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Testing for bias in the evolution of coloniality: a demonstration in cyclostome bryozoans
Published online by Cambridge University Press: 08 April 2016
Abstract
Colonial organisms vary in the degree to which they are individuated at the colony level, i.e., in the degree to which the colony constitutes a unified whole, as opposed to a group of independent lower-level entities. Various arguments have been offered suggesting that evolutionary change along this continuum may be biased, that increases may be more probable than decreases. However, counterarguments can be devised, and the existing evidence is meager and inconclusive. In this paper, we demonstrate how the question can be addressed empirically by conducting a test for bias in a group of stenolaemate bryozoans, the cyclostomes. More specifically, we suggest three criteria for colony individuation: degree of connectedness among lower-level entities (in this case, zooids), degree of differentiation among lower-level entities, and number of intermediate-level parts. And we show how these criteria can be used together with a phylogeny and ancestral-state reconstruction methods to test for bias. In this case, results do not unambiguously support any single interpretation but are somewhat supportive of a null hypothesis of no bias in favor of increase.
As part of the demonstration, we also show how results can be transformed into a quantitative estimate of an upper limit on bias. Finally, we place the question of bias in a larger context, arguing that the same criteria and methods we employ here can be used to test for bias in other colonial taxa, and also at other hierarchical levels, for example, in the transitions from free-living eukaryotic cells to multicellular organisms.
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Literature Cited
Allen, T. F. H., and Hoekstra, T. W. 1992. Toward a unified ecology. Columbia University Press, New York.Google Scholar
Alroy, J. 1998. Cope's rule and the dynamics of body mass evolution in North American fossil mammals. Science 280:731–734.CrossRefGoogle ScholarPubMed
Alroy, J. 2000. Understanding the dynamics of trends within evolving lineages. Paleobiology 26:319–329.Google Scholar
American Naturalist. 1997. Multilevel selection: a symposium organized by David Sloan Wilson. American Naturalist 150 (Suppl.).Google Scholar
Anderson, C., and McShea, D. W. 2001. Individual versus social complexity, with particular reference to ant colonies. Biological Reviews 76:211–237.Google Scholar
Banta, W. C. 1973. Evolution of avicularia in cheilostome Bryozoa. Pp. 295–303in Boardman, et al. 1973.Google Scholar
Banta, W. C., McKinney, F. K., and Zimmer, R. L. 1974. Bryozoan monticules: excurrent water outlets? Science 185:783–784.Google Scholar
Beklemishev, W. N. 1969. Principles of comparative anatomy of invertebrates. In Kabata, Z., ed. Translated by MacLennan, J. M.Propmorphology. Vol. I. University of Chicago Press, Chicago.Google Scholar
Bell, G., and Mooers, A. O. 1997. Size and complexity among multicellular organisms. Biological Journal of the Linnean Society 60:345–363.Google Scholar
Boardman, R. S. 1983. General features of the class Stenolaemata. Pp. 49–137in Boardman, R. S. et al. Bryozoa. Part G of R. A. Robison, ed.Treatise on invertebrate paleontology. Geological Society of America, Boulder, Colo., and University of Kansas, Lawrence.Google Scholar
Boardman, R. S. 1998. Reflections on the morphology, anatomy, evolution, and classification of the class Stenolaemata (Bryozoa). Smithsonian Contributions to Paleobiology No. 86.Google Scholar
