Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-29T22:56:22.124Z Has data issue: false hasContentIssue false

The concepts of astogeny and ontogeny in stenolaemate bryozoans, and their illustration in colonies of Tabulipora carbonaria from the Lower Permian of Kansas

Published online by Cambridge University Press:  20 May 2016

Joseph F. Pachut
Affiliation:
Department of Geology (Cavanaugh Hall), Indiana University–Purdue University at Indianapolis, 425 University Boulevard, Indianapolis 46202
Roger J. Cuffey
Affiliation:
Department of Geosciences (Deike Building), Pennsylvania State University, University Park 16802
Robert L. Anstey
Affiliation:
Department of Geological Sciences (Natural Science Building), Michigan State University, East Lansing 48224

Abstract

Recognition of ontogeny within a stenolaemate bryozoan colony requires separating the individualistic aspects of a zooid's growth from those of its neighbors. The ancestrula is the only zooid within a colony that always displays a partially independent ontogeny that ceases when it starts to experience shared changes with its neighboring daughter zooids during subsequent accretionary skeletal growth.

Stenolaemate astogeny (shared changes across multiple zooids during the growth of both the ancestrular zooid and its asexual descendants) includes all coordinated changes in the size, shape, number, and calcification of autozooids, polymorphs, and extrazooidal structures, as well as changes within autozooids or polymorphs, such as the formation of basal diaphragms and brown bodies. Despite the fact that many of these directional changes occur within individual zooids, they are not part of ontogeny because they are taking place simultaneously across zooids that share a common skeleton, extrazooidal tissues, and pseudocoelomic spaces.

Shared directional multizooidal changes occurring during colony growth provide a confirmatory test for the existence of astogeny. Astogeny was statistically evaluated in 6–15 characters measured within the exozones of four colonies of Tabulipora carbonaria (Worthen in Worthen and Meek, 1875). Statistically significant (at P ≤ 0.05) directional changes took place across growth stages within the exozone in the following morphometric characters: zooecial density, zooecial wall surface area, acanthostyle density, zooecial wall thicknesses, maximum acanthostyle diameters, and intrazooecial diaphragm abundances. Overall, earlier exozonal growth stages differ statistically from those of the later exozone, with characteristics of intermediate growth stages intergrading between the two. Discriminant function analysis segregated intervals of exozonal growth into early-, intermediate-, and late-stage clusters, confirming patterns delineated by univariate statistical tests.

Based on these exozonal growth patterns, heterochronic changes in exozone astogeny characterized evolution within and across species of Tabulipora. Onshore populations of T. carbonaria were astogenetically progenetic relative to offshore ones along an environmental gradient across Kansas, whereas local populations became temporally more hypermorphic in a short-term stratigraphic succession of similar environments. Tabulipora carbonaria originated by astogenetic recapitulation in populations of its probable ancestor, T. ramosa. Therefore, speciation, microevolution, and clinal variation in Tabulipora all involved heterochronic modifications of exozone astogeny.

