Biological theory, like all theory in science, is an attempt to order the diversity of facts of the world. But the history of science consistently shows that the same "facts" can be interpreted in various ways and that what is chosen or accepted as fact is often culturally rather than, or as well as, objectively determined. An excellent and in some senses founding treatment of this now commonplace idea was presented by the Polish physician Ludwik Fleck (Fleck 1979), in the context of the way that the history of Western culture affected the drive to understand the causal nature of syphilis (Weiss 2003). That science is in part a product of its history and cultural context often means that alternative interpretations that we have not thought of or have minimalized or rejected might be of comparable utility. Better explanations might be rejected or not even considered because of such factors. It is interesting to consider some of the prevailing notions in evolutionary biology and how they may reflect the culture in which that theory developed.
In the 17th century, René Descartes promulgated the view that organisms were machines and could be understood in mechanical terms. Professional biology developed during the flowering of the industrial or machine age of the 19 th century. Many important biological advances, particularly in genetics, occurred during the computer or information age of the 20th century; today, the prevailing view is that an organism is not just a machine but is the computable product of the information stored in its inherited DNA.
The machine analogy is in a curious way related to the 19th century's Lamarckian view of evolution. A machine is teleologically designed. It works because its parts are individually and independently manufactured in advance to serve a particular function. It is assembled from the outside and can be repaired part by part. Modifications can be introduced in various ways, some by chance perhaps, by purposive testing and experimenting with some objective in mind. Overall, the important characteristics of a machine are that it is prospectively and purposively designed and manufactured.
However, the same biology that views organisms in this way unambiguously denies that organisms have come about through teleological, lamarckian processes. Instead, an organism is the product of contingent processes, not de novo design. An organism develops from the inside, rather than being assembled by an external factory, and it evolved by modifications of that process, which works on the whole organism and not part by part and without any end objective in mind.We know that organisms are a patchwork of messy construction, yet we persist in analyzing them as if they can be decomposed part by part.
In a similar way, the computer age has led us to view genes as the sole blueprint for an organism, as if it were a simple storehouse of digital information for the assembly of an organism, a computer program for an organism. This metaphor has many problems (Kay 2000; Lewontin 2000). A program is modified not by overall natural selection but by debuggers that look for syntax errors and logical errors relative to the preconceived function and built-in syntax rules. Programs might be very different if all that we require of them is that they do something, as opposed to this thing. Selection works on organisms, not DNA, and we know that much of the DNA in this world is affected at most only weakly by selection (selectively neutral DNA; see Chapter 3). Nonetheless, much of modern biology is dedicated to the treatment of organisms as if they can be decomposed—and, for genetic engineers, repaired— gene by gene, just as we can execute a computer program step by step.
Of course, at some levels of approximation and for carefully chosen purposes, machine and information analogies work very well. Recently, however, we are learning that in important ways these analogies are frustrating at best and can be seriously misleading, and examples of these will be presented. Descartes did say that the body was a machine driven by the spirit.
natural Selection: Cooperation as Well as Competition
Another element of the cultural context of the development of modern biology relates to ideas about the role of competition in evolution. We are not the first to observe that the formalized justification of competition is a core aspect of the industrial age in which evolutionary biology developed. It is often argued that were
Darwin not a wealthy industrialist in the world's Imperial power, he would not have produced his theory and it would not have been embraced by others. Nonetheless, for whatever reasons, although they differed in details, competition for scarce resources was central to the formulation of evolutionary ideas by both Darwin and Wallace. To both, the requisite force was the culling back of Malthusian overproduction by an environment that favors those more "fit" for their circumstances. In the 20th century, it came to be widely believed this was to be explained not in terms of competition among individuals but by reduction all the way to a gene's eye view, in which the fundamental molecules of life—genes—are seen as "selfish", self-perpetuating units relentlessly trying to outdo each other and exploit each other for their own ends (e.g., see Hurst et al. 1996), most widely known through the uncompromising popularizations of this view by Richard Dawkins (Dawkins 1981).