Boardman, R. S., and Cheetham, A. H. 1973. Degrees of colony dominance in stenolaemate and gymnolaemate Bryozoa. Pp. 121–220in Boardman, et al. 1973.Google Scholar
Boardman, R. S., and Cheetham, A. H. 1987. Phylum Bryozoa. Pp. 497–549in Boardman, R. S., Cheetham, A. H., and Rowell, A. J., eds. Fossil invertebrates. Blackwell Scientific, Palo Alto, Calif.Google Scholar
Boardman, R. S., Cheetham, A. H., and Oliver, W. A. Jr., eds. 1973. Animal colonies: development and function through time. Dowden, Hutchinson, and Ross, Stroudsburg, Penn.Google Scholar
Boardman, R. S., Cheetham, A. H., and Cook, P. L. 1983. Introduction to the Bryozoa. Pp. 3–48in Boardman, R. S. et al. Bryozoa. Part G of R. A. Robison, ed. Treatise on invertebrate paleontology. Geological Society of America, Boulder, Colo., and University of Kansas, Lawrence.Google Scholar
Bonner, J. T. 1988. The evolution of complexity. Princeton University, Princeton, N.J.Google Scholar
Borg, F. 1926. Studies on recent cyclostomatous Bryozoa. Zoologiska Bidrag från Uppsala 10:181–507.Google Scholar
Bourke, A. F. G. 1999. Colony size, social complexity and reproductive conflict in social insects. Journal of Evolutionary Biology 12:245–257.Google Scholar
Brandon, R. N. 1996. Concepts and methods in evolutionary biology. Cambridge University Press, Cambridge.Google Scholar
Brandon, R. N. 1999. The units of selection revisited: the modules of selection. Biology and Philosophy 14:167–180.CrossRefGoogle Scholar
Buss, L. W. 1987. The evolution of individuality. Princeton University Press, Princeton, N.J.Google Scholar
Campbell, D. T. 1958. Common fate, similarity, and other indices of the status of aggregates of persons as social entities. Behavioral Sciences 3:14–25.Google Scholar
Cheetham, A. H. 1973. Study of cheilostome polymorphism using principal components analysis. Pp. 385–409in Larwood, G. P., ed. Living and fossil Bryozoa. Academic Press, London.Google Scholar
Cisne, J. L. 1974. Evolution of the world fauna of aquatic free-living arthropods. Evolution 28:337–366.Google Scholar
Coates, A. G., and Oliver, W. A. Jr. 1973. Coloniality in zoantharian corals. Pp. 3–27in Boardman, et al. 1973.Google Scholar
Cook, P. L. 1979. Some problems in interpretation of hetero-morphy and colony integration in Bryozoa. Pp. 3–27in Larwood, and Rosen, 1979.Google Scholar
Cowen, R., and Rider, J. 1972. Functional analysis of fenestellid bryozoans. Lethaia 5:145–164.CrossRefGoogle Scholar
Cunningham, C. W. 1999. Some limitations of ancestral character-state reconstruction when testing evolutionary hypotheses. Systematic Biology 48:665–674.CrossRefGoogle Scholar
Cunningham, C. W., Omland, K. E., and Oakley, T. H. 1998. Reconstructing ancestral character states: a critical reappraisal. Trends in Ecology and Evolution 13:361–366.Google Scholar
Danchin, E., and Wagner, R. H. 1997. The evolution of coloniality: the emergence of new perspectives. Trends in Ecology and Evolution 12:342–347.Google Scholar
Danforth, B. N. 2002. Evolution of sociality in a primitively eu-social lineage of bees. Proceedings of the National Academy of Sciences USA 99:286–290.CrossRefGoogle Scholar
Danforth, B. N., and Eickwort, G. C. 1997. The evolution of social behavior in the augochlorine sweat bees (Hymenoptera: Halictidae) based on a phylogenetic analysis of the genera. Pp. 270–292in Choe, J. C. and Crespi, B. J., eds. The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge.Google Scholar
Dewel, R. A. 2000. Colonial origin for Eumetazoa: major morphological transitions and the origin of bilaterian complexity. Journal of Morphology 243:35–74.Google Scholar
