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Phylogeny reconstruction and the tempo of speciation in cheilostome Bryozoa

Published online by Cambridge University Press:  08 February 2016

Jeremy B. C. Jackson
Affiliation:
Center for Tropical Paleoecology and Archaeology, Smithsonian Tropical Research Institute, Box 1072, Balboa, Republic of Panama
Alan H. Cheetham
Affiliation:
Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560

Abstract

We compared phylogenies derived from morphological data for two cheilostome bryozoan genera, Stylopoma and Metrarabdotos, with genetic differences between species (Stylopoma) and the stratigraphic occurrence of fossils (both genera). Correspondence between species of Stylopoma defined by protein electrophoresis and on preservable skeletal morphology is excellent, despite great morphological variability within colonies and the predominance of quantitative over discrete characters. Moreover, agreement between genetic and morphological classifications increased greatly when morphological discrimination was pushed to the limit, despite inability to consistently assign all specimens to species with high confidence. This “splitting” strategy also maximized the correlation between genetic distances and the distances between species in cladistically derived phylogenies.

Fossil and living species of both genera are sufficiently abundant and widespread to provide credible limits for inferred ancestral relationships. Inclusion of fossils in cladistic analyses of Stylopoma increased the consistency of cladistic hypotheses by up to 30% and provided a more effective means of rooting trees than comparison with living species of the most closely related genus (“outgroup”). Moreover, in the case of Metrarabdotos, failure to incorporate stratigraphic information turned the cladogram virtually upside down, so that postulated ancestors first appear in the fossil record 6–16 m.y. after their putative descendants became extinct.

Stratigraphically rooted trees suggest that most well-sampled Metrarabdotos and Stylopoma species originated fully differentiated morphologically and persisted unchanged for > 1 to > 16 m.y., typically alongside their putative ancestors. Moreover, the tight correlation between phenetic, cladistic, and genetic distances among living Stylopoma species suggests that changes in all three variables occurred together during speciation. All of these observations support the punctuated equilibrium model of speciation.