We do not have to be stopped by the obvious fact that selfishness is a very human concept with many culture-specific nuances to agree that there is competition in nature and that those not fit to survive that competition are unlikely to do so. This was a natural way to view the world in the heady and dominant days of the British Empire and the competition and class hierarchies associated with industrialization and the growing organizational hierarchy of large, urbanizing societies. Selection does not screen on genes directly; however, it is true that over time some genetic variants become more common than others, thus winning a competition. But the historiographic explanation of evolutionary theory is weakened by the fact that Wallace was not a wealthy or socially conservative industrialist. Nonetheless it is fair to ask whether cultural circumstances affect how nature's observers interpret what they see; there are other ways to view the processes by which species might evolve. Competition is not all that occurs in nature.
As far as we know, life originated in some chemical mix in which the original organized molecules—whatever they were—increased by incorporating nearby molecules. Although initially life forms could have lived strictly by incorporating materials that were not previously involved in life or the decayed detritus of former life, the supply of such material would eventually have been exhausted. An important change occurred, in which living material depended on incorporating materials from other living organisms: the dawn of predation.
Obtaining nutrients from other living forms obviously became a successful way to do business and thus proliferated. It is easy to see how such a source of nutrition could be favorable, as the prey has been made to do the work of preparing the molecules needed by the predator (e.g., by making protein, carbohydrates, sugars, etc.). Consequently, a corresponding path to success emerged in the form of the ability to avoid being incorporated by another organism. Thomas Hobbes' war of all against all was on! Much of the structure of individual organisms and of ecosystems throughout the biosphere reflects billions of years of this arms race.
Recycling of dead matter by plants and many animals and, even better, capturing it in the form of living prey are major results of this history. Anyone reflecting on a meadow, forest, or pond (or on his own dinner plate) can see the importance and pervasiveness of this kind of interspecific competition. Systematic pressures of predatory or other limiting aspects of the environment can lead to increased organizational structure among living forms over time, and that is what Darwin and Wallace realized. It is easy to see how predation and other forms of competi tion that eliminate the sluggish could systematically produce organized traits in organisms if and when the traits of winner or loser are heritable. But this is not the whole story.
If we look at descendants over time, we can view those that increased in relative number as having acted in a way that served selfishly competitive ends. The notion of competition transformed scientific thinking by adding a dynamic process to a static worldview driven by religious dogma. However, much can also be learned by viewing things in terms of cooperation. Competition and cooperation are often viewed as antithetical, but biological processes almost by definition involve the interaction among molecules or other components of life. Success in life often depends on successful interactions. A purely selfish gene cannot even replicate itself. One can translate many of the phenomena now viewed in competitive terms into terms of cooperation (of course, as with competition, the entities need not be aware of what they are doing). A gene that gets along with others in its community— of molecules, cells, organisms, or even species—may have a better chance of succeeding. "Better chance" may be viewed as competition but "gets along" is just as necessary.
Within an organism, cells of different types are produced by a tree of descent from a common ancestral cell (the fertilized egg). These different cells perform vital complementary functions in very intricate ways. Without these functions, the organism perishes. Cooperation has been a basic strategy for building larger, complex organisms, as many chapters to follow will illustrate. Cells communicate with each other so that each differentiates in a way that is good for the organism. There is cooperative housekeeping, as nutrients and oxygen are delivered to all cells. Some cells protect other cells from damage by pathogens. Some communicate behavioral instructions from a central nervous system. At many stages in animal development, in the process known as apoptosis, cells self-destruct to make way, so to speak, for other cells. Animals require energy fixed by plants to survive. In plants, cells in roots deliver water to leaves.