Duffy, J. E., Morrison, C. L., and Ríos, R. 2000. Multiple origins of eusociality among sponge-dwelling shrimps (Synalpheus). Evolution 54:503–516.Google Scholar
Foote, M., and Sepkoski, J. J. Jr. 1999. Absolute measures of completeness of the fossil record. Nature 398:415–417.Google Scholar
Gadagkar, R. 1997. Social evolution—has nature ever rewound the tape? Current Science 72:950–956.Google Scholar
Ghiselin, M. T. 1997. Metaphysics and the origin of species. State University of New York Press, Albany.Google Scholar
Gould, S. J. 1996. Full house: the spread of excellence from Plato to Darwin. Harmony Books, New York.Google Scholar
Gould, S. J., and Lloyd, E. A. 1999. Individuality and adaptation across levels of selection: how shall we name and generalize the unit of Darwinism. Proceedings of the National Academy of Sciences USA 96:11904–11909.CrossRefGoogle Scholar
Harvell, C. D. 1994. The evolution of polymorphism in colonial invertebrates and social insects. Quarterly Review of Biology 69:155–185.Google Scholar
Hayward, P. J., and Ryland, J. S. 1985. Cyclostome bryozoans. Synopses of the British Fauna (New Series), No. 34. Bath Press, Avon, England.Google Scholar
Huelsenbeck, J. P. 1994. Comparing the stratigraphic record to estimates of phylogeny. Paleobiology 20:470–483.Google Scholar
Hughes, D. J., and Jackson, J. B. C. 1990. Do constant environments promote complexity of form? The distribution of bryozoan polymorphism as a test of hypotheses. Evolution 44:889–905.CrossRefGoogle ScholarPubMed
Hull, D. L. 1980. Individuality and selection. Annual Review of Ecology and Systematics 11:311–332.Google Scholar
Hutchings, M. J., and Wijesinghe, D. K. 1997. Patchy habitats, division of labour and growth dividends in clonal plants. Trends in Ecology and Evolution 12:390–394.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
Keller, L., ed. 1999. Levels of selection in evolution. Princeton University Press, Princeton, N.J.Google Scholar
Keller, L., and Reeve, H. K. 1999. Dynamics of conflict within insect societies. Pp. 153–175in Keller, 1999.Google Scholar
Key, M. M. Jr., Thrane, L., and Collins, J. A. 2001. Functional morphology of maculae in a giant ramose bryozoan from the Permian of Greenland. In Wyse Jackson, P. N., Butler, C. J., and Jones, M. S., eds. Bryozoan studies 2001. Balkema, Rotterdam(in press).Google Scholar
Kitchen, D M., and Packer, C. 1999. Complexity in vertebrate societies. Pp. 176–196in Keller, 1999.Google Scholar
Larwood, G., and Rosen, B. R., eds. 1979. Biology and systematics of colonial organisms. Systematics Association Special Volume 11. Academic Press, London.Google Scholar
Larwood, G. P., and Taylor, P. D. 1979. Early structural diversification and ecological diversification in the Bryozoa. In House, M. R., ed. The origin of the major invertebrate groups. Systematics Association Special Volume 12:209–234. Academic Press, London.Google Scholar
Leigh, E. G. Jr. 1983. When does the good of the group override the advantage of the individual? Proceedings of the National Academy of Sciences USA 80:2985–2989.CrossRefGoogle Scholar
Leigh, E. G. Jr. 1991. Genes, bees and ecosystems: the evolution of a common interest among individuals. Trends in Ecology and Evolution 6:257–262.Google Scholar
Lidgard, S. 1985. Zooid and colony growth in encrusting bryozoans. Palaeontology 28:255–291.Google Scholar
Lidgard, S. 1986. Ontogeny in animal colonies: a persistent trend in the bryozoan fossil record. Science 232:230–232.Google Scholar
Lidgard, S., and Jackson, J. B. C. 1989. Growth in encrusting cheilostome bryozoans. I. Evolutionary trends. Paleobiology 15:255–282.Google Scholar
