akester, R. J., and Martel, A. L. 2000. Shell shape, dysodont tooth morphology, and hinge-ligament thickness in the bay mussel Mytilus trossulus correlate with wave exposure. Canadian Journal of Zoology 78:240253.Google Scholar
Ali-zade, A. A., Aliev, G. A., Aliev, M. M., Aliiulla, K., and Khalilov, A. G. 1988. Melovaia fauna Azerbaidzhana [Cretaceous Fauna of Azerbaijan]. Akademiia Nauk Azerbaidzhanskoi SSR, Institut Geologii, Baku, Azerbaijan. [In Russian.] Google Scholar
Appleton, R. D., and Palmer, A. R. 1988. Water-borne stimuli released by predatory crabs and damaged prey induce more predator resistant shells in a marine gastropod. Proceedings of the National Academy of Sciences USA 85:43874391.Google Scholar
Carroll, S. B. 2001. The big picture. Nature 409:669.Google Scholar
Carter, R. M. 1968. Functional studies on the Cretaceous oyster Arctostrea . Palaeontology 11:458485.Google Scholar
Crampton, J. S. 1996. Biometric analysis, systematics and evolution of Albian Actinoceramus (Cretaceous Bivalvia, Inoceramidae). Institute of Geological and Nuclear Sciences Monograph 15:180.Google Scholar
Crampton, J. S., and Haines, A. J. 1996. Users' manual for programs HANGLE, HMATCH, and HCURVE for the Fourier shape analysis of two-dimensional outlines. Institute of Geological and Nuclear Sciences Science Report 96/37:128.Google Scholar
Crampton, J. S., and Maxwell, P. A. 2000. Size: all it's shaped up to be? Evolution of shape through the lifespan of the Cenozoic bivalve Spissatella (Crassatellidae). In E. M. Harper, J. D. Taylor, and J. A. Crame. Evolutionary biology of the Bivalvia. Geological Society of London Special Publication 177:399423.Google Scholar
Curran-Everett, D. 2000. Multiple comparisons: philosophies and illustrations. American Journal of Physiology (Regulatory, Integrative and Comparative Physiology) 279:R1R8.Google Scholar
de Beer, G., Rowlands, M. J., and Skramovsky, B. M. 1967. Darwin's notebooks on transmutation of species, Part VI; pages excised by Darwin. Bulletin of the British Museum (Natural History), Historical Series 3:1176.Google Scholar
d'Orbigny, A. 1846 [in 1844–1847]. Paléontologie Française. Descriptions Zoologique et Géologique de tous les Animaux Mollusques et Reyonnés Fossiles de France. Terrains Crétacés, Vol. 3. Lamellibranchia. Arthus Bertrand, Paris.Google Scholar
DeWitt, T. J., Sih, A., and Wilson, D. S. 1998. Costs and limits of phenotypic plasticity. Trends in Ecology and Evolution 13:7781.Google Scholar
Erwin, D. H. 2000. Macroevolution is more than repeated rounds of microevolution. Evolution and Development 2:7884.Google Scholar
Fiet, N., Beaudoin, B., and Parize, O. 2001. Lithostratigraphic analysis of Milankovitch cyclicity in pelagic Albian deposits of central Italy: implications for the duration of the stage and substages. Cretaceous Research 22:265275.CrossRefGoogle Scholar
Gale, A. S., Huggett, J. M., and Gill, M. 1996a. The stratigraphy and petrography of the Gault Clay Formation (Albian, Cretaceous) at Redcliff, Isle of Wight. Proceedings of the Geologists Association 107:287298.Google Scholar
Gale, A. S., Kennedy, W. J., Burnett, J. A., Caron, M., and Kidd, B. E. 1996b. The Late Albian to Early Cenomanian succession at Mont Risou near Rosans (Drôme, SE France): an integrated study (ammonites, inoceramids, planktonic foraminifera, nannofossils, oxygen and carbon isotopes). Cretaceous Research 17:515606.Google Scholar