Sexual reproduction has been viewed as fundamentally competitive at least since Charles Darwin wrote Descent of Man or Selection and Selection in Relation to Sex in 1871. Darwin quickly realized that competition to get or to avoid becoming food was not all there was to nature. Obtaining mates could also provide a strong selective force. Individuals of one sex choosing the "best" mate they can get or of the same sex competing with each other for access to the opposite sex, can in principle generate major phenotypic changes. This kind of competition can become exaggerated, a positive-feedback display race (Figure 2-3). Of course it is always difficult to infer after the fact whether this, or some more material type of competition, might actually have been responsible.
Beyond these kinds of organismal behavioral aspects of sexual selection, many modern darwinists peer into the intricacies of sexual reproduction to see all sorts of elements of competition—among individuals, among sperm, among fetus and mother, and so on (Hurst 1995; Hurst, Atlan et al. 1996; Parker and Partridge 1998; Partridge and Hurst 1998). Sexual reproduction has evolved many times, and the consensus reason is that this enabled species to be more diverse and responsive to changing environments, but it also has fundamental elements of cooperation. In addition, organisms from bacteria to humans manifest all sorts of cooperation,
including altruism and special dependency relationships such as that between plants and their pollinators, bees and their queen, or even bacterial cells and each other.
What is real here? A historiographic analysis can suggest that today, in the intensely competitive world of industrialized science, we view life through competitive lenses. If life must be viewed as competition for success in circumstances of limited resources, one would feel compelled to explain these phenomena as favor ing genes leading to this behavior at the expense of less competitive genes. We see such interpretations at every turn.
However, from another point of view, this sounds quite forced. The best way to understand life in many cases is to view these phenomena in terms of their driving force—the cooperation that they are. Like Janus, the Roman god of change from past to future who has two faces, we should not ignore one view at the expense of the other, because that may blind us to understanding. How far we can take this is probably a matter of judgment and the viability of our interpretations. As we'll see in Chapter 8, prey can be viewed as cooperating with predators (by providing them food), as the essential nature of ecosystems. That cooperation is vital is easy to see: when the body dies, its perfectly normal cells die, but not the bacteria that were in the organism at the time.
Besides organized cooperation, there is at least one other way in which adaptive evolution can occur. Nature, like Hell in the play No Exit by Jean-Paul Sartre (Sartre and Gilbert 1947), can be portrayed as trapping organisms with each other, like people in a small room, for all eternity—or like throwing one piece of meat into an Roman arena and watching the lions kill each other to get it.
This is an accurate way to think of many circumstances in which species or local populations sometimes find themselves. But it is not the only way that life is lived, and there are ways to succeed other than by direct competition to the death. In many if not most situations, environments are complex. Organisms—even plants— actively seek environments in which they can survive, where their particular skills are suitable. A major characteristic of organisms is this kind of "plasticity" or adaptability and it is thoroughly integrated into their nature (West-Eberhard 2003). This is manifest by the great diversity of species of closely related animals (plants, fish, insects, mammals, etc.) found within the same lake or forest. The organisms have found many subenvironments in which to live.
As John McPhee (McPhee 2002) said offhandedly when observing the shape of the fins of American shad fish, "One look at that tail and you know that the fish is active in the middle of the water column and not sitting around on the bottom like a bullhead catfish, whose tail is so rounded it looks like a coin." In their preferred environment, they will meet and mate with like individuals. If migration is rare, or some mating or physical barrier arises, the individuals can become sequestered enough that they can diverge and eventually produce new species.
This is organismal selection, that is, active selection of the environment by organisms rather than passive selection of organisms by the environment, a reversal of the usual darwinian notion of natural selection. Over time, variation can accumulate, leading organisms to seek ever more specialized environments or to be more reluctant to leave the current one.
This self-selection may, but need not, initially involve genetically determined aspects of the organism. Divergence among populations that leads to subsequent speciation can then be aided by genetic changes that are unrelated to environment but provide mating barriers between individuals in the new and old environments. It may only take a very few such changes to create a reproductive barrier, and that is the definition of new species (Navarro and Barton 2003; Via 2001). Somewhat similar ideas have been expressed under rubrics like sympatric speciation or the Simpson-Baldwin effect, or "organic" selection, referring to the evolutionary effects of nongenetic transmission, that can eventually be canalized genetically (e.g., Hall 1999; Schlichting and Pigliucci 1998, and see Chapter 3).Though some of these terms have connotations from earlier disputes about evolution, sometimes offered in opposition to the notion of darwinian evolution, that need not be the case.