Mackie, G. O. 1986. From aggregates to integrates: physiological aspects of modularity in colonial animals. Philosophical Transactions of the Royal Society of London B 313:175–196.Google Scholar
Maddison, W. P., and Maddison, D. R. 1992. MacClade: analysis of phylogeny and character evolution, Version 3.0. Sinauer, Sunderland, Mass.Google Scholar
Maynard Smith, J. 1988. Evolutionary progress and levels of selection. Pp. 219–230in Nitecki, M. H., ed. Evolutionary progress. University of Chicago Press, Chicago.Google Scholar
Maynard Smith, J., and Szathmáry, E. 1995. The major transitions in evolution. W. H. Freeman, Oxford.Google Scholar
McKinney, F. K. 1984. Feeding currents of gymnolaemate bryozoans: better organization with higher colonial integration. Bulletin of Marine Sciences 34:315–319.Google Scholar
McKinney, F. K. 1986. Historical record of erect bryozoan growth forms. Proceedings of the Royal Society of London B 228:133–149.Google Scholar
McKinney, F. K. 1990. Feeding and associated colonial morphology in marine bryozoans. Reviews in Aquatic Sciences 2:255–280.Google Scholar
McKinney, F. K., and Jackson, J. B. C. 1989. Bryozoan evolution. University of Chicago Press, Chicago.Google Scholar
McKinney, F. K., Jackson, J. B. C., and Taylor, P. D. 1997. Life histories of some Mesozoic encrusting cyclostome bryozoans. Palaeontology 40:515–556.Google Scholar
McShea, D. W. 1996. Metazoan complexity and evolution: is there a trend? Evolution 50:477–492.Google Scholar
McShea, D. W. 2001a. The “minor transitions” in hierarchical evolution and the question of directional bias. Journal of Evolutionary Biology 14:502–518.Google Scholar
McShea, D. W. 2001b. Hierarchical complexity of organisms: a scale and documentation of a trend in the maximum. Paleobiology 27:405–423.Google Scholar
McShea, D. W., and Venit, E. P. 2001. What is a part? Pp. 259–284in Wagner, G. P., ed. The character concept in evolutionary biology. Academic Press, San Diego.Google Scholar
McShea, D. W., Venit, E. P., and Simon, V. 1999. Hierarchical complexity of organisms: dynamics of a well-known trend. Geological Society of America Abstracts with Programs 31:A171.Google Scholar
Michod, R. E. 1999. Darwinian dynamics: evolutionary transitions in fitness and individuality. Princeton University Press, Princeton, N.J.Google Scholar
Mishler, B. D., and Brandon, R. N. 1987. Individuality, pluralism, and the phylogenetic species concept. Biology and Philosophy 2:397–414.Google Scholar
Mooers, A. Ø., and Schluter, D. 1999. Reconstructing ancestor states with maximum likelihood: support for one- and two-rate models. Systematic Biology 48:623–633.Google Scholar
Moritz, R. F. A., and Southwick, E. E. 1992. Bees as superorganisms. Springer, Berlin.Google Scholar
Nielsen, C., and Pedersen, K. J. 1979. Cystid structure and protrusion of the polypide in Crisia (Bryozoa, Cyclostomata). Acta Zoologica (Stockholm) 60:65–88.Google Scholar
Omland, K. E. 1997. Examining two standard assumptions of ancestral reconstructions: repeated loss of dichromatism in dabbling duck (Anatini). Evolution 51:1636–1646.Google Scholar
Omland, K. E. 1999. The assumptions and challenges of ancestral state reconstructions. Systematic Biology 48:604–611.Google Scholar
Pagel, M. 1994. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London B 255:37–45.Google Scholar
Pagel, M. 1997. Inferring evolutionary processes from phylogenies. Zoologica Scripta 26:331–348.Google Scholar
Pagel, M. 1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology 48:612–622.Google Scholar
Ree, R. H., and Donoghue, M. J. 1999. Inferring rates of change in flower symmetry in asterid angiosperms. Systematic Biology 48:633–641.Google Scholar
