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Key innovations, convergence, and success: macroevolutionary lessons from plant phylogeny

Published online by Cambridge University Press:  08 April 2016

Michael J. Donoghue
Michael J. Donoghue*
Affiliation:
Department of Ecology and Evolutionary Biology and Peabody Museum of Natural History, Yale University, New Haven, Connecticut 06520. E-mail: michael.donoghue@yale.edu
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Abstract

Improvements in our understanding of green plant phylogeny are casting new light on the connection between character evolution and diversification. The repeated discovery of paraphyly has helped disentangle what once appeared to be phylogenetically coincident character changes, but this has also highlighted the existence of sequences of character change, no one element of which can cleanly be identified as the “key innovation” responsible for shifting diversification rate. In effect, the cause becomes distributed across a nested series of nodes in the tree. Many of the most conspicuous plant “innovations” (such as macrophyllous leaves) are underlain by earlier, more subtle shifts in development (such as overtopping growth), which appear to have enabled the exploration of a greater range of morphological designs. Often it appears that these underlying changes have been brought about at the level of cell interactions within meristems, highlighting the need for developmental models and experiments focused at this level. The standard practice of attempting to identify correlations between recurrent character change (such as the tree growth habit) and clade diversity is complicated by the observation that the “same” trait may be constructed quite differently in different lineages (e.g., different forms of cambial activity), with some solutions imposing more architectural limitations than others. These thoughts highlight the need for a more nuanced view, which has implications for comparative methods. They also bear on issues central to Stephen Jay Gould's vision of macroevolution, including exaptation and evolutionary recurrence in relation to constraint and the repeatability of evolution.

Type
Generating Diversity
Information
Paleobiology , Volume 31 , Issue S2 , 2005 , pp. 77 - 93
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Andrews, H. N. 1948. Fossil tree ferns of Idaho. Archaeology 1:190–195.Google Scholar
Andrews, H. N., and Murdy, W. H. 1958. Lepidophloios and ontogeny in arborescent lycopods. American Journal of Botany 45:552–560.Google Scholar
Bateman, R. M. 1994. Evolutionary-developmental change in the growth architecture of fossil rhizomorphic lycopsids: scenarios constructed on cladistic foundations. Biological Reviews of the Cambridge Philosophical Society 69:527–597.CrossRefGoogle Scholar
Bateman, R. M., DiMichele, W. A., and Willard, D. A. 1992. Experimental cladistic analyses of anatomically preserved arborescent lycopsids from the Carboniferous of Euramerica: an essay in paleobotanical phylogenetics. Annals of the Missouri Botanical Garden 79:500–559.Google Scholar
Bateman, R. M., Crane, P. R., DiMichele, W. A., Kenrick, P. R., Rowe, N. P., Speck, T., and Stein, W. E. 1998. Early evolution of land plants: phylogeny, physiology and ecology of the primary terrestrial radiation. Annual Review of Ecology and Systematics 29:263–292.Google Scholar
Baum, D. A., and Donoghue, M. J. 2002. Transference of function, heterotopy, and the evolution of plant development. Pp. 52–69in Cronk, Q., Bateman, R., and Hawkins, J., eds. Developmental genetics and plant evolution. Taylor and Francis, London.Google Scholar
Boyce, C. K., and Knoll, A. H. 2002. Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28:70–100.Google Scholar