Of course, whether organismal selection, cooperation, classical competition, or just chance provides the best account for any given case is a separate question and sometimes difficult to answer.
Phenotypic Drift: Could Complex Traits Have Evolved by Chance?
As noted earlier, Darwin hungered for an old age to the Earth because that would provide enough time for natural selection to do its work. However, in an ironic way, an old age might relieve the necessity of invoking specific and highly discriminating natural selection to hurry along the process of adaptation. If the Earth is old, slower mechanisms can lead to organismal changes.
Defenders of creationist views of life accuse biologists of saying that creatures arose by chance. According to the alternative Argument by Design, finely tuned biological structures like the eye could not plausibly arise by chance. Biologists agree with this, and they never argued that adaptation occurs by chance in the sense that their opponents suggest. Biological organization is viewed as having arisen systematically by natural selection, but without any teleology because selection feeds on genetic change arising by chance relative to the needs of organisms. Selection is systematic, but opportunistic, working only on variation that happens—by chance—to be present.
Actually, classical darwinian explanations do not have to assume that selection is persistent and systematic enough to enable a complex trait to arise gradually from nothing. Instead, the evolution of such traits is assumed to be by a stepwise rather than via a continual teleological process. A complex state like bat flight or eyes with focusing lenses evolves through a series of earlier states. Each state itself became adapted by selection relevant to conditions at each time and place, unrelated to future states or needs. The variation that selection worked on at each stage had itself arisen by chance, without regard to states or needs. Because it only works with whatever is at hand and under the local circumstances at the time, evolution is known as a contingent process.
What the local selective reasons may have been at any stage is open to debate (or, perhaps, inherently speculative). Whatever their adaptive reasons for being, the earlier states, sometimes called exaptations (Gould and Vrba 1982) became available for selection that led to the next step, ending up in their final—that is, their present—use. For example, rudimentary wings useless for flight may have been selected for their value in thermal regulation, mating display, surface-gliding on streams (e.g., Thomas et al. 2000), and so on. Darwin called these traits "incipient stages," but that implies that they were functional rudiments of the present state, which is probably not the case for the evolution of novel function.
This view is essentially deterministic in that each stage is thought to be adaptive in the usual darwinian sense. But chance not aided by selection may have played a much larger role than usually assumed. Most organisms die for no reason related to their particular genetic makeup compared with that of their peers. Think of the millions of acorns whose unlucky fate it is to fall into shade or be eaten by squirrels.
Chance effects on reproductive success will affect heritable phenotypic variation, and the traits involved will thus change randomly over time. For example, their means, variances, or other characteristics will change in ways unrelated to their environment. Organisms might become larger, greener, rounder, and the like, by chance. Such phenotypic drift has nothing to do with natural selection except to the very general extent that the phenotypic changes must be compatible with successful reproduction.
Biologists are generally comfortable with the notion that a substantial fraction of genetic variation is due to chance aspects of reproduction from generation to generation (Chapter 3). In fact, random change of selectively neutral variation in DNA sequence has replaced selection as a theoretical baseline by which evolutionary dynamics are evaluated, and it can be shown theoretically that the effects of chance can even prevail over weak selection. But evolutionary biologists have been reluctant to apply the same view to phenotypes because of our long-standing adaptationist bias.
The working title of Darwin's Origin of Species was Natural Selection (1859), and he said his purpose was to show "that there is such an unerring power at work in natural selection." Wallace felt the same. Darwin later mused in Descent of Man (1872) that if he had overstressed the role of selection it was to show that creationist explanations were not needed to account for biological diversity. Selection provided a way out of creationist explanations.