Ryland, J. S. 1979. Structural and physiological aspects of coloniality in Bryozoa. Pp. 211–242in Larwood, and Rosen, 1979.Google Scholar
Salthe, S. N. 1985. Evolving hierarchical systems. Columbia University Press, New York.Google Scholar
Sanderson, M. J. 1993. Reversibility in evolution: a maximum likelihood approach to character gain/loss bias in phylogenies. Evolution 47:236–252.Google Scholar
Schluter, D., Price, T., Mooers, A. Ø., and Ludwig, D. 1997. Likelihood of ancestor states in adaptive radiation. Evolution 51:1699–1711.Google Scholar
Schopf, T. J. M. 1973. Ergonomics of polymorphism: its relation to the colony as the unit of natural selection in species of the phylum Ectoprocta. Pp. 247–294in Boardman, et al. 1973.Google Scholar
Silén, L. 1977. Polymorphism. Pp. 183–231in Woollacott, R. M. and Zimmer, R. L., eds. Biology of bryozoans. Academic Press, New York.CrossRefGoogle Scholar
Simon, H. A. 1962. The architecture of complexity. Proceedings of the American Philosophical Society 106:467–482.Google Scholar
Sober, E., and Wilson, D. S. 1994. A critical review of the philosophical work on the units of selection problem. Philosophy of Science 61:534–555.Google Scholar
Swofford, D. L. 1998. PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer, Sunderland, Mass.Google Scholar
Taylor, P. D. 1999. Bryozoans. Pp. 623–646in Savazzi, E., ed. Functional morphology of the invertebrate skeleton. Wiley, New York.Google Scholar
Taylor, P. D. 2000. Cyclostome systematics: Phylogeny, suborders, and the problem of skeletal organization. Pp. 87–103in Herrera-Cubilla, A. and Jackson, J. B. C., eds. Proceedings of the 11th International Bryozoology Association Conference. Smithsonian Tropical Research Institute, Balboa, Republic of Panama.Google Scholar
Taylor, P. D., and Furness, R. W. 1978. Astogenetic and environmental variation of zooid size within colonies of Jurassic Stomatopora (Bryozoa, Cyclostomata). Journal of Paleontology 52:1093–1102.Google Scholar
Taylor, P. D., and Weedon, M. J. 2000. Skeletal ultrastructure and phylogeny of cyclostome bryozoans. Zoological Journal of the Linnean Society 128:337–399.CrossRefGoogle Scholar
Taylor, P. D., and Wilson, M. A. 1996. Cuffeyella, a new bryozoan genus from the Late Ordovician of North America, and its bearing on the origin of post-Paleozoic cyclostomates. Pp. 351–360in Gordon, D. P., Smith, A. M., and Grant-Mackie, J. A., eds. Bryozoans in space and time. NIWA, Wellington, New Zealand.Google Scholar
Valentine, J. W., Collins, A. G., and Meyer, C. P. 1994. Morphological complexity increase in metazoans. Paleobiology 20:131–142.Google Scholar
Vermeij, G. J. 1987. Evolution and escalation. Princeton University Press, Princeton, N.J.Google Scholar
Wagner, G. P., and Laubichler, M. D. 2000. Character identification in evolutionary biology: the role of the organism. Theory in Biosciences 119:20–40.Google Scholar
Wagner, P. J. 1996. Contrasting the underlying patterns of active trends in morphologic evolution. Evolution 50:990–1007.Google Scholar
Wagner, P. J., and Erwin, D. H. 1995. Phylogenetic patterns as tests of speciation models. Pp. 87–122in Erwin, D. H. and Anstey, R. L., eds. New approaches to speciation in the fossil record. Columbia University Press, New York.Google Scholar
Wcislo, W. T., and Danforth, B. N. 1997. Secondarily solitary: the evolutionary loss of social behavior. Trends in Ecology and Evolution 12:468–474.Google Scholar
Wilson, E. O. 1975. Sociobiology: the new synthesis. Harvard University Press, Cambridge.Google Scholar
Wilson, J. 1999. Biological individuality: the identity and persistence of living entities. Cambridge University Press, Cambridge.Google Scholar