Goldfuss, G. A. 1836 [in 1834–1840]. Petrefacta Germaniæ tam ea, quae in Museo Universitatis Regiae Borussicae Fridericiae Wilhelmiae Rhenanae servantur quam alia quaecunque in Museis Hoeninghusiano, Muensteriano allisque extant, icon-ibus et descriptionibus illustrata, Vol. 2(5):69140. Arnz, Düsseldorf.Google Scholar
Gradstein, F. M., Agterberg, F. P., Ogg, J. G., Hardenbol, J., van Veen, P., Thierry, J., and Huang, Z. 1995. A Triassic, Jurassic and Cretaceous time scale. In Berggren, W. A., Kent, D. V., Aubry, M. P., and Hardenbol, J., eds. Geochronology, time scales and global stratigraphic correlation. SEPM Special Publication 54:95126.Google Scholar
Hardenbol, J., Thierry, J., Farley, M. B., Jacquin, T., Graciansky, P.-C. d., and Vail, P. R. 1998. Mesozoic and Cenozoic sequence chronostratigraphic framework of European basins. In de Graciansky, P.-C., Hardenbol, J., Jacquin, T., and Vail, P. R., eds. Mesozoic and Cenozoic sequence stratigraphy of European basins. SEPM Special Publication 60:313 + 8 charts.CrossRefGoogle Scholar
Harries, P. J., and Crampton, J. S. 1998. The inoceramids. American Paleontologist 6:26.Google Scholar
Kauffman, E. G., and Caldwell, W. G. E. 1993. The Western Interior Basin in space and time. In Caldwell, W. G. E. and Kauffman, E. G., eds. Evolution of the Western Interior Basin. Geological Association of Canada Special Paper 39:130.Google Scholar
Kemp, P. D., and Bertness, M. D. 1984. Snail shape and growth rates: evidence for plastic shell allometry in Littorina littorea . Proceedings of the National Academy of Sciences USA 81:811813.Google Scholar
Kennedy, W. J., Gale, A. S., Hancock, J. M., Crampton, J. S., and Cobban, W. A. 1999. Ammonites and inoceramid bivalves from close to the middle-upper Albian boundary around Fort Worth, Texas. Journal of Paleontology 73:11011125.Google Scholar
Khalilov, A. G. 1959. Lower Cretaceous inoceramids from the eastern Minor Caucasus. Izvestiia Akademii Nauk Azerbaidzhanskoi SSR, Seriia Geologo-geograficheskikh Nauk 1959:2737. [In Russian.]Google Scholar
Knight, R. I. 1997. Benthic paleoecology of the Gault Clay Formation (Mid- and basal Upper Albian) of the western Anglo-Paris Basin. Proceedings of the Geologists Association 108:81103.Google Scholar
Knight, R. I., and Morris, N. J. 1996. Inoceramid larval planktotrophy: evidence from the Gault Formation (middle and basal upper Albian), Folkestone, Kent. Palaeontology 39:10271036.Google Scholar
Leonard, G. H., Bertness, M. D., and Yund, P. O. 1999. Crab predation, waterborne cues, and inducible defences in the blue mussel, Mytilus edulis . Ecology 80:114.Google Scholar
Leroi, A. M. 2000. The scale independence of evolution. Evolution and Development 2:6777.Google Scholar
Mantell, G. 1822. The fossils of the South Downs; or illustrations of the geology of Sussex. Lupton Relfe, London.Google Scholar
Marcinowski, R., Walaszczyk, I., and Olszewska-Nejbert, D. 1996. Stratigraphy and regional development of the mid-Cretaceous (Upper Albian through Coniacian) of the Mangyshlak Mountains, Western Kazakhstan. Acta Geologica Polonica 46:160.Google Scholar
Owen, H. G. 1971. Middle Albian stratigraphy in the Anglo-Paris Basin. Bulletin of the British Museum (Natural History), Geology 8(Suppl.):1164.Google Scholar
Owen, H. G. 1975. The stratigraphy of the Gault and Upper Greensand of the Weald. Proceedings of the Geologists Association 86:475498.Google Scholar
Owen, H. G. 1984. The Albian Stage: European province chronology and ammonite zonation. Cretaceous Research 5:329344.Google Scholar
