Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T06:23:10.312Z Has data issue: false hasContentIssue false
  • English
  • Français

A developmental explanation of stability-diversity-variation hypotheses: morphogenetic regulation in Ordovician bryozoan colonies

Published online by Cambridge University Press:  08 February 2016

Joseph F. Pachut  and
Robert L. Anstey
Joseph F. Pachut
Affiliation:
Department of Geology, Indiana University - Purdue University at Indianapolis, Indianapolis, Indiana 46202
Robert L. Anstey
Affiliation:
Department of Geology, Michigan State University, East Lansing, Michigan 48824
Get access Rights & Permissions [Opens in a new window]

Abstract

A paradoxical relationship exists between the genetic and morphologic adaptive strategies of benthic marine invertebrates; morphologically variable species from unstable environments have been shown to possess less genetic variability than species with more constant phenotypes from stable habitats. The mode of growth of Ordovician bryozoans provides an insight into this paradox. These bryozoans exhibit morphologic gradients within zooidal subcolonies that change throughout colony development. Entire clusters of zooids begin and cease growth as a function of their spatial position with respect to neighboring clusters. A comparison of the within-colony and among-colony components of developmental and morphologic variability was made from populations inhabiting Ordovician environments of differing stability. In four stratigraphically persistent species, the level of developmental variability is homogeneous within species, but varies significantly across taxa. The two species with the highest levels of developmental variability (less canalized development) fit the concept of r-selected opportunistic species and are most abundant in communities of lowest diversity. The other two species have much lower levels of variability (more canalized development), fit the concept of K-selected equilibrium species, and are most abundant in the communities of highest diversity. Within-colony morphologic variability is also higher in the opportunistic rather than the equilibrium species, indicating that the higher morphologic variability observed in unstable environments is the product of within-genotype deregulation, and not the result of higher genetic polymorphism. The equilibrium species in stable environments have lower levels of morphologic deregulation and correspondingly greater variation among genotypes than within genotypes in fossil populations.

Type
Research Article
Information
Paleobiology , Volume 5 , Issue 2 , Spring 1979 , pp. 168 - 187
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Abrahamson, W. G. and Gadgil, M. 1973. Growth form and reproductive effort in goldenrods (Solidago, Compositae). Am. Nat. 107:651–661.CrossRefGoogle Scholar
Anstey, R. L. 1978. Taxonomic survivorship and morphologic complexity in Paleozoic bryozoan genera. Paleobiology. 4:407–418.CrossRefGoogle Scholar
Anstey, R. L. and Pachut, J. F. 1976. Morphophysiology of a fossil bryozoan: natural experiments that test a biological hypothesis. Geol. Soc. Am. Abstr. with Program. 8:461.Google Scholar
Anstey, R. L. and Pachut, J. F. 1977. Recognition of new polymorphs in Paleozoic bryozoans: specialized morphoregulatory zooids. Geol. Soc. Am. Abstr. with Program. 9:236–237.Google Scholar
Anstey, R. L., Pachut, J. F., and Prezbindowski, D. R. 1976. Morphogenetic gradients in Paleozoic bryozoan colonies. Paleobiology. 2:131–146.CrossRefGoogle Scholar