Type
Research Article
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Archie, J. W. 1985. Methods for coding variable morphological features for numerical taxonomic analysis. Systematic Zoology 34:326334.CrossRefGoogle Scholar
Archie, J. W., Simon, C., and Martin, A. 1989. Small sample size does decrease the stability of dendrograms calculated from allozyme-frequency data. Evolution 43:678683.Google ScholarPubMed
Bell, G. 1982. The masterpiece of nature: the evolution and genetics of sexuality. Croom Helm, London.Google Scholar
Best, M. B., Boekschoten, G. J., and Oosterbaan, A. 1984. Species concept and ecomorph variation in living and fossil Scleractinia. Palaeontographica Americana 54:7079.Google Scholar
Budd, A. F., and Coates, A. G. 1992. Non-progressive evolution in a clade of Cretaceous Montastrea-like corals. Paleobiology 18:425446.CrossRefGoogle Scholar
Budd, A. F., and Mishler, B. 1990. Species and evolution in clonal organisms—summary and discussion. Systematic Botany 15:166171.CrossRefGoogle Scholar
Canu, F., and Bassler, R. S. 1920. North American early Tertiary Bryozoa. United States National Museum Bulletin 106:1879.Google Scholar
Canu, F., and Bassler, R. S. 1923. North American later Tertiary and Quaternary Bryozoa. United States National Museum Bulletin 125:1302.Google Scholar
Cheetham, A. H. 1966. Cheilostomatous Polyzoa from the Upper Bracklesham Beds (Eocene) of Sussex. Bulletin British Museum (Natural History) Geology 13:1115.CrossRefGoogle Scholar
Cheetham, A. H. 1968. Morphology and systematics of the bryozoan genus Metrarabdotos. Smithsonian Miscellaneous Collections 153:1121.Google Scholar
Cheetham, A. H. 1973. Study of cheilostome polymorphism using principal components analysis. Pp. 385409in Larwood, G. P., ed. Living and fossil Bryozoa. Academic Press, London.Google Scholar
Cheetham, A. H. 1986. Tempo of evolution in a Neogene bryozoan: rates of morphologic change within and across species boundaries. Paleobiology 12:190202.CrossRefGoogle Scholar
Cheetham, A. H. 1987. Tempo of evolution in a Neogene bryozoan: are trends in single morphologic characters misleading? Paleobiology 13:286296.CrossRefGoogle Scholar
Cheetham, A. H., and Hayek, L. C. 1988. Phylogeny reconstruction in the Neogene bryozoan Metrarabdotos: a paleontological evaluation of methodology. Historical Biology 1:6583.CrossRefGoogle Scholar
Cheetham, A. H., and Jackson, J. B. C. 1994a. Process from pattern: tests for selection versus random change in punctuated bryozoan speciation. In Erwin, D. H. and Anstey, R. L., eds. New approaches to speciation in the fossil record. Columbia University Press, New York(in press).Google Scholar
Cheetham, A. H., and Jackson, J. B. C. 1994b. Speciation, extinction, and the decline of arborescent growth in Neogene and Quaternary cheilostome Bryozoa of tropical America. In Jackson, J. B. C., Coates, A. G., and Budd, A. F., eds. Evolution and environment in tropical America. University of Chicago Press, Chicago(in press).Google Scholar
Cheverud, J. M. 1988. A comparison of genetic and phenotypic correlations. Evolution 42:958968.CrossRefGoogle ScholarPubMed
Coates, A. G., Jackson, J. B. C., Collins, L. S., Cronin, T. M., Dowsett, H. J., Bybell, L. M., Jung, P., and Obando, J. A. 1992. Closure of the Isthmus of Panama: the near-shore marine record of Costa Rica and western Panama. Geological Society of America Bulletin 104:814828.2.3.CO;2>CrossRefGoogle Scholar
Cook, P. L. 1973. Settlement and early colony development in some Cheilostomata. Pp. 6571in Larwood, G. P., ed. Living and fossil Bryozoa. Academic Press, London.Google Scholar
Cook, P. L. 1986. Bryozoa from Ghana—a preliminary survey. Koninklijk Museum voor Midden-Afrika (Tevuren, België), Annalen Zoologische Wetenschappen 238:1315.Google Scholar
Cracraft, J. 1989. Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. Pp. 2859in Otte, and Endler, 1989.Google Scholar
Donoghue, M. J., Doyle, J. A., Gauthier, J., Kluge, A. G., and Rowe, T. 1989. The importance of fossils in phylogeny reconstruction. Annual Reviews of Ecology and Systematics 20:431460.CrossRefGoogle Scholar
Eldredge, N., and Gould, S. J. 1972. Punctuated equilibria: an alternative to phyletic gradualism. Pp. 82115in Schopf, T. J. M., ed. Models in paleobiology. Freeman, San Francisco.Google Scholar
