Why don’t zebras have machine guns? Adaptation, selection, and constraints in evolutionary theory

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Abstract

In an influential paper, Stephen Jay Gould and Richard Lewontin (1979) contrasted selection-driven adaptation with phylogenetic, architectural, and developmental constraints as distinct causes of phenotypic evolution. In subsequent publications Gould (e.g., 1997a,b, 2002) has elaborated this distinction into one between a narrow “Darwinian Fundamentalist” emphasis on “external functionalist” processes, and a more inclusive “pluralist” emphasis on “internal structuralist” principles. Although theoretical integration of functionalist and structuralist explanations is the ultimate aim, natural selection and internal constraints are treated as distinct causes of evolutionary change. This distinction is now routinely taken for granted in the literature in evolutionary biology. I argue that this distinction is problematic because the effects attributed to non-selective constraints are more parsimoniously explained as the ordinary effects of selection itself. Although it may still be a useful shorthand to speak of phylogenetic, architectural, and developmental constraints on phenotypic evolution, it is important to understand that such “constraints” do not constitute an alternative set of causes of evolutionary change. The result of this analysis is a clearer understanding of the relationship between adaptation, selection and constraints as explanatory concepts in evolutionary theory.

Introduction

 

I can see no limit to the amount of change, to the beauty and infinite complexity of the coadaptations between all organic beings, one with another and with their physical conditions of life, which may be effected in the long course of time by nature’s power of selection. (Darwin, 1859, p. 109)

It would be difficult to find a more optimistic expression of the power of natural selection to shape living things to any imaginable degree of biological perfection. Such claims abound in Darwin’s writings (e.g., ibid., pp. 60, 235, 489). Living things are described in such passages as being, or as becoming, exquisitely adapted both to other living things and to their physical environments. Beauty, harmony, and perfection of design are the hallmarks of life. Indeed, one of Darwin’s chief aims in the Origin was to show ‘how the innumerable species inhabiting this world have been modified, so as to acquire that perfection of structure and coadaptation which most justly excites our admiration’ (ibid., p. 3). However, he was also acutely aware that there are good reasons for expecting that living things will not be perfectly adapted, and that in many instances they will fall far short of this ideal. As he observed, ‘Natural selection will not produce absolute perfection, nor do we always meet, as far as we can judge, with this high standard under nature’ (ibid., p. 202). Darwin wrestled with the problem of reconciling ‘that perfection of structure and coadaptation’ which we so often find in nature, with the co-existence of ‘the want of absolute perfection’ (ibid., p. 472). That story constitutes a fascinating chapter in the history of evolutionary biology (Shanahan, 2004).

Despite significant advances since Darwin in our understanding of evolution, in a fundamental sense his problem remains our own. If natural selection is so powerful in forging “perfect” adaptations in some situations, why does it seem so ineffectual in others? A common response is to cite the existence of various “constraints” on natural selection. Given free rein, selection can forge that “perfection of structure” of which Darwin spoke. Constraints prevent this. Problem solved. Yet the distinction between selection and constraints is not nearly as clear as this terse response suggests. Indeed, the more closely one examines this commonly accepted distinction, the less clear it becomes. This distinction therefore deserves careful re-examination. Whereas natural selection and phylogenetic, architectural, and developmental constraints are commonly treated as distinct causes of phenotypic evolution, I will argue that this distinction is deeply problematic because the effects attributed to such constraints are more parsimoniously explained as effects of the ordinary operation of natural selection. Consequently, although it may still be a useful shorthand to refer to such “constraints” in explaining why evolution does or does not proceed in a certain way, they do not constitute an alternative set of causes of evolutionary change. The result of this analysis is a clearer account of the relationship between adaptation, selection, and constraints as explanatory concepts in evolutionary theory.

Because this conclusion runs contrary to some widely assumed views in evolutionary biology, in order to provide a convincing case for it I need to approach the relevant issues carefully and systematically. After reviewing the pertinent details of an influential critique of “the adaptationist programme” (Section 2), I clarify the relationship between “adaptation”, “adaptiveness”, and “selection” (Section 3), provide a brief, non-exhaustive taxonomy of types of “constraints” (Section 4), critically examine the purported distinction between phylogenetic, architectural, and developmental constraints, and natural selection (Section 5), and then consider objections to my thesis that this distinction is deeply problematic (Section 6). In a concluding section (Section 7) I address the question posed in the title of this paper in light of the foregoing analysis, and identify what I take to be the philosophical significance of this analysis for an understanding of natural science.

Section snippets

Against the “adaptationist programme”

 

The paper demonstration that such and such a character was or might be adaptive was regarded by many writers as sufficient proof that it must owe its existence to Natural Selection … Paley redivivus, one might say, but philosophically upside down, with Natural Selection instead of a Divine Artificer as the Deus ex machina. (Huxley, 1942, p. 23)

Julian Huxley was referring to the degenerate state of Darwinism in the late nineteenth century, but according to more recent critics of “adaptationism”

Adaptiveness, adaptation, and selection

 

[Discovering] the use of each trifling detail of structure is far from a barren search to those who believe in Natural Selection. (Darwin, 1862, pp. 351–352).

Begin with a fundamental and widely agreed-upon distinction. A phenotypic characteristic is adaptive for an organism if it confers a fitness benefit on its possessor by giving it some advantage in relation to survival and/or reproduction. How the organism came to possess that characteristic is irrelevant for its status as adaptive.

Constraints

Organisms must be analyzed as integrated wholes, with Baupläne (fundamental body plans) so constrained by phyletic heritage, pathways of development, and general architecture that the constraints themselves become more interesting and more important in delimiting pathways of change than the selective force that may mediate change when it occurs. (Gould & Lewontin, 1979, p. 581)

Although a variety of classifications of different kinds of “constraint” can be found in the vast and sometimes

Constraints vs. selection?

The persistence of [basic structural similarities across diverse species] over hundreds of millions of years is as striking as the existence of complex adaptations, and it is not explained by natural selection. (Sterelny & Griffiths, 1999, p. 227)

With this brief taxonomy of constraints in mind, we are now in a better position to consider the relationship between constraints and natural selection. Gould and Lewontin maintained that constraints arising from ‘phyletic heritage, pathways of

Objections and replies

The Selectionist Constraint Thesis for which I have been arguing runs contrary to a view expressed not only by Gould and Lewontin, but also (thanks in large part to their influential paper) by many biologists (e.g., Herrel et al., 2004, Poulin, 1997, Seghers and Magurran, 1995) who appear to assume that if some phenotypic feature cannot be explained as an adaptation, then it must be explained as the effect of one or more non-selective constraints. Consequently, by this point a number of

Conclusions: African ungulates without automatic weapons

 

The reason zebras don’t have machine guns with which to repel lion attacks is not that firing machine guns would have been less adaptive than running away; the trait didn’t evolve because it was not available as a variation on which selection could act ancestrally. (Fitelson & Sober, 1998, p. 120)

Thought-experiments are a staple of theoretical science (Brown, 1993). Asking why something is not the case often can be a useful way of understanding why the world is the way that it is, and can

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