Anstey, R. L. and Perry, T. G. 1973. Eden Shale bryozoans: a numerical study (Ordovician, Ohio Valley). Mich. State Univ., Publ. Mus., Paleontol. Ser. 1:1–80.Google Scholar
Ashton, J. H. and Rowell, A. J. 1975. Environmental stability and species proliferation in Late Cambrian trilobite faunas: a test of the niche-variation hypothesis. Paleobiology. 1:161–174.CrossRefGoogle Scholar
Astrova, G. G. 1973. Polymorphism and its development in the trepostomatous Bryozoa. Pp. 1–10. In: Larwood, F. P., ed. Living and Fossil Bryozoa. 634 pp.Academic Press; London and New York.Google Scholar
Ayala, F. J., Powell, J. R., Tracey, M. L., Mourao, C. A., and Perez-Sales, S. 1972. Enzyme variability in the Drosophila willistoni groups. IV. Genic variation in natural populations of Drosophila willistoni. Genetics. 70:113–139.CrossRefGoogle ScholarPubMed
Ayala, F. J., Valentine, J. W., DeLaca, T. E., and Zumwalt, G. S. 1975a. Genetic variability of the Antarctic brachiopod Liothyrella notorcadenis and its bearing on mass extinction hypotheses. J. Paleontol. 49:1–9.Google Scholar
Ayala, F. J., Valentine, J. W., Hedgecock, D., and Barr, G. 1975b. Deep sea asteroids—high genetic variability in a stable environment. Evolution. 29:203–212.CrossRefGoogle Scholar
Ayala, F. J., Valentine, J. W., and Zumwalt, G. S. 1975c. Electrophoretic study of the Antarctic zooplankter Euphausia superba. Limn. Oceanogr. 20:635–640.CrossRefGoogle Scholar
Banta, W. C., McKinney, F. K., and Zimmer, R. L. 1974. Bryozoan monticules: excurrent water outlets? Science. 185:783–784.CrossRefGoogle ScholarPubMed
Boardman, R. S. 1973. Body walls and attachment organs in some Recent cyclostomes and Paleozoic trepostomes. Pp. 231–246. In: Larwood, G. P., ed. Living and Fossil Bryoza. 634 pp.Academic Press; London and New York.Google Scholar
Boardman, R. S. and Cheetham, A. H. 1973. Degrees of colony dominance in stenolaemate and gymnolaemate bryozoa. Pp. 121–220. In: Boardman, R. S., Cheetham, A. H. and Oliver, W. A., eds. Animal Colonies. 603 pp.Dowden, Hutchinson and Ross; Stroudsburg, Pa.Google Scholar
Bonner, J. T. 1974. On Development. 282 pp. Harvard Univ. Press; Cambridge, Mass.Google Scholar
Borg, F. 1926. Studies on Recent cyclostomatous bryozoa. Zool. Bidrag Uppsala. 10:181–507.Google Scholar
Borg, F. 1933. A revision of the Recent Heteroporidae (Bryozoa). Zool. Bidrag Uppsala. 14:254–394.Google Scholar
Braverman, M. H. 1963. Studies on hydroid differentiation II. Colony growth and the initiation of sexuality. J. Embryol. Exp. Morph. 11:239–253.Google Scholar
Braverman, M. H. and Schrandt, R. G. 1966. Colony development of a polymorphic hydroid as a problem in pattern formation. Pp. 169–198. In: Rees, W. J., ed. The Cnidaria and Their Evolution. Symp. No. 16, Zool. Soc. London.Google Scholar
Bretsky, P. W. and Lorenz, D. M. 1970. Adaptive response to environmental stability: a unifying concept in paleobiology. North Am. Paleontol. Conv., Chicago, 1969. Proc., pt. E, pp. 522–550.Google Scholar
Bretsky, S. S. and Bretsky, P. W. 1977. Morphological variability and change in the paleotaxodont bivalve mollusk Nuculites planulatus (Upper Ordovician of Quebec). J. Paleontol. 51:256–271.Google Scholar
Bronstein, G. 1939. Sur les gradients physiologiques dans une colonie de Bryozoaires. C. R. hebd. Seance Acad. Sci., Paris, 209:602–603.Google Scholar
Burnett, A. L. 1966. A model of growth and cell differentiation in Hydra. Am. Nat. 100:165–190.CrossRefGoogle Scholar
