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Increasing hierarchical complexity throughout the history of life: phylogenetic tests of trend mechanisms

Published online by Cambridge University Press:  14 July 2015

Jonathan D. Marcot
Affiliation:
Department of Biology, Duke University, Box 90338, Durham, North Carolina 27708-0338. E-mail: [email protected]
Daniel W. McShea
Affiliation:
Department of Biology, Duke University, Box 90338, Durham, North Carolina 27708-0338. E-mail: [email protected]

Abstract

The history of life is punctuated by a number of major transitions in hierarchy, defined here as the degree of nestedness of lower-level individuals within higher-level ones: the combination of single-celled prokaryotic cells to form the first eukaryotic cell, the aggregation of single eukaryotic cells to form complex multicellular organisms, and finally, the association of multicellular organisms to form complex colonial individuals. These transitions together constitute one of the most salient and certain trends in the history of life, in particular, a trend in maximum hierarchical structure, which can be understood as a trend in complexity. This trend could be produced by a biased mechanism, in which increases in hierarchy are more likely than decreases, or by an unbiased one, in which increases and decreases are about equally likely. At stake is whether or not natural selection or some other force acts powerfully over the history of life to drive complexity upward.

Too few major transitions are known to permit rigorous statistical discrimination of trend mechanisms based on these transitions alone. However, the mechanism can be investigated by using “minor transitions” in hierarchy, or, in other words, changes in the degree of individuation of the upper level. This study tests the null hypothesis that the probability (or rate) of increase and decrease in individuation are equal in a phylogenetic context. We found published phylogenetic trees for clades spanning minor transitions across the tree of life and identified changes in character states associated with those minor transitions. We then used both parsimony- and maximum-likelihood-based methods to test for asymmetrical rates of character evolution. Most analyses failed to reject equal rates of hierarchical increase and decrease. In fact, a bias toward decreasing complexity was observed for several clades. These results suggest that no strong tendency exists for hierarchical complexity to increase.