Chapman, R. L., Buchheim, M. L., Delwiche, C. F., Friedl, T., Huss, V. A. R., Karol, K. G., Lewis, L. A., Manhart, J., McCourt, R. M., Olsen, J. L., and Waters, D. A. 1998. Molecular systematics of green algae. Pp. 508–540in Soltis, D., Soltis, P., and Doyle, J., eds. Systematics of plants II. Kluwer Academic, New York.Google Scholar
Chase, M. W., Soltis, D. E., Soltis, P. S., Rudall, P. J., Fay, M. F., Hahn, W. J., Sullivan, S., Joseph, J., Molvray, M., Kores, P. J., Givnish, T. J., Sytsma, K. J., and Pires, J. C. 2000. Higher-level systematics of the monocotyledons: an assessment of current knowledge and a new classification. Pp. 3–16in Wilson, K. and Morrison, D., eds. Monocots: systematics and evolution. CSIRO Publishing, Collingwood, Victoria, Australia.Google Scholar
Cichan, M. A. 1986. Conductance of the wood of selected Carboniferous plants. Paleobiology 12:302–310.Google Scholar
Cichan, M. A., and Taylor, T. N. 1990. Evolution of cambium in geological time—a reappraisal. Pp. 213–228in Iqbal, M., ed. The vascular cambium. Wiley, Somerset, U.K.Google Scholar
Coddington, J. A. 1994. The role of homology and convergence in studies of adaptation. Pp. 53–78in Eggleton, P. and Vane-Wright, R., eds. Phylogenetics and ecology. Academic Press, London.Google Scholar
Morris, S. Conway 1998. The crucible of creation. Oxford University Press, Oxford.Google Scholar
Morris, S. Conway 2003. Life's solution: inevitable humans in a lonely universe. Cambridge University Press, Cambridge.Google Scholar
Morris, S. Conway, and Gould, S. J. 1998. Showdown on the Burgess shale. [The Challenge by Conway Morris and the Reply by S. J. Gould.]. Natural History 107:48–55.Google Scholar
Cracraft, J., and Donoghue, M. J., eds. 2004. Assembling the tree of life. Oxford University Press, New York.Google Scholar
Delwiche, C. F., Anderson, R. A., Bhattacharya, D., Mishler, B. D., and McCourt, R. M. 2004. Algal evolution and the early radiation of green plants. Pp. 121–137in Cracraft, and Donoghue, , 2004.Google Scholar
de Queiroz, A. 2002. Contingent predictability in evolution: key traits and diversification. Systematic Biology 51:917–929.Google Scholar
Des Marais, D. L., Smith, A. R., Britton, D. M., and Pryer, K. M. 2003. Phylogenetic relationships and evolution of extant horsetails, Equisetum, based on chloroplast DNA sequence data (rbcL and trnL-F). International Journal of Plant Sciences 164:737–751.CrossRefGoogle Scholar
DiMichele, W. A., and Phillips, T. L. 1985. Arborescent lycopod reproduction and paleoecology in a coal-swamp environment of Late Middle Pennsylvanian age (Herrin Coal, Illinois, USA). Review of Paleobotany and Palynology 44:1–26.Google Scholar
Donoghue, M. J. 1989. Phylogenies and the analysis of evolutionary sequences, with examples from seed plants. Evolution 43:1137–1156.CrossRefGoogle ScholarPubMed
Donoghue, M. J. 1992. Homology. Pp. 170–179in Keller, E. and Lloyd, E., eds. Keywords in evolutionary biology. Harvard University Press, Cambridge.Google Scholar
Donoghue, M. J. 2002. Plants. Pp. 911–918in Pagel, M., ed. Encyclopedia of evolution, Vol. 2. Oxford University Press, Oxford.Google Scholar
Donoghue, M. J. 2004. Immeasurable progress on the Tree of Life. Pp. 548–552in Cracraft, and Donoghue, , 2004.Google Scholar
Donoghue, M. J., and Doyle, J. A. 2000. Demise of the anthophyte hypothesis? Current Biology 10:R106–R109.Google Scholar
Donoghue, M. J., and Ree, R. H. 2000. Homoplasy and developmental constraint: a model and an example from plants. American Zoologist 40:759–769.Google Scholar
Donoghue, M. J., Bell, C. D., and Winkworth, R. C. 2003. The evolution of reproductive characters in Dipsacales. International Journal of Plant Sciences 164:S453–S464.CrossRefGoogle Scholar