Burns, J. M. and Johnson, F. M. 1971. Esterase polymorphism in butterfly Hemiargus isola: stability in a variable environment. Proc. Nat. Acad. Sci. 68:34.CrossRefGoogle Scholar
Child, C. M. 1941. Patterns and Problems of Development. 811 pp. Univ. Chicago Press; Chicago, Ill.CrossRefGoogle Scholar
Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs. Science. 199:1302–1310.CrossRefGoogle ScholarPubMed
Cowen, R. 1966. The distribution of punctae on the brachiopod shell. Geol. Mag. 103:269–275.CrossRefGoogle Scholar
Cumings, E. R. 1912. Development and systematic position of the monticuliporoids. Geol. Soc. Am. Bull. 23:357–370.CrossRefGoogle Scholar
De Beer, G. R. 1958. Embryos and Ancestors. 197 pp. Oxford Univ. Press; Oxford.Google Scholar
Delmet, D. A. and Anstey, R. L. 1974. Fourier analysis of morphological plasticity within an Ordovician bryozoan colony. J. Paleontol. 48:217–226.Google Scholar
Doyle, R. W. 1971. Genetic differentiation of ophiuroid populations on the lower continental slope. Ecol. Soc. Am. Bull. 52:45.Google Scholar
Doyle, R. W. 1972. Genetic variation in Ophiomusium lymani (Echinodermata) populations in the deep sea. Deep-Sea Res. 19:199–208.Google Scholar
Dzik, J. 1975. The origin and early phylogeny of the cheilostomatous Bryozoa. Acta Paleontol. Polon. 29:395–423.Google Scholar
Eldredge, N. 1974. Stability, diversity, and speciation in Paleozoic epeiric seas. J. Paleontol. 48:541–548.Google Scholar
Eldredge, N. and Gould, S. J. 1972. Punctuated equilibria: an alternative to phyletic gradualism. Pp. 82–115. In: Schopf, T. J. M., ed. Models in Paleobiology. Freeman, Cooper and Co.; San Francisco, Cal.Google Scholar
Farmer, J. D. and Rowell, A. J. 1973. Variation in the Bryozoan Fistulipora decora (Moore and Dudley) from the Beil Limestone of Kansas. Pp. 377–394. In: Boardman, R. S., Cheetham, A. H. and Oliver, W. A. Jr., eds. Animal Colonies. Dowden, Hutchinson and Ross, Inc.; Stroudsburg, Pa.Google Scholar
Flessa, K. W. and Bray, R. G. 1977. On the measurement of size-independent morphological variability: an example using successive populations of a Devonian spiriferid brachiopod. Paleobiology. 3:350–359.CrossRefGoogle Scholar
Gadgil, M. and Solbrig, O. T. 1972. The concept of r- and K-selection: evidence from wild flowers and some theoretical considerations. Am. Nat. 106:14–31.CrossRefGoogle Scholar
Gooch, J. L. and Schopf, T. J. M. 1973. Genetic variability in the deep sea: relation to environmental variability. Evolution. 26:545–552.CrossRefGoogle Scholar
Gordon, D. P. 1973. A fine-structure study of brown bodies in the gymnolaemate Cryptosula pallasiana (Moll). Pp. 275–286. In: Larwood, G. P., ed. Living and Fossil Bryozoa. 634 pp.Academic Press; London and New York.Google Scholar
Gould, S. J. 1968. Ontogeny and the explanation of form: an allometric analysis. In: Macurda, D. B., ed. Paleobiological Aspects of Growth and Development, a Symposium. Paleontol. Soc., Mem. 2 (J. Paleontol. 42, no. 5, suppl.), pp. 81–98.Google Scholar
Gould, S. J. and Garwood, R. A. 1969. Levels of integration in mammalian dentitions: an analysis of correlations in Nesophontes micus (Insectivora) and Oryzomys couesi (Rodentia). Evolution. 23:276–300.CrossRefGoogle Scholar
Grassle, J. F. 1972. Species diversity, genetic variability and environmental uncertainty. Fifth European Mar. Biol. Symp. Piccin, Padua, pp. 19–26.Google Scholar