Palmer, A. R. 1985. Quantum changes in gastropod shell morphology need not reflect speciation. Evolution 39:699705.Google Scholar
Palmer, A. R. 1990. Effect of crab effluent and scent of damaged conspecifics on feeding, growth, and shell morphology of the Atlantic dogwhelk Nucella lapillus (L.). Hydrobiologia 193:155182.CrossRefGoogle Scholar
Parsons, K. E. 1997. The role of dispersal ability in the phenotypic differentiation and plasticity of two marine gastropods. I. Shape. Oecologia 110:461471.Google Scholar
Parsons, K. E. 1998. The role of dispersal ability in the phenotypic differentiation and plasticity of two marine gastropods. II. Growth. Journal of Experimental Marine Biology and Ecology 221:125.Google Scholar
Pokhialainen, V. P. 1985. The structure of inoceram populations. Pp. 91103 In Pokhialainen, V. P., ed. Dvustvorchatye i golovonogie molliuski Mezozoia Severo-Vostoka SSSR [Bivalve and Cephalopod Molluscs of the Mesozoic of the North-Eastern USSR], Dal'nevostochnyi Nauchnyi Tsentr, Severo-Vostochnyi Kompleksnyi Nauchno-Issledovatel'skii Institut, Magadan, Russia. [In Russian.] Google Scholar
Röhl, U., and Ogg, J. G. 1996. Aptian-Albian sea level history from guyots in the western Pacific. Paleoceanography 11:595624.Google Scholar
Roopnarine, P. D. 2001. The description and classification of evolutionary mode: a computational approach. Paleobiology 27:446465.Google Scholar
Roopnarine, P. D., Byars, G., and Fitzgerald, P. 1999. Anagenetic evolution, stratophenetic patterns, and random walk models. Paleobiology 25:4157.Google Scholar
Samadi, S., Patrice, D., and Jarne, P. 2000. Variation of shell shape in the clonal snail Melanoides tuberculata and its consequences for the interpretation of fossil series. Evolution 54:492502.Google Scholar
Savazzi, E. 1990. Biological aspects of theoretical shell morphology. Lethaia 23:195212.CrossRefGoogle Scholar
Savel'ev, A. A. 1962. Albian inocerams of Mangyshlak. Trudy Vsesoiuznogo Neftianogo Nauchno-Issledovatel'skogo Geologo-Razvedochnogo Instituta (VNIGRI) [Leningrad] 196:219254. [In Russian.]Google Scholar
Smith, L. D., and Jennings, J. A. 2000. Induced defensive responses by the bivalve Mytilus edulis to predators with different attack modes. Marine Biology 136:461469.CrossRefGoogle Scholar
Sowerby, J. 1821 [in 1818–1821]. The mineral conchology of Great Britain; or coloured figures and descriptions of those testaceous animals or shells, which have been preserved at various times and depths in the Earth, Vol. III. The author, London.Google Scholar
Trussell, G. C. 1997. Phenotypic plasticity in the foot size of an intertidal snail. Ecology 78:10331048.Google Scholar
Trussell, G. C. 2000. Phenotypic clines, plasticity, and morphological trade-offs in an intertidal snail. Evolution 54:151166.Google Scholar
Trussell, G. C., and Smith, L. D. 2000. Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proceedings of the National Academy of Sciences USA 97:21232127.Google Scholar
Whiteaves, J. F. 1884. Mesozoic fossils, Vol. 1, Part III. On the fossils of the coal-bearing deposits of the Queen Charlotte Islands collected by Dr. G. M. Dawson in 1858. Geological Survey of Canada, Montreal.Google Scholar
Woods, H. 1912. The evolution of Inoceramus in the Cretaceous Period. Quarterly Journal of the Geological Society of London 68:120.CrossRefGoogle Scholar
Yeap, K. L., Black, R., and Johnson, M. S. 2001. The complexity of phenotypic plasticity in the intertidal snail Nodilittorina australis . Biological journal of the Linnean Society 72:6376.Google Scholar