Type
Articles
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Adams, D. G. 2000. Heterocyst formation in cyanobacteria. Current Opinion in Microbiology 3:618624.Google Scholar
Akaike, H. 1973. Information theory and an extension of the maximum likelihood principle. Pp. 267281 in Petrov, B. N. and Csáki, F., eds. Second international symposium on information theory. Akadémiai Kiadó, Budapest.Google Scholar
Akaike, H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19:716723.CrossRefGoogle Scholar
Alroy, J. 2000. Understanding the dynamics of trends within evolving lineages. Paleobiology 26:219329.2.0.CO;2>CrossRefGoogle Scholar
Anderson, C., and McShea, D. W. 2001. Individual versus social complexity, with particular reference to ant colonies. Biological Reviews 76:211237.Google Scholar
Boardman, R. S., and Cheetham, A. H. 1973. Degrees of colony dominance in stenolaemate and gymnolaemate bryozoa. Pp. 121220 in Boardman, R. S., Cheetham, A. H., and Oliver, W. A. Jr., eds. Animal colonies: development and function through time. Dowden, Hutchinson, and Ross, Stroudsburg, Penn. Google Scholar
Bonner, J. T. 1988. The evolution of complexity. Princeton University Press, Princeton, N.J. Google Scholar
Bonner, J. T. 1998. The origins of multicellularity. Integrative Biology: Issues, News, and Reviews 1:2736.Google Scholar
Bonner, J. T. 2003. On the origin of differentiation. Journal of Biosciences 28:523528.Google Scholar
Brandon, R. N. 1999. The units of selection revisited: the modules of selection. Biology and Philosophy 14:167180.Google Scholar
Burnham, K. P., and Anderson, D. R. 2004. Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods and Research 33:261304.CrossRefGoogle Scholar
Connolly, S. R., and Miller, A. I. 2002. Global Ordovician faunal transitions in the marine benthos: ultimate causes. Paleobiology 28:2640.Google Scholar
Cunningham, C. W. 1999. Some limitations of ancestral character-state reconstruction when testing evolutionary hypotheses. Systematic Biology 48:665674.Google Scholar
Danforth, B. N. 2002. Evolution of sociality in a primitively eusocial lineage of bees. Proceedings of the National Academy of Sciences USA 99:286290.Google Scholar
Danforth, B. N., Conway, L., and Ji, S. 2003. Phylogeny of eusocial Lasioglossum reveals multiple losses of eusociality within a primitively eusocial clade of bees (Hymenoptera: Halictidae). Systematic Biology 52:2336.Google Scholar
Dollo, L. 1893. Les lois de l'évolution. Bulletin de la Société Belge de Géologie, de Paléontologie, et de Hydrologie 7:164166.Google Scholar
Edwards, A. W. F. 1992. Likelihood. Johns Hopkins University Press, Baltimore.CrossRefGoogle Scholar
Foote, M. 1996. On the probability of ancestors in the fossil record. Paleobiology 22:141151.Google Scholar
Foote, M. 2005. Pulsed origination and extinction in the marine realm. Paleobiology 31:620.Google Scholar
Gould, S. J. 1970. Dollo on Dollo's Law: irreversibility and the status of evolutionary laws. Journal of the History of Biology 3:189212.CrossRefGoogle ScholarPubMed
Gould, S. J. 1996. Full house: the spread of excellence from Plato to Darwin. Harmony, New York.CrossRefGoogle Scholar
Harvell, C. D. 1991. Coloniality and inducible polymorphism. American Naturalist 138:114.Google Scholar
Harvell, C. D. 1994. The evolution of polymorphism in colonial invertebrates and social insects. Quarterly Review of Biology 69:155185.Google Scholar
Huelsenbeck, J. P., and Rannala, B. 1997. Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276:227232.Google Scholar
Knoll, A. H., and Bambach, R. K. 2000. Directionality in the history of life: diffusion from the left wall or repeated scaling of the right? In Erwin, D. H. and Wing, S. L., eds. Deep time: Paleobiology's perspective. Paleobiology 26(Suppl. to No. 4):114.Google Scholar
Lewis, P. O. 2001. Maximum likelihood phylogenetic inference: modeling discrete morphological characters. Systematic Biology 50:913925.Google Scholar
Maddison, D. R., and Maddison, W. P. 2002. MacClade, Version 4. 06. Sinauer, Sunderland, Mass. Google Scholar
Maddison, W. P., and Maddison, D. R. 2004a. StochChar: a package of Mesquite modules for stochastic models of character evolution, Version 1. 05.Google Scholar
Maddison, W. P., and Maddison, D. R. 2004b. Mesquite: a modular system for evolutionary analysis, Version 1. 05.Google Scholar
Margulis, L., and Chapman, M. J. 1998. Endosymbioses: cyclical and permanent in evolution. Trends in Microbiology 6:342345.Google Scholar
Smith, J. Maynard, and Szathmáry, E. 1995. The major transitions in evolution. W. H. Freeman, Oxford.Google Scholar
McShea, D. W. 1994. Mechanisms of large-scale evolutionary trends. Evolution 48:17471763.Google Scholar
McShea, D. W. 1996. Metazoan complexity and evolution: is there a trend? Evolution 50:477492.Google ScholarPubMed