Grassle, J. F. and Sanders, H. L. 1973. Life histories and the role of disturbance. Deep-Sea Res. 20:643–659.Google Scholar
Hyman, L. H. 1959. The Invertebrates: Smaller Coelomate Groups, Vol. 5. 783 pp. McGraw-Hill; New York.Google Scholar
Johnson, G. B. 1973. Relationship of enzyme polymorphism to species diversity. Nature. 242:193–194.CrossRefGoogle ScholarPubMed
Kaesler, R. L. and Brondos, M. D. 1975. Indices of diversity in paleoecology. Geol. Soc. Am. Annu. Meet. Abstr. 7:1137.Google Scholar
Lerner, I. M. 1954. Genetic Homeostasis. 134 pp. John Wiley; New York.Google Scholar
Levins, R. 1968. Evolution in Changing Environments. Princeton Univ. Press; Princeton, New Jersey. 120 pp.CrossRefGoogle Scholar
Levinton, J. S. 1970. The paleoecological significance of opportunistic species. Lethaia. 3:69–78.CrossRefGoogle Scholar
Lloyd, M. and Ghelardi, R. J. 1964. A table for calculating the “equitability” component of species diversity. J. Animal Ecol. 33:217–225.CrossRefGoogle Scholar
Lorenz, D. M. 1973. Edenian (Upper Ordovician) Benthic Community Ecology in North-Central Kentucky. 318 pp. Unpubl. Ph.D. dissertation, Northwestern Univ.; Evanston, Ill.Google Scholar
MacArthur, R. H. 1960. On the relative abundance of species. Am. Nat. 94:25–36.CrossRefGoogle Scholar
Odum, E. P. 1971. Fundamentals of Ecology. 574 pp. W. B. Saunders Co.; Philadelphia, Pa.Google Scholar
Osborn, J. W. 1978. Morphogenetic gradients in mammalian dentition. Pp. 250–275. In: Butler, P. M. and Joysey, K. A., eds. Development, Function and Evolution of Teeth. 524 pp.Academic Press; London and New York.Google Scholar
Pachut, J. F. 1977. Environmental Stability and Morphogenetic Relaxation in Bryozoan Colonies from the Eden Shale (Ordovician, Ohio Valley): A Developmental Explanation of Stability-Diversity-Variation Hypotheses. 61 pp. Unpubl. Ph.D. dissertation, Mich. State Univ.; East Lansing, Mich.Google Scholar
Pachut, J. F. and Anstey, R. L. 1977. Diversity, stability and stratigraphic gradients in bryozoan dominated communities of the Eden Shale (Cincinnatian, Ohio Valley). Geol. Soc. Am. Abstr. with Program. 9:638–639.Google Scholar
Pielou, E. C. 1966. The measurement of diversity in different types of biological collections. J. Theoret. Biol. 13:131–144.CrossRefGoogle Scholar
Pielou, E. C. 1966. Species-diversity and pattern diversity in the study of ecological succession. J. Theoret. Biol. 10:370–383.CrossRefGoogle Scholar
Pielou, E. C. 1969. An Introduction to Mathematical Ecology. 286 pp. Wiley-Interscience; New York.Google Scholar
Pielou, E. C. 1974. Population and Community Ecology. 424 pp. Gordon and Breach Sci. Publ.; New York.Google Scholar
Podell, M. E. 1978. The Interrelationship of Early Colony Development, Monticules, and Branches in Paleozoic Bryozoans. 37 pp. Unpubl. M.S. thesis, Mich. State Univ.; East Lansing, Mich.Google Scholar
Powell, J. R. 1971. Genetic polymorphism in varied environments. Science. 174:1035–1036.CrossRefGoogle ScholarPubMed
Rollins, H. B. and Donahue, J. 1975. Towards a theoretical basis of paleoecology—concepts of community dynamics. Lethaia. 8:255–270.CrossRefGoogle Scholar
Rothstein, S. I. 1973. The niche-variation model—is it valid? Am. Nat. 107:598–620.CrossRefGoogle Scholar
Ryland, J. S. 1970. Bryozoans. 175 pp. Hutchinson Univ. Library; London.Google Scholar
Schoener, T. W. 1969. Optimal size and specialization in constant and fluctuating environments: an energy-time approach. Brook-haven Symp. Biol. 22:103–114.Google ScholarPubMed