Type
Research Article
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

Alberch, P., Gould, S. J., Oster, G. F., and Wake, D. B. 1979. Size and shape in ontogeny and phylogeny. Paleobiology, 5:296317.Google Scholar
Anstey, R. L. 1981. Zooid orientation structures and water flow patterns in Paleozoic bryozoan colonies. Lethaia, 14:287302.Google Scholar
Anstey, R. L. 1987. Astogeny and phylogeny: evolutionary heterochrony in Paleozoic bryozoans. Paleobiology, 13:2043.Google Scholar
Anstey, R. L. 1990. Bryozoans, p. 232252. In McNamara, K. J. (ed.), Evolutionary Trends. Belhaven Press, London.Google Scholar
Anstey, R. L., and Bartley, J. W. 1984. Quantitative stereology: an improved thin section biometry for bryozoans and other colonial organisms. Journal of Paleontology, 58:612625.Google Scholar
Anstey, R. L., Pachut, J. F., and Prezbindowski, D. R. 1976. Morphogenetic gradients in Paleozoic bryozoan colonies. Paleobiology, 2:131146.Google Scholar
Bartley, J. W., and Anstey, R. L. 1987. Growth of monilae in the Permian trepostome Tabulipora carbonaria: evidence for periodicity and a new model of stenolaemate wall calcification, p. 916. In Ross, J. R. P. (ed.), Bryozoa: Present and Past. Western Washington University.Google Scholar
Bassler, R. S. 1953. Bryozoa, In Moore, R. C. (ed.), Treatise on Invertebrate Paleontology, Pt. G1-253. Geological Society of America and University of Kansas Press, Lawrence, 253 p.Google Scholar
Blackstone, N. W., and Yund, P. O. 1989. Morphological variation in a colonial marine hydroid: a comparison of size-based and age-based heterochrony. Paleobiology, 15:110.Google Scholar
Blake, D. B. 1976. Functional morphology and taxonomy of branch dimorphism in the Paleozoic bryozoan genus Rhabdomeson. Lethaia, 9:169178.Google Scholar
Bordman, R. S. 1954. Morphologic variation and mode of growth of Devonian trepostomatous Bryozoa. Science, 120:322.Google Scholar
Bordman, R. S. 1960. Trepostomatous Bryozoa of the Hamilton Group of New York. U.S. Geological Survey Professional Paper 340, 87 p.Google Scholar
Bordman, R. S., and Cheetham, A. H. 1969. Skeletal growth, intracolony variation, and evolution in Bryozoa: a review. Journal of Paleontology, 43:205233.Google Scholar
Bordman, R. S., and Cheetham, A. H. 1973. Degrees of colony dominance in stenolaemate and gymnolaemate Bryozoa, p. 121220. In Boardman, R. S., Cheetham, A. H., and Oliver, W. A. Jr. (eds.), Animal Colonies. Dowden, Hutchinson and Ross, Stroudsburg, Pennsylvania.Google Scholar
Bordman, R. S., Blake, D. B., Utgaard, J., Karklins, O. L., Cook, P. L., Sandberg, P. A., Lutaud, G., and Wood, T. S. 1983. Treatise on Invertebrate Paleontology, Pt. G, Bryozoa Revised. Geological Society of America and University of Kansas Press, Lawrence, 625 p.Google Scholar
Bordman, R. S., and Cook, P. L. 1970. Intracolony variation and the genus concept in Bryozoa. North American Paleontological Convention, Chicago, 1969, Proceedings C:294320.Google Scholar
Bordman, R. S., and McKinney, F. K. 1976. Skeletal architecture and preserved organs of four-sided zooids in convergent genera of Paleozoic Trepostomata (Bryozoa). Journal of Paleontology, 50:2578.Google Scholar
Bronstein, G. 1939. Sur les gradients physiologiques dans une colonie de Bryozoaires. C. R. hebd. Séance Academie of Science, Paris, 209:602603.Google Scholar
Buss, L. W., and Grossberg, R. K. 1990. Morphogenetic basis for phenotypic differences in hydroid competitive behavior. Nature, 343:6366.Google Scholar
Cuffey, R. J. 1967. Bryozoan Tabulipora carbonaria in Wreford Megacyclothem (Lower Permian) of Kansas. University of Kansas Paleontological Contributions, Bryozoa, Article 1:196.Google Scholar
Cumings, E. R. 1904. Development of some Paleozoic Bryozoa. American Journal of Science, Series 4, 17:4978.Google Scholar
Cumings, E. R. 1912. Development and systematic position of the monticuliporids. Geological Society of America, Bulletin, 23:357370.Google Scholar
Delmet, D. A., and Anstey, R. L. 1974. Fourier analysis of morphological plasticity within an Ordovician bryozoan colony. Journal of Paleontology, 48:217226.Google Scholar
Dommergues, J.-L., David, B., and Marchand, D. 1986. Les relations ontogenese–phylogenese: applications palaeontologiques. Geobios, 19:335356.Google Scholar
Edgecomb, G. D., and Chatterton, B. D. E. 1987. Heterochrony in the Silurian radiation of encrinurine trilobites. Lethaia, 20:337351.Google Scholar
Gautier, T. G. 1970. Interpretive morphology and taxonomy of bryozoan genus Tabulipora. University of Kansas Paleontological Contributions, Paper 48:121.Google Scholar
Gould, S. J. 1977. Ontogeny and Phylogeny. Harvard University Press, Cambridge, 501 p.Google Scholar