Doyle, J. A. 1998. Phylogeny of the vascular plants. Annual Review of Ecology and Systematics 29:567–599.Google Scholar
Doyle, J. A., and Donoghue, M. J. 1986. Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Botanical Review 52:321–431.Google Scholar
Eggert, D. A. 1961. The ontogeny of Carboniferous arborescent Lycopsida. Palaeontographica Abteilung B 108B:43–92.Google Scholar
Eggert, D. A. 1962. The ontogeny of Carboniferous arborescent Sphenopsida. Palaeontographica 110B:99–127.Google Scholar
Eggert, D. A. 1972. Petrified Stigmaria of sigillarian origin from North America. Review of Paleobotany and Palynology 14:85–99.Google Scholar
Eggert, D. A., and Kanemoto, N. Y. 1977. Stem phloem of Middle Pennsylvanian Lepidodendron. Botanical Gazette 138:102–111.Google Scholar
Feild, T. S., Arens, N. C., Doyle, J. A., Dawson, T. E., and Donoghue, M. J. 2004. Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30:82–107.Google Scholar
Geeta, R. 2003. Variation and diversification in plant evo-devo [book review]. American Journal of Botany 90:1257–1261.CrossRefGoogle Scholar
Gifford, E. M., and Foster, A. S. 1989. Morphology and evolution of vascular plants, 3d ed.W. H. Freeman, New York.Google Scholar
Givnish, T. J. 1997. Adaptive radiation and molecular systematics: issues and approaches. Pp. 1–54in Givnish, T. and Sytsma, K., eds. 1997. Molecular evolution and adaptive radiation. Cambridge University Press, Cambridge.Google Scholar
Gould, S. J. 1989. Wonderful life: the Burgess shale and the nature of history. Norton, New York.Google Scholar
Gould, S. J. 2002. The structure of evolutionary theory. Harvard University Press, Cambridge.Google Scholar
Gould, S. J., and Vrba, E. S. 1982. Exaptation—a missing term in the science of form. Paleobiology 8:4–15.Google Scholar
Graham, L. E. 1993. Origin of the land plants. Wiley, New York.Google Scholar
Heilbuth, J. C. 2000. Lower species richness in dioecious clades. American Naturalist 156:221–241.CrossRefGoogle ScholarPubMed
Hunter, J. P. 1998. Key innovations and the ecology of macroevolution. Trends in Ecology and Evolution 13:31–36.CrossRefGoogle ScholarPubMed
Judd, W. S., Campbell, C. S., Kellogg, E. A., Stevens, P. F., and Donoghue, M. J. 2002. Plant systematics: a phylogenetic approach, 2d ed.Sinauer, Sunderland, Mass.Google Scholar
Karol, K. G., McCourt, R. M., Cimino, M. T., and Delwiche, C. F. 2001. The closest living relatives of land plants. Science 294:2351–2353.Google Scholar
Kenrick, P. 2000. The relationships of vascular plants. Philosophical Transactions of the Royal Society of London B 355:847–855.Google Scholar
Kenrick, P, and Crane, P. R. 1997. The origin and early diversification of land plants: a cladistic study. Smithsonian Institution Press, Washington, D.C.Google Scholar
Knoll, A. H., Grant, S. W. F., and Tsao, J. W. 1986. The early evolution of land plants. In Broadhead, T., ed. Land plants: notes for a short course. Studies in Geology 15:45–63. Department of Geology, University of Tennessee, Knoxville.Google Scholar
Lankester, E. R. 1870. On the use of the term homology in modern zoology, and the distinction between homogenetic and homoplastic agreements. Annals of the Magazine of Natural History, 4th series, 6:34–43.Google Scholar
Mishler, B. D., and Churchill, S. P. 1985. Transition to a land flora: phylogenetic relationships of the green algae and bryophytes. Cladistics 1:305–328.Google Scholar
Moore, B. R., Chan, K. M. A., and Donoghue, M. J. 2004. Detecting diversification rate variation in supertrees. Pp. 487–533in Bininda-Emonds, O., ed. Phylogenetic supertrees: combining information to reveal the tree of life. Kluwer Academic, New York.Google Scholar
Nickrent, D., Parkinson, C. L., Palmer, J. D., and Duff, R. J. 2000. Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Molecular Biology and Evolution 17:1885–1895.CrossRefGoogle ScholarPubMed