Schopf, T. J. M. 1976. Environmental versus genetic causes of morphologic variability in bryozoan colonies from the deep sea. Paleobiology. 2:156–165.CrossRefGoogle Scholar
Schopf, T. J. M. and Dutton, A. R. 1976. Parallel clines in morphologic and genetic differentiation in a coastal zone marine invertebrate: the bryozoan Schizoporella errata. Paleobiology. 2:255–264.CrossRefGoogle Scholar
Schopf, T. J. M. and Gooch, J. L. 1971. A natural experiment using deep-sea invertebrates to test the hypothesis that genetic homozygosity is proportional to environmental stability. Biol. Bull. 141:401.Google Scholar
Schopf, T. J. M. and Gooch, J. L. 1972. A natural experiment to test the hypothesis that loss of genetic variability was responsible for mass extinctions of the fossil record. J. Geol. 80:481–483.CrossRefGoogle Scholar
Seilacher, A., Drozdzewski, G., and Haude, R. 1968. Form and function of the stem in a pseudoplanktonic crinoid (Seiocrinus). Paleontology. 11:275–282.Google Scholar
Somero, G. N. and Soulé, M. 1974. Genetic variation in marine fishes as a test of the niche-variation hypothesis. Nature. 249:670–672.CrossRefGoogle ScholarPubMed
Soulé, M., Yang, S. Y., Weiler, M. G. W., and Gorman, G. C. 1973. Island lizards: the genetic-phenetic variation correlation. Nature. 242:191–193.CrossRefGoogle ScholarPubMed
Spiller, J. 1973. Character variation and microevolutionary accelerations. Geol. Soc. Am. Abstr. with Program. 5:817–818.Google Scholar
Urbanek, A. 1973. Organization and evolution of graptolite colonies. Pp. 441–514. In: Boardman, R. S., Cheetham, A. H. and Oliver, W. A., eds. Animal colonies. 603 pp.Dowden, Hutchinson and Ross; Stroudsburg, Pa.Google Scholar
Utgaard, J. 1973. Mode of colony growth, autozooids, and polymorphism in the bryozoan order Cystoporata. Pp. 317–360. In: Boardman, R. S., Cheetham, A. H. and Oliver, W. A., eds. Animal Colonies. 603 pp.Dowden, Hutchinson and Ross; Stroudsburg, Pa.Google Scholar
Valentine, J. W. 1969. Niche diversity and niche size patterns in marine fossils. J. Paleontol. 43:905–915.Google Scholar
Valentine, J. W. 1971. Resource supply and species diversity patterns. Lethaia. 4:51–61.CrossRefGoogle Scholar
Valentine, J. W. 1972. Conceptual models of ecosystem evolution. Pp. 192–214. In: Schopf, T. J. M., ed. Models in Paleobiology. Freeman, Cooper and Co.; San Francisco, Calif.Google Scholar
Valentine, J. W. 1976. Genetic strategies of adaptation. Pp. 78–94. In: Ayala, F. J., ed. Molecular Evolution. Sinauer Associates, Inc.; Sunderland, Mass.Google Scholar
Valentine, J. W. and Ayala, F. J. 1974. Genetic variation in Frieleia halli, a deep-sea brachiopod. Deep-Sea Res. 22:37–44.Google Scholar
Valentine, J. W. and Campbell, C. A. 1975. Genetic regulation and the fossil record. Am. Sci. 63:673–680.Google ScholarPubMed
Van Valen, L. 1962. Growth fields in the dentition of Peromyscus. Evolution. 16:272–277.CrossRefGoogle Scholar
Van Valen, L. 1965. Morphological variation and width of ecological niche. Am. Nat. 99:377–390.CrossRefGoogle Scholar
Waage, K. M. 1968. The type Fox Hills Formation, Cretaceous (Maastrichtian), South Dakota. Part 1. Stratigraphy and Paleoenvironments. Peabody Mus. Bull. Yale Univ., Bull. 27:1–171.Google Scholar
Whittaker, R. H. 1964. Dominance diversity in land plant communities. Science. 147:250–260.CrossRefGoogle Scholar
Wilson, A. C. 1976. Gene regulation in evolution. Pp. 225–234. In: Ayala, F. J., ed. Mollecular Evolution. Sinauer Associates, Inc.; Sunderland, Mass.Google Scholar