Eldredge, N., and Novacek, M. J. 1985. Systematics and paleobiology. Paleobiology 11:6574.CrossRefGoogle Scholar
Farris, J. S. 1988. Hennig86 reference, Version 1.5. Farris, Stony Brook, N.Y.Google Scholar
Felsenstein, J. 1988. Phylogenies and quantitative characters. Annual Review of Ecology and Systematics 18:445471.CrossRefGoogle Scholar
Foster, A. B. 1980. Environmental variation in skeletal morphology within the Caribbean reef corals Montastrea annularis and Siderastrea siderea. Bulletin of Marine Science 30:678709.Google Scholar
Foster, A. B. 1984. The species concept in fossil hermatypic corals: a statistical approach. Palaeontographica Americana 54:5869.Google Scholar
Gauthier, J., Kluge, A. G., and Rowe, T. 1988. Amniote phylogeny and the importance of fossils. Cladistics 4:105209.CrossRefGoogle ScholarPubMed
Geary, D. H. 1990. Patterns of evolutionary tempo and mode in the radiation of Melanopsis (Gastropoda; Melanopsidae). Paleobiology 16:492511.CrossRefGoogle Scholar
Gingerich, P. D. 1979. The stratophenetic approach to phylogeny reconstruction in vertebrate paleontology. Pp. 4177in Cracraft, J. and Eldredge, N., eds. Phylogenetic analysis and paleontology. Columbia University Press, New York.CrossRefGoogle Scholar
Gordon, D. P. 1989. The marine fauna of New Zealand: Bryozoa: Gymnolaemata (Cheilostomida Ascophorina) from the western South Island continental shelf and slope. New Zealand Ocean-ographic Institute Memoir 97:1158.Google Scholar
Gould, S. J., and Eldredge, N. 1993. Punctuated equilibrium comes of age. Nature 366:223227.CrossRefGoogle ScholarPubMed
Harmer, S. F. 1957. The Polyzoa of the Siboga Expedition, part IV, Cheilostomata Ascophora. Siboga-Expeditie 28:6411147.Google Scholar
Harris, H., and Hopkinson, D. A. 1976. Handbook of enzyme electrophoresis in human genetics. North Holland, Amsterdam.Google Scholar
Hayward, P. J., and Ryland, J. S. 1979. British ascophoran bryozoans. Academic Press, London.Google Scholar
Hayward, P. J., and Thorpe, J. P. 1987. The systematic position of Smittia inclusa Waters, an endemic Antarctic bryozoan. Journal of Natural History 21:14691476.CrossRefGoogle Scholar
Hillis, D. M. 1987. Molecular versus morphological approaches to systematics. Annual Review of Ecology and Systematics 18:2342.CrossRefGoogle Scholar
Huelsenbeck, J. P. 1991. When are fossils better than extant taxa in phylogenetic analysis? Systematic Zoology 40:458469.CrossRefGoogle Scholar
Hughes, D. J., and Jackson, J. B. C. 1992. Distribution and abundance of cheilostome bryozoans on the Caribbean reefs of central Panama. Bulletin of Marine Science 51:443465.Google Scholar
Hughes, R. N. 1989. A functional biology of clonal animals. Chapman and Hall, London.Google Scholar
Jackson, J. B. C. 1984. Ecology of cryptic coral reef communities. III. Abundance and aggregation of encrusting organisms with particular reference to cheilostome Bryozoa. Journal of Experimental Marine Biology and Ecology 75:3757.CrossRefGoogle Scholar
Jackson, J. B. C. 1985. Distribution and ecology of clonal and aclonal benthic invertebrates. Pp. 297355in Jackson, J. B. C., Buss, L. W., and Cook, R. E., eds. Population biology and evolution of clonal organisms. Yale University Press, New Haven, Conn.Google Scholar
Jackson, J. B. C., and Cheetham, A. H. 1990. Evolutionary significance of morphospecies: a test with cheilostome Bryozoa. Science 248:579583.CrossRefGoogle ScholarPubMed
Jackson, J. B. C., and Cheetham, A. H. 1991. Bryozoan morphological and genetic correspondence: what does it prove? Science 251:319.CrossRefGoogle Scholar
Jackson, J. B. C., and Coates, A. G. 1986. Life cycles and evolution of clonal (modular) animals. Philosophical Transactions of the Royal Society of London B 313:722.Google Scholar
Jackson, J. B. C., Buss, L. W., and Cook, R. E., eds. 1985. Population biology and evolution of clonal organisms. Yale University Press, New Haven, Conn.Google Scholar
Klassen, G. J., Mool, R. D., and Locke, A. 1991. Consistency indices and random data. Systematic Zoology 40:446457.CrossRefGoogle Scholar
Knowlton, N. 1993. Sibling species in the sea. Annual Review of Ecology and Systematics 24:189216.CrossRefGoogle Scholar
Knowlton, N., and Jackson, J. B. C. 1994. Jack of all trades or master of some? new taxonomy and niche partitioning on coral reefs. Trends in Ecology and Evolution 9:79.CrossRefGoogle ScholarPubMed