Niklas, K. J. 1997. The evolutionary biology of plants. University of Chicago Press, Chicago.Google Scholar
O'Hara, R. J. 1992. Telling the tree: narrative representation and the study of evolutionary history. Biology and Philosophy 7:135–160.Google Scholar
Osborn, H. F. 1905. The ideas and terms of modern philosophical anatomy. Science 21:959–961.Google Scholar
Patterson, C. 1982. Morphological characters and homology. Pp. 21–74in Joysey, K. and Friday, A., eds. Problems of phylogenetic reconstruction. Academic Press, London.Google Scholar
Phillips, T. L., and DiMichele, W. A. 1992. Comparative ecology and life-history biology of arborescent lycopsids in Late Carboniferous swamps of Euramerica. Annals of the Missouri Botanical Garden 79:560–588.Google Scholar
Pryer, K. M., Schneider, H., and Magallón, S. 2004. The radiation of vascular plants. Pp. 138–153in Cracraft, and Donoghue, , 2004.Google Scholar
Remy, W., Gensel, P. G., and Hass, H. 1993. The gametophyte generation of some early Devonian land plants. International Journal of Plant Sciences 154:35–58.CrossRefGoogle Scholar
Renzaglia, K. S., Duff, R. J., Nickrent, D. L., and Garbary, D. J. 2000. Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Philosophical Transactions of the Royal Society of London B 355:768–793.Google Scholar
Rudall, P. J. 1991. Lateral meristems and stem thickening growth in monocotyledons. Botanical Review 57:150–161.Google Scholar
Sanderson, M. J. 1998. Reappraising adaptive radiation. American Journal of Botany 85:1650–1655.Google Scholar
Sanderson, M. J., and Donoghue, M. J. 1989. Patterns of variation in levels of homoplasy. Evolution 43:1781–1795.Google Scholar
Sanderson, M. J., and Donoghue, M. J. 1996. The relationship between homoplasy and confidence in a phylogenetic tree. Pp. 67–89in Sanderson, M. and Hufford, L., eds. Homoplasy and the evolutionary process. Academic Press, San Diego.Google Scholar
Sattler, R. 1984. Homology—a continuing challenge. Systematic Botany 9:382–394.Google Scholar
Sattler, R. 1991. Process homology: structural dynamics in development and evolution. Canadian Journal of Botany 70:708–714.Google Scholar
Schneider, H., Pryer, K. M., Cranfill, R., Smith, A. R., and Wolf, P. G. 2002. Evolution of vascular plant body plans: a phylogenetic perspective. Pp. 330–363in Cronk, Q., Bateman, R., and Hawkins, J., eds. Developmental genetics and plant evolution. Taylor and Francis, London.Google Scholar
Soltis, P. S., Soltis, D. E., Chase, M. W., Endress, P. K., and Crane, P. R. 2004. The diversification of flowering plants. Pp. 154–167in Cracraft, and Donoghue, , 2004.Google Scholar
Stewart, W. N., and Rothwell, G. W. 1993. Paleobotany and the evolution of plants, 2d ed.Cambridge University Press, New York.Google Scholar
Tomlinson, P. B. 1995. Non-homology of vascular organization in monocotyledons and dicotyledons. Pp. 589–622in Rudall, P., Cribb, P., Cutler, D., and Humphries, C., eds. Monocotyledons: systematics and evolution, Vol. II. Royal Botanic Gardens, Kew, U.K.Google Scholar
Tomlinson, P. B., and Zimmermann, M. H. 1969. Vascular anatomy of monocotyledons with secondary growth—an introduction. Journal of the Arnold Arboretum 50:159–179.Google Scholar
Vamosi, J. C., Otto, S. P., and Barrett, S. C. H. 2003. Phylogenetic analysis of the ecological correlates of dioecy in angiosperms. Journal of Evolutionary Biology 16:1006–1018.Google Scholar
Zanis, M. J., Soltis, D. E., Solits, P. S., Mathews, S., and Donoghue, M. J. 2002. The root of the angiosperms revisited. Proceedings of the National Academy of Sciences USA 99:6848–6853.Google Scholar
Zimmermann, W. 1965. Die Telomtheorie. Fischer, Stuttgart.Google Scholar