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1 September 2006 Evolvability, Plausibility, and Possibility
ALAN C. LOVE
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Resolving Darwin's Dilemma. Marc W. Kirschner and John C. Gerhart. Yale University Press, New Haven, CT, 2005. 314 pp., illus. $30.00 (ISBN 0300108656 cloth).

Judgments of plausibility involve appearance of the truth or reasonableness, which is always a function of background knowledge. What anyone will countenance is conditioned by what they already know (or think they know). Marc Kirschner (professor of systems biology at Harvard) and John Gerhart (professor of molecular and cell biology at the University of California–Berkeley) aim to show that molecular, cellular, and developmental processes relevant to the generation of phenotypic variation in anatomy, physiology, and behavior demonstrate how evolutionary processes, especially the origins of novelty, are plausible. The outstanding question for Kirschner and Gerhart concerns not the modification of structures but their origination—a question unanswered by the theoretical framework of the modern synthesis.

Two different audiences are in view: scientific researchers interested in the structure of evolutionary theory and the skeptical (but open-minded) public attuned to controversies over the adequacy of evolutionary theory. Kirschner and Gerhart adopt a mediating tactic between these audiences by keeping technical jargon to a minimum (and supplying a useful glossary) while locating their commitments within the broad space of alternatives seen in the history of evolutionary theorizing. The backbone of their argument is that the plausibility of evolution is conditioned by the possibilities of phenotypic variation available to natural selection. These possibilities of variation are underwritten by a set of conserved core processes that contribute to the increasing evolvability of life on this planet. The book is tightly argued and highly readable despite a wealth of biological detail (all effectively chosen and succinctly presented with illustrations). It synthesizes contemporary research and expands on the authors' earlier joint publications emphasizing the significance of molecular and cellular development for comprehending evolutionary dynamics.

That plausibility increases with a widening of the space of possibilities relates directly to complaints about the inability of evolutionary theory to explain the origins of novelty. If there are many ways to generate variation in components relevant to eyes, for example, then the plausibility of selection seizing on those variations to cumulatively produce varieties of complex optical structures is enhanced. In the background are three necessary conditions for the operation of natural selection—variation, fitness differences, and heritability—each uncontroversially present in nature. Variation is observed for most phenotypic features to which fitness differences readily attach. Heritability usually comes via genetic material, which presumes a connection with phenotypic variation through random genetic mutation. The missing link concerns how genetic variation translates into phenotypic variation via ontogeny. This is where the authors seek to fill the gap in evolutionary theory, or “resolve Darwin's dilemma,” by explaining how phenotypic variation originates. It is a gap long recognized, and recent discoveries of deep genetic similarity across taxa, with no correlation between gene number and organismal complexity, have made it more conspicuous.

The explanation offered by Kirschner and Gerhart is “facilitated (phenotypic) variation.” Although facilitated genetic variation (whereby mutation is biased to be viable, to give functional outcomes, and to be relevant to ecology) is not empirically supported, random genetic variation can lead to biased phenotypic variation as a consequence of the properties of core cellular processes (e.g., transcription) operating during development. These properties include weak regulatory linkage (easily modified connections among components), exploratory behavior (developmental selection), and compartmentation (localization of components or activities). The processes are highly conserved by selection because they confer robustness, flexibility, and versatility on ontogeny but make possible a multitude of phenotypic variations through recombination during development at different times and places, and in differing amounts. These regulatory capacities are manifested in the organism's ability to physiologically adapt within each generation as well as in developmental plasticity (e.g., insect polyphenisms). Thus, phenotypic variation will tend to be viable, to give functional outcomes, and to increase genetic diversity, which means that selective processes will be facilitated to produce evolutionary change. On a larger scale, the history of life is punctuated by the emergence and stabilization of new core processes (e.g., multicellularity) followed by the exploration of new possibilities emerging from the consequent facilitated phenotypic variation.

How well does facilitated variation address the plausibility concerns of those outside the scientific community? The answer is mixed. Because plausibility rests on background knowledge, and facilitated variation relies on much of existing evolutionary theory (it is technically a completion of existing natural selection theory, not a genuinely new evolutionary theory), its persuasiveness will be conditioned by the degree to which these other ideas are assimilated (arguably a major part of the problem in the first place). And yet it is clear that the origins of novelty have been a consistent irritant surrounding the adequacy of evolutionary theory. Therefore this book successfully broadens the space of possibilities through appeal to how actual molecular, cellular, and developmental processes produce phenotypic variation. Exploratory behavior in the formation of the vascular and nervous systems goes a long way toward addressing how multiple changes occur simultaneously during the origins of novelty. It is also a reminder that organismal “parts” are multifunctional and therefore disanalogous in many ways to the parts of artifacts such as watches.

How well does facilitated variation address plausibility concerns among scientists? The answer here too is mixed. Whereas those not specifically working in evolutionary biology are likely to find that facilitated variation augments the plausibility of evolutionary transformations, many researchers intimately associated with standard evolutionary theory will not be so easily moved. For example, some population biologists welcome findings from molecular developmental biology but have already begun arguing that these results do not warrant revamping evolutionary theory. This highlights diversity in the background knowledge of biological researchers, which is due to differing areas of expertise. The plausibility of a particular conception of evolutionary theory has often been directly connected to the methods favored by those offering the conception. Background knowledge is not equally distributed among biologists, and this affects plausibility judgments pertinent to evolutionary theory and the acceptance of the empirical results canvassed by Kirschner and Gerhart.

Although I am sympathetic to the argument that facilitated variation confers a higher plausibility on both the pattern and the process of evolutionary change, this argument has another, less conspicuous consequence. The possibilities of phenotypic variation that increase the plausibility of the origin of novelty simultaneously raise issues of how to discriminate between these possibilities. We want explanations that pin causal responsibility on one or more of the plausible mechanisms, especially for historical phenomena for which we lack experimental access. Paraphrasing the 19th-century philosopher of science John Herschel, identifying “true causes” for the origin of natural phenomena requires a demonstration of their existence, capability, and responsibility. Existence and capability are fully documented in this book. Discriminating which possibility is responsible for the origin of variation relevant to particular novelties, however, goes beyond plausibility and remains part of nascent research in evolutionary developmental biology.

Several outstanding issues remain. For example, Kirschner and Gerhart indicate a commitment to reductionist methodology: “To understand novelty in evolution, we need to understand organisms down to their individual building blocks, down to the workings of their deepest components” (p. ix). But many challenges to the completeness of evolutionary theory have arisen from those holding that a hierarchical conception of evolutionary (and developmental) processes better explains life's diversity. Whether evolvability has been selected for is also contentious, and hierarchy emerges here as well, because the authors'rationale includes selection at multiple levels (individual, population, group, clade). Other slippery notions permeating the text are “complexity” and “novelty,” which can have different meanings for biological researchers, as well as for the public. This affects the authors' interpretation of empirical cases, such as the evolution of direct development in echinoids. But the judicious temperament and comprehensive nature of Kirschner and Gerhart's presentation of facilitated variation should serve not only as a plank in the case for the general plausibility of evolutionary processes but also as a key point of departure for exploring evolutionary possibilities more thoroughly, including the nature of evolvability.

ALAN C. LOVE "Evolvability, Plausibility, and Possibility," BioScience 56(9), 772-774, (1 September 2006). https://doi.org/10.1641/0006-3568(2006)56[772:EPAP]2.0.CO;2
Published: 1 September 2006
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