Knowlton, N., Weil, E., Weigt, L. A., and Guzman, H. M. 1992. Sibling species in Montastrea annularis, coral bleaching, and the coral climate record. Science 255:330333.CrossRefGoogle Scholar
Lang, J. 1984. Whatever works: the variable importance of skeletal and non-skeletal characters in scleractinian taxonomy. Palaeontographica Americana 54:1844.Google Scholar
Larson, A. 1989. The relationship between speciation and morphological evolution. Pp. 579598in Otte, and Endler, 1989.Google Scholar
Levinton, J. S. 1988. Genetics, paleontology and macroevolution. Cambridge University Press, Cambridge, United Kingdom.Google Scholar
Levinton, J. S. 1991. Bryozoan morphologic and genetic correspondence: what does it prove? Science 251:318319.CrossRefGoogle ScholarPubMed
Lidgard, S. 1985. Zooid and colony growth in encrusting cheilostome bryozoans. Palaeontology 28:255291.Google Scholar
Lidgard, S., and Jackson, J. B. C. 1989. Growth in encrusting bryozoans. I. Evolutionary trends. Paleobiology 15:255282.CrossRefGoogle Scholar
Marshall, C. R. 1990. Confidence intervals on stratigraphic ranges. Paleobiology 16:110.CrossRefGoogle Scholar
Marshall, C. R. 1991. Estimation of taxonomic ranges from the fossil record. Pp. 1938in Gilinsky, N. L. and Signor, P. L., eds. Analytical paleobiology. The Paleontological Society, Knoxville, Tenn.Google Scholar
Marshall, C. R. 1994. Stratigraphy, the true order of species' originations and extinctions, and testing ancestor-descendant hypotheses among Caribbean Neogene bryozoans. In Erwin, D. H. and Anstey, R. L., eds. New approaches to speciation in the fossil record. Columbia University Press, New York(in press).Google Scholar
Maturo, F. J. S. Jr., and Schopf, T. J. M. 1968. Ectoproct and entoproct type material: reexamination of species from New England and Bermuda named byVerrill, A. E., Dawson, J. W. and Dessor, E.Postilla 120:195.Google Scholar
Morse, D. E., Hooker, N., Morse, A. N. C., and Jensen, R. A. 1988. Control of larval metamorphosis and recruitment in sympatric agariciid corals. Journal of Experimental Marine Biology and Ecology 116:193217.CrossRefGoogle Scholar
Nei, M., Tajima, F., and Tateno, Y. 1983. Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. Journal of Molecular Evolution 19:153170.CrossRefGoogle ScholarPubMed
Nelson, G. 1989. Species and taxa: systematics and evolution. Pp. 6081in Otte, and Endler, 1989.Google Scholar
Norusis, M. J. 1990. SPSS/PC+ advanced statistics 4.0 for the IBM PC/XT/AT and PS/2. SPSS, Chicago.Google Scholar
Novacek, M. J. 1992. Fossils, topologies, missing data, and the higher level phylogeny of eutherian mammals. Systematic Biology 41:5873.CrossRefGoogle Scholar
Otte, D., and Endler, J. A., eds. 1989. Speciation and its consequences. Sinauer, Sunderland, Mass.Google Scholar
Potts, D. C. 1984. Generation times and the Quaternary evolution of reef-building corals. Paleobiology 10:4858.CrossRefGoogle Scholar
Selander, R. K., Smith, M. H., Yang, S. Y., Johnson, W. E., and Gentry, J. R. 1971. Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old-field mouse (Peromyscus polionotos). Studies in genetics VI. University of Texas Publication 7103:4990.Google Scholar
Shaffer, H. B., Clark, J. M., and Kraus, F. 1991. When molecules and morphology clash: a phylogenetic analysis of the North American ambystomatid salamanders (Caudata: Ambystomatidae). Systematic Zoology 40:284303.CrossRefGoogle Scholar
Wei, K.-Y., and Kennett, J. P. 1988. Phyletic gradualism and punctuated equilibrium in the late Neogene planktonic foraminiferal clade Globoconella. Paleobiology 14:345363.CrossRefGoogle Scholar
Winston, J. E. 1982. Marine bryozoans (Ectoprocta) of the Indian River area (Florida). Bulletin of the American Museum of Natural History 173:99176.Google Scholar
Winston, J. E., and Jackson, J. B. C. 1984. Ecology of cryptic coral reef communities. IV. Community development and life histories of encrusting cheilostome Bryozoa. Journal of Experimental Marine Biology and Ecology 76:121.CrossRefGoogle Scholar
Wood-Jones, F. 1907. On the growth forms and supposed species in corals. Proceedings of the Zoological Society of London 77:518566.Google Scholar
Zlatarski, V. N., and Estalella, N. M. 1982. Les Scléractinaires de Cuba avec des données sur les organismes associés. Editions de l'Académie Bulgare des Sciences, Sofia, Bulgaria.Google Scholar