Based on what could actually be observed in nature and domesticated species, adaptation could in principle occur—as Darwin repeatedly stressed—through the accumulation of slight variations, that is, slowly, gradually, and essentially determin-
istically. Even to Darwin, weak selection was the most prevalent kind, which is why he wanted the Earth to be old enough. These are just the circumstances in which phenotypic drift will occur and perhaps predominate. The general notion has been around for some time (e.g., Gulick 1872).
The difference between phenotypic drift and slow, local stepwise selection can be so little as to be philosophical rather than testable. In fact, darwinian selection is not even so parsimonious an explanation. It requires environmental factors that are steady, persistent, durable, and sensitive enough to mold organisms systematically in some way. Stepwise models help in some senses, but the meandering course of a series of exaptations is another way in which evolution is essentially "random." A stepwise scenario becomes nearly vacuous as an explanation if we take to heart the anthropic principle. It is at least as parsimonious to view chance as the ground state of phenotypic change and to invoke selection only when we have cause.
Energetics and Evolutionary Explanations: The Not-So-Thrifty Genotype
Characteristics of our age and culture include concepts of energetics, productivity, and efficiency. The evolution of biological traits is commonly explained the way we account for successful industry, as if natural selection can detect and favor subtle differences in form or physiology if they are more energy efficient. The idea is that efficiency would be favored because it costs less metabolic energy and hence less food and less struggle to acquire it. This essentially asserts that nature, like science, favors parsimony.
Energetic efficiency may be favored in many instances, especially in selection against very inefficient mutants, but this is not the only plausible view of life. Purging inefficiency in the face of mutations, organismal imperfections, and the sloppiness of the environment might levy a higher energetic cost on organisms than simply tolerating a degree of inefficiency. Such "noise" is pervasive in nature, and it is by no means clear whether natural selection is stringent enough to detect it. What reproduces, reproduces. Contrary to widespread notions of the genotype as a "thrifty" product of a prescriptive natural selection, tolerance of inefficiency may actually be a baseline—and more important—characteristic of evolution.
It is worth bearing in mind that it is we human interpreters who determine what is "efficient." One type of locomotion may be more efficient than another in terms of ground covered per calorie, but animals cover ground for particular purposes. Does a bird or bat expend fewer calories to catch a bug than a spider? Is it a mark of reptilian inefficiency that they cannot prey on big ungulates as a lion can? Clearly, energetics alone cannot be viewed as a very useful predictive or interpretive criterion. We should invoke energetic arguments only when there is a good, specific reason for them.
Three C's of Evolution
Evolutionary change involves the three C's of chance, competition, and cooperation in a way that is sometimes inextricable or even philosophically nondiscriminable. Different explanations can be offered for the same facts. For example, chance in small populations can have the same effect on variation as selection in larger ones. Afterward or even at the time, the empirical fact of change in heritable variation over generations can be translated as the result of chance, competition, or cooperation. A genetic variant that advances an organism's prospects has to be compatible with the cooperation among molecules and cells, and sometimes organisms, to succeed. If it succeeds relative to other variants at the same gene by leaving more copies in the next generation, this can be viewed as having out-competed the other variation and as "selfish." But the same result could be due to good luck.
In Chapter 3 we will see ways in which we may sometimes be able to distinguish between chance and selection, but this is usually a statistical criterion and not a direct observation of cause. Only in limited circumstances can we make convincing inferences of selection, and these usually require us to have a clear mechanism. But even classic cases of selection purportedly directly observed in action, such as industrial melanism in the peppered moth and the evolution of beak size and shape in the Galapagos finches, are not entirely clear-cut (Weiss 2002).
These points do not just relate to the degree to which our explanations are satisfying and consistent but can affect how we design experiments, draw generalizations, assess the role of genes in biological traits, and view Darwin's entangled bank of nature, the image with which he concluded his famous book (see Chapter 17).
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