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Evolution of land plant architecture: beyond the telome theory

Published online by Cambridge University Press:  08 April 2016

William E. Stein  and
James S. Boyer
William E. Stein
Affiliation:
Department of Biological Sciences, State University of New York, Binghamton, New York 13902-6000. E-mail: [email protected]
James S. Boyer
Affiliation:
Education Department, New York Botanical Garden, Bronx, New York 10458-5126. E-mail: [email protected]
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Abstract

For well over 50 years, the telome theory of Walter Zimmermann has been extremely influential in interpreting the evolutionary history of land plant architecture. Using the “telome/mesome” distinction, and the concept of universal “elementary processes” underlying the change in form in all plants, the theory was an ambitious synthesis based on the proposition that evolutionary change might be understood by a simple set of developmental or evolutionary rules. However, a major problem resides in deciding exactly how assertions of change are to span both developmental and evolutionary domains simultaneously, and, we argue, the theory critically fails testability as a scientific theory. Thus, despite continued popularity for the descriptive terms derived from the theory in evolutionary studies of early land plants, time has come to replace it with a more explicit, testable approach. Presented here is an attempt to clarify perhaps the most important issue raised by the telome theory—whether simple changes in basic developmental processes suffice to describe much of early land plant evolution. Considering the morphology of Silurian–Devonian fossil members, it is hypothesized that early land plants possessed a common set of developmental processes centered on primary growth of shoot apical meristems. Among these were (1) the capacity to monitor and act upon internal physiological status here modeled as “apex strength,” (2) a mechanism for allocation of apex strength in a context-dependent way at each point of branching, (3) a rule for context-dependent apex angle for branches, (4) a largely invariant phyllotaxis unrelated to physiological status, and (5) a simple switch for terminating primary growth, based in part on genetics. Implemented as a set of developmental rules within a simple L-system model, these aspects of primary development in plants determine a sizable range of resultant morphologies, some of which are highly reminiscent of the early fossils. Thus, some support is found, perhaps, for Zimmermann's intuition. However, traditional concepts of growth patterns in plants, including the contrast between epidogenesis and apoxogenesis, require updating. In our reformulation, developmental processes, stated as rules of developmental dynamics, together constitute what we term the plant's developmental state. Using a hypothetico-deductive format, one may hypothesize intrinsic (or genetic) developmental processes that play out as realized developmental activity in specific spatial/temporal contexts, as modified by multiple context factors. The resultant plant morphology is highly dependent on multiple and simultaneous pathway ontogenetic trajectories. Within a likely set of developmental rules reasonably inferred from plant development, some of Zimmermann's elementary processes are perhaps recognizable whereas others are not. Progressively “overtopped” morphologies are easily produced by modifying intrinsic branch allocation. However, even so, the other developmental rules have a profound effect on final architectures. Planate architectures and circination vernation, often treated as special cases by plant morphologists, are perhaps better understood in terms of recurrent or iterative developmental relationships. Much analytic work remains before a completely specified system of rules will emerge. A well-articulated relationship between ontogeny and phylogeny remains fundamentally important in assessing evolutionary change. Fossil and living plants make it abundantly clear that current evolutionary concepts involving modification of a single ontogenetic trajectory from ancestor to descendant need to be greatly expanded into consideration of the entire logical geometry of causation in development. A mechanism for testing is also required that need not wait for complete elucidation at the molecular level. The relative simplicity of plant development, combined with an outstanding fossil record of early members, offers unique opportunities along these lines.

Type
Articles
Information
Paleobiology , Volume 32 , Issue 3 , Summer 2006 , pp. 450 - 482
Copyright
Copyright © The Paleontological Society 

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