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Grappling for Light, Stability and Reproductive Success

Michael Purugganan

The Evolutionary Biology of Plants. Karl J. Niklas. 468 pp. University of Chicago Press, 1997. $19.95.

Odilon Redon was a French symbolist artist who in the early 1900s began to execute a series of riotously colorful and decorative paintings that incorporated botanical subjects. Redon was intrigued with the evolutionary ideas of the past century, and it was through his friendship with Armand Clavaud, the curator of the botanical garden in Bordeaux, that the artist became acquainted with Darwinian evolutionary thought.

Increasingly complex Click to Enlarge Image

Redon's paintings at the turn of the 20th century, with their depiction of near-surreal flowers, were whimsical expressions of his natural sensibilities. The plants he painted straddled reality and fantasy and fulfilled his own aesthetic sensibility that art should, as he noted, portray "the logic of the visible to the service of the invisible." It may not be too fanciful to suppose that Redon coined his aesthetic aphorism with the ideas of evolutionary biology in mind. Uncovering the evolutionary logic that sculpts the visible structure of organisms and probing the invisible forces of nature that shape adaptations—these have remained major components of the current research program of today's evolutionists.

Karl Niklas's new work, a well-thought-out and elegantly written guide to the origins and causes of diversity among plant groups, allows us to grapple with the logic behind evolutionary change. Niklas weaves a discourse on evolutionary principles, illustrated with liberal examples from the plant kingdom of how evolutionary forces shape the structural innovations that characterize these organisms. In The Evolutionary Biology of Plants, we begin to understand once again why the story of plant evolution must remain central to any narrative of the history of life on earth. It was, after all, the origin of photosynthesis, assuring the large-scale conversion of light energy into biomass, that must certainly rank as one of the most pivotal events in the annals of our planet. And the conquest of the land, which plants undertook around 500 million years ago, must surely rate as one of the more momentous episodes in life's chronicles.

The plant-centered approach is certainly refreshing. Most students of biology are woefully ignorant when it comes to the trends and patterns that characterize the evolution of plant life. Although the broad brushstrokes of evolution that shape adaptations have much in common for both plants and animals, interesting biology can always be found in the significant differences in detail. Plants, for example, are largely sessile creatures and are at the mercy of changing and fickle environments that can vary day to day, and even minute to minute. Plants are literally rooted in place, and cannot run away when nature turns too hot or cold or dry or wet or just plain annoying. To deal with change, these organisms have evolved not the neuron-driven behaviors of animals, but rather plastic developmental programs that respond rapidly to environmental cues and allow them to deploy their growth in ways that maximize their chances of surviving ecological challenges.

The Evolutionary Biology of Plants covers a wide range of topics, but for the most part the book revolves around questions regarding the nature of plant adaptations. Adaptation to life on land or, as Niklas rightly points out, to life in air, presented early terrestrial plants with formidable challenges. These plant pioneers had to reproduce and thrive in a desiccating atmosphere when they departed from their ancestral aquatic waterscape, and their evolutionary trajectories led to a reorganization of their anatomies and their morphologies, and to the advent of new tissue constructions and even cellular dispositions. During the next 500 million years, diverse lineages experimented and succeeded with spectacular innovations—water- and food-conducting vascularization, the seed habit and the flower, to name a few—that permitted plants to occupy almost every conceivable ecological niche.

Niklas is fascinated with the design of these adaptations that have so successfully allowed plants to prosper. His approach is to treat plant adaptations as living engineered structures that selective forces have molded to function in the face of physical challenges. The challenges have to do with living in the physical universe, in which Adolph Fick's law determines the rate of diffusion, and ballistic principles rule the behavior of aerodynamic particles such as seeds. In this terrestrial milieu, what is the best way to conduct water? What structure would intercept light in the most efficient manner? How do you successfully disperse pollen? If selective forces engineered these structures, what evolutionary designs would be most suitable?

The treatment of plant design in physical, engineering terms has been profitably explored by Niklas and others in a series of papers over the past two decades, and has been summarized in one of his other books, Plant Biomechanics, as well as in the current work. This design-oriented approach may strike many as being overly simplistic, but at one level it does work. It works because for the most basic adaptations, the evolutionary challenges are constrained by relatively simple physical laws that remain constant in time and space, and usually result in predictable outcomes. If simple physics were all the challenges one had to deal with, then understanding the evolution of plant structures would require nothing more than a good sense of engineering design.

The beauty of this approach is that, for these very simple obstacles, one can presumably lay out a fitness landscape that associates different designs with different fitness values. In the 1930s, Sewall Wright originated the use of the adaptive landscape as an evolutionary metaphor, and the analogy has been used profitably by biologists ever since. The problem with the adaptive landscape is that it is extraordinarily difficult to a priori assess the topography in a biologically realistic fashion. Niklas's simplified approach permits us to map out the adaptive landscape with the fewest intrinsic assumptions. We can, for example, explore how patterns of plant branching may evolve if we consider only that the plant has to maximize the interception of sunlight.

The results are a series of computer-simulated adaptive walks that suggest which designs look beneficial for a plant and which are potentially unfit. Intriguingly, the structures that appear to be the most fit in these computer-generated evolutionary scenarios uncannily resemble the morphologies one finds in living or fossil plants. It appears that if the fitness problems are simple enough, the path through the fitness landscape is both evident and well trodden.

The problems arise, as Niklas points out, when a design is required to do numerous tasks simultaneously. At this point trade-offs become apparent, and design compromises are necessary to allow plants to do many things at the same time (reproduce, conduct water and intercept light, for example). This is where things begin to get interesting, since an axiom of engineering design is that the more tasks a design is supposed to fulfill, the greater the number of equally good designs one can devise. Moreover, the number of parameters one has to contend with increases dramatically, and the resulting multidimensional landscapes become unwieldy. Any analyses along these lines can bog down rapidly. Nevertheless, the simplified approach Niklas and others have pursued remains instructive, and it allows us to marvel at the logic that governs the evolution of basic structural elements in plants.

The danger lies in thinking that plants are just simple machines. They may be machines, but they are anything but simple. What happens in the intricacies faced in the real, biotic world when things become very complex very fast? The numerous subtle interactions that we know must exist surely must play a role in determining the selective forces that shape any adaptation. And there is another danger in that we may begin to lose sight of the importance of historical contingency as a factor in evolution. The vagaries of chance, as is becoming increasingly apparent, shape living things in ways that are unpredictable and may not be repeatable. If we were, to paraphrase Stephen Jay Gould, to rewind the tape of life and play it again, would we get the same plants? We do not know; the experiment has not been done. It seems probable that the basic structural motifs would probably recur, although details are apt to change. Flowers, for example, might not evolve again in this brave new world, but vascular water-conducting tissues might very likely be found in any terrestrial plant-like creature that might reemerge. There are many ways to have sex, but few easy ways to get water from point A to point B.

Niklas does not presume that these simple engineering-design considerations are the ultimate arbiter of plant adaptation, but the simplicity of it all is seductive. Furthermore, although the walks through the adaptive landscape were the most intriguing, the other parts of the book were also equally enlightening. One of the strengths of this book is that it does cover a wide array of topics, including plant anatomy, systematics, paleobotany, population biology—even molecular and developmental genetics and molecular evolution. There is a desire to be comprehensive, but this of course is difficult in such a rich field. Given that this book advances a certain way of viewing the biological world, there will be moments here and there when the reader may not agree with the ideas being propounded. Niklas writes, however, about matters worth thinking about, and those interested in the evolution of plant life, and in evolution in general, will certainly find this work insightful and well worth reading.—Michael D. Purugganan, Genetics, North Carolina State University

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