McShea, D. W. 2001a. The hierarchical structure of organisms: a scale and documentation of a trend in the maximum. Paleobiology 27:405423.Google Scholar
McShea, D. W. 2001b. The minor transitions in hierarchical evolution and the question of a directional bias. Journal of Evolutionary Biology 14:502518.Google Scholar
McShea, D. W. 2001c. Parts and integration: the consequences of hierarchy. Pp. 2760 in Jackson, J., Lidgard, S., and McKinney, K., eds. Evolutionary patterns: growth, form, and tempo in the fossil record. University of Chicago Press, Chicago.Google Scholar
McShea, D. W. 2002. Complexity drain on cells in the evolution of multicellularity. Evolution 56:441452.Google Scholar
McShea, D. W. 2005a. The evolution of complexity without natural selection, a possible large-scale trend of the fourth kind. Paleobiology 31:146156.Google Scholar
McShea, D. W. 2005b. A universal generative tendency toward increased organismal complexity. Pp. 435453 in Hallgrímsson, B., and Hall, B. K., eds. Variation: a central concept in biology. Elsevier, Amsterdam.Google Scholar
McShea, D. W., and Changizi, M. A. 2003. Three puzzles in hierarchical evolution. Integrative and Comparative Biology 43:7481.Google Scholar
McShea, D. W., and Venit, E. P. 2002. Testing for bias in the evolution of coloniality: a demonstration in cyclostome bryozoans. Paleobiology 28:308327.Google Scholar
Meeks, J. C., Campbell, E. L., Summers, M. L., and Wong, F. C. 2002. Cellular differentiation in the cyanobacterium Nostoc punctiforme . Archives of Microbiology 178:395403.Google Scholar
Michener, C. D. 1974. The social behavior of the bees: a comparative study. Harvard University Press, Cambridge.Google Scholar
Mooers, A. Ø., and Schluter, D. 1999. Reconstructing ancestor states with maximum likelihood: support for one- and two-rate models. Systematic Biology 48:623633.Google Scholar
Pagel, M. 1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology 48:612622.CrossRefGoogle Scholar
Posada, D., and Crandall, K. A. 2001. Selecting best-fit model of nucleotide substitution. Systematic Biology 50:580601.Google Scholar
Roze, D., and Michod, R. E. 2001. Mutation, multilevel selection, and the evolution of propagule size during the origin of multicellularity. American Naturalist 158:638654.Google Scholar
Salthe, S. N. 1985. Evolving hierarchical systems. Columbia University Press, New York.Google Scholar
Salthe, S. N. 1993. Development and evolution: complexity and change in biology. MIT Press, Cambridge.Google Scholar
Sanderson, M. J. 1993. Reversibility in evolution: a maximum likelihood approach to character gain/loss bias in phylogenies. Evolution 47:236252.Google Scholar
Schlichting, C. D. 2003. Origins of differentiation via phenotypic plasticity. Evolution and Development 5:98105.Google Scholar
Sterelny, K., and Griffiths, P. E. 1999. Sex and death: an introduction to philosophy of biology. University of Chicago Press, Chicago.CrossRefGoogle Scholar
Sullivan, J., and Joyce, P. 2005. Model selection in phylogenetics. Annual Review of Earth and Planetary Sciences 36:445466.Google Scholar
Szathmáry, E., and Smith, J. Maynard 1995. The major evolutionary transitions. Nature 374:227232.Google Scholar
Urbanek, A. 2003. Organization and evolution of animal colonies. Biology Bulletin 30:18.Google Scholar
Valentine, J. W., and May, C. L. 1996. Hierarchies in biology and paleontology. Paleobiology 22:2333.CrossRefGoogle Scholar
Van Valen, L. 1984. A resetting of Phanerozoic community evolution. Nature 307:5052.CrossRefGoogle Scholar
Vermeij, G. J. 1987. Evolution and escalation: an ecological history of life. Princeton University Press, Princeton, N.J. Google Scholar
Wagner, P. J. 1996. Contrasting the underlying patterns of active trends in morphologic evolution. Evolution 50:9901007.Google Scholar
Wang, S. C. 2001. Quantifying passive and driven large-scale evolutionary trends. Evolution 55:849858.Google Scholar
Wcislo, W. T., and Danforth, B. N. 1997. Secondarily solitary: the evolutionary loss of social behavior. Trends in Ecology and Evolution 12:468474.Google Scholar
Wimsatt, W. C. 1974. Complexity and organization. Pp 6786 in Schaffner, K. F. and Cohen, R. S., eds. Biennial Meeting of the Philosophy of Science Association. Reidel, Dordrecht.Google Scholar
Wimsatt, W. C. 1994. The ontology of complex systems: levels of organization, perspectives, and causal thickets. Canadian Journal of Philosophy 20:S207S274.Google Scholar
Wolk, C. P. 1996. Heterocyst formation. Annual Review of Genetics 30:5978.Google Scholar
Wright, S. 1967. Comments on the preliminary working papers of Eden and Waddington. Pp. 117120 in Moorehead, P. S. and Kaplan, M. M., eds. Mathematical challenges to the Neo-Darwinian interpretation of evolution. Wistar Institutional Press, Philadelphia.Google Scholar
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