Hattin, D. E. 1957. Depositional environment of the Wreford Megacyclothem (Lower Permian) of Kansas. Kansas Geological Survey Bulletin 124, 150 p.Google Scholar
Hickey, D. R. 1988. Bryozoan astogeny and evolutionary novelties: their role in the origin and systematics of the Ordovician monticu-liporid trepostome genus Peronopora. Journal of Paleontology, 62:180203.Google Scholar
Horowitz, A. S., and Pachut, J. F. 1989. In search of the elusive earliest stages of colony development in the Paleozoic bryozoan order Cystoporida—an aid in phylogenetic reconstruction? Geological Society of America, Abstracts with Programs, 22:113.Google Scholar
McKinney, F. K. 1977. Autozooecial budding patterns in dendroid Paleozoic bryozoans. Journal of Paleontology, 51:303329.Google Scholar
McKinney, F. K. 1978. Astogeny of the lyre-shaped Carboniferous fenestrate bryozoan Lyroporella. Journal of Paleontology, 52:8390.Google Scholar
McKinney, F. K., and Jackson, J. B. C. 1989. Bryozoan Evolution. Unwin Hyman, Inc., Boston, 238 p.Google Scholar
McKinney, M. L. 1984. Allometry and heterochrony in an Eocene echinoid lineage: morphological change as a by-product of size selection. Paleobiology, 10:207219.Google Scholar
McKinney, M. L. 1986. Ecological causation of heterochrony: a test and implications for evolutionary theory. Paleobiology, 12:282289.Google Scholar
McNamara, K. J. 1984. Taxonomy and evolution of the Cainozoic spatangoid echinoid Protenaster. Palaeontology, 28:311330.Google Scholar
Meyer, A. 1987. Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution, 41:13571369.Google Scholar
Nie, M. H., Hull, C. H., Jenkins, J. G., Steinbrenner, K., and Bent, D. H. 1975. SPSS: Statistical Package for the Social Sciences. McGraw-Hill Book Company, New York, 675 p.Google Scholar
Oliver, W. A. 1979. Corals, p. 226235. In Fairbridge, R. W. and Jablonski, D. (eds.), The Encyclopedia of Paleontology. Dowden, Hutchinson and Ross, Stroudsburg, Pennsylvania.Google Scholar
Pachut, J. F. 1982. Morphologic variation within and among genotypes in two Devonian bryozoan species: an independent indicator of paleostability? Journal of Paleontology, 56:703716.Google Scholar
Pachut, J. F. 1987. Population genetics of four species of Ordovician bryozoans: stereology and jackknifed analysis of variance. Journal of Paleontology, 61:927941.CrossRefGoogle Scholar
Pachut, J. F. 1989. Heritability and intraspecific heterochrony in Ordovician bryozoans from environments differing in diversity. Journal of Paleontology, 63:182194.Google Scholar
Pachut, J. F., and Anstey, R. L. 1979. A developmental explanation of stability–diversity–variation hypotheses: morphogenetic regulation in Ordovician bryozoan colonies. Paleobiology, 5:168187.Google Scholar
Perry, T. G., and Hattin, D. E. 1958. Astogenetic study of fistuliporoid bryozoans. Journal of Paleontology, 32:10391050.Google Scholar
Podell, M. E., and Anstey, R. L. 1979. The interrelationship of early colony development, monticules and branches in Paleozoic bryozoans. Palaeontology, 22:965982.Google Scholar
Ross, J. P. 1967. Evolution of ectoproct genus Prasopora in Trentonian time (Middle Ordovician) in northern and central United States. Journal of Paleontology, 41:403416.Google Scholar
Ruedemann, R. 1904. Graptolites of New York, Pt. I, Graptolites of the Lower Beds. New York State Museum, Memoir 7:455803.Google Scholar
Russ, J. C. 1986. Practical Stereology. Plenum Press, New York, 185 p.Google Scholar
Ryland, J. S. 1970. Bryozoans. Hutchinson and Co., Ltd., London, 175 p.Google Scholar
Silen, L. 1977. Polymorphism, p. 183231. In Woollacott, R. M. and Zimmer, R. L. (eds.), Biology of Bryozoans. Academic Press, New York.CrossRefGoogle Scholar
Simms, M. J. 1988. Patterns of evolution among Lower Jurassic crinoids. Historical Biology, 1:1744.Google Scholar
Sokal, R. R., and Rohlf, F. J. 1981. Biometry. W. H. Freeman and Co., San Francisco, 850 p.Google Scholar
Taylor, P. D. 1988. Colony growth pattern and astogenetic gradients in the Cretaceous cheilostome bryozoan Herpetopora. Palaeontology, 31:519549.Google Scholar
Tissot, B. N. 1988. Geographic variation and heterochrony in two species of cowries (genus Cypraea). Evolution, 42:103117.Google Scholar
Urbanek, A. 1973. Organization and evolution of graptolite colonies, p. 441514. In Boardman, R. S., Cheetham, A. H., and Oliver, W. A. (eds.), Animal Colonies. Dowden, Hutchinson and Ross, Stroudsburg, Pennsylvania.Google Scholar
Weibel, E. R. 1980. Stereological Methods. Academic Press, Orlando, Florida, 416 p.Google Scholar
Worthen, A. H., and Meek, F. B. 1875. Description of invertebrates. Geological Survey of Illinois, 6:489532.Google Scholar