The song of the jubjub

Field: Arts and Humanities (Social Sciences)

Anthropologists might call humans the thinking beasts, but we're often creatures of herd and habit. We can suspend critical judgment and accept things as true if we hear them repeated often enough. As Captain the Bellman (Fig. 1) said in Lewis Carroll's nonsense poem The Hunting of the Snark1 when he landed his motley crew from the ship that had sailed under his direction: “Just the place for a Snark! I have said it twice: That alone should encourage the crew. Just the place for a Snark! I have said it thrice: What I tell you three times is true.” The Bellman from Hunting of the Snark. Sorry, but I can't show you an actual Snark. From a drawing by Henry Holliday, public domain. Of course there was no such thing as a snark...was there? According to the poem (assuming it makes any sense at all), if the snark is a boojum, then when you find one you disappear. And of course that's what happened. At least I think it is. Just because something is repeated doesn't make it so. It's risky to accept too casually things that are often said. Things that are said about evolutionary biology are no exception. We perceive evolution only darkly through the misty sea-spray of deep time. However, in 1858, 16 years before the snark hunt, Darwin and Wallace gave us a simple framework to clarify the interpretation of life. They argued that species arise by descent with modification, adapted to their environment by natural selection. It's a very beamish theory that's persuasively consistent with all existing data. However, consistency is not the same as truth. Moreover, it's well known that evolutionary theory sails close to the tautological wind by saying that what is here today is here because what was better yesterday persisted to be here today. Unlike Carroll's poem, evolution isn't nonsense, but there can be a lot of nonsense when it is discussed. One problem has been what some see as excess determinism, by which natural selection is repeatedly characterized as an all-seeing fine-tuning process that screens highly determinative genotypes. Those are the unmistakable marks invoked by the oft-repeated phrase “survival of the fittest.” Determinism is the belief that nothing changes in nature except as the specific causal result of prior physical changes in the state of mass or energy. But even from a materialistic viewpoint, and metaphysical objections aside, important aspects of nature seem to be inherently probabilistic. They behave in a statistical way so that a given cause leads only to a distribution of possible results. One can specify the relative probabilities of observing various states, but cannot say with certainty which will occur. The classic Mendelian example is which of her copies of a gene a parent will transmit to a given offspring. Mutations introduce new variation in genes in a way that seems entirely random relative to the functional effect that the change may have. Nobody thinks of this as immaterial, but it is often unclear whether the phenomenon simply looks probabilistic, masking a snarkishly elusive deterministic truth, or is truly probabilistic.2, 3 The result of these chance factors in life is known as genetic drift. Genetic drift is change over generations in the frequency of genetic alleles (DNA sequence variants) that occur strictly by chance. But when an allele changes frequency, how do we know that there is nothing but chance to hunt for as an explanation? Not everyone has a mimsy view of drift, because it's seen as a direct challenge to natural selection. The argument is that chance cannot construct organized biological traits, any more than a snark can arise out of the Bellman's list of its fearful characteristics. Randomly assembled traits would be nonadaptive (a very uffish concept for biology). The ultimate evolutionary truth is differential proliferation. From today's starting point, some alternative alleles will become more common tomorrow than will others. Viewed from today looking into the past, everything that is in place today was at lower frequency in the past because it had to embark on its sojourn in life as a single lonely copy of a new mutation. But differential proliferation is not the same as natural selection. Selection is a specific kind of differential proliferation. It is systematic. The concept is basically deterministic materialism, according to which everything about an organism must have at least some effect, which in turn must be screened by selection fostering whichever change is more favorable to reproduction. From this point of view, arguing otherwise verges on nonsense that only a Dodgson would believe, because at the very least there is some energy cost to maintaining each genetic alternative, and selection will hunt all but the least costly out of existence.2 It is often said that genetic drift applies only to “neutral” DNA sequence elements, which, if they exist at all, have no functional effect and while, yes, they are inherited, only the functional aspects of genomes matter when one seeks to understand adaptive evolution. But that mistakenly equates function with fitness; that is, with differential reproductive success. There is no reason other than an assumption of Darwinian fundamentalism that functional effects cannot change solely due to drift. Chance events can deprive the next generation even of beamish genes, an icon of perfection, fitness a probabilistic rather than deterministic concept. Even Adonis, an icon of perfection, had an anteclimactic end in Aphrodite's arms after being gored by a galumphing boar. And since evolution works from today forward, chance changes are not just temporary statistical ripples in the evolutionary current, but instead determine the array of possibilities available for the future. In this sense, realized fitness has a probabilistic component. Even a “good” gene can be lost by bad luck. There's no controversy about that. Indeed, fitness differences themselves can also be inherently probabilistic. A good trait may itself only confer an edge on average, not inevitably. You may run faster than your peers for genetic reasons, giving you an edge in escaping a boojum. But it may only be a probabilistic edge: if you zig rather than zag when the boojum happens to zig too, you could suddenly vanish despite your zip. While in both the popular and scientific literature there's a lot of sloppy invocation of selection as a deterministic force, there really is no controversy about this role of chance either. In seeking the snark, the ship's brave Captain seemed confused. He was using a featureless map (Fig. 2), but at least it was one they could all understand. When he cried “Steer to starboard, but keep her head larboard!” it bewildered the crew, but they apparently made it to Snarkland anyway (the Captain said so three times, after all). Even if natural selection is as force-like as is repeatedly asserted, we can liken it to a slow ocean current. It may have a speed and direction, like a force, but with probabilistic eddies, and ships can drift off course. So, like the Bellman's doubting crew, we can ask what we know about the conditions that affect the role of drift and the ways in which it may relate to highly organized function and adaptive change in nature. “A map they could all understand.” Drawing by Henry Holiday, public domain. Under some assumptions about population size and structure, it is possible to predict theoretically the probability that a selectively neutral allele, the frequency of which changes by genetic drift alone, will eventually become fixed in the population; that is, that it will replace all other existing alleles. The prediction could not be simpler: The probability of ultimate fixation equals the allele's current frequency in the population. One can also predict the probability of fixation of an allele that is favored by a specified selective intensity. It might seem that if an allele has an upward selective push it is predestined for the glory of fixation, because in each generation its bearers would contribute disproportionately to the next generation. That would be the classical Darwinian view that natural selection is a deterministic force like gravity.2 But it is wrong. The fate of newly arisen alleles depends not just on the selective wind in its sails, but also the size of the crew. If the selective push has considerably small effect relative to the population size, as it usually does in species like humans or jubjubs, chance rather than selection will dominate the allele's destiny. Some alleles with small adaptive advantage will indeed rise in frequency, but most new variants, including not just harmful alleles, but even favorable variants, will suffer the frumious fate of extinction. This seems nonsensical, and not just because it definitely is not the image of how natural selection works. In principle it means that in the real world an allele that's harmful in the fitness sense we're discussing—can increase in frequency, meaning it must be helping and isn't doing harm! Is this a snarkish concept, or what? How can something be harmful if it helps? In fact, much of evolution may have worked this way. The details and their theoretical support are given in a lively and clear way by the evolutionary biologist Michael Lynch.4, 5 The argument goes roughly like this: Among the factors that affect evolution, mutation introduces new variants, recombination occurs among existing variants, and genetic drift are all nondirectional and hence nonadaptive because they happen randomly with respect to any function they affect. Gene flow (migration or mate exchange) between populations often is like this, too. In the classical pantheon of evolutionary factors, only natural selection is held to be adaptive and hence, directional or force-like. But how substantial are these nonadaptive factors? Most traits are affected by many different genes. The more genes there are, the more places there are for mutations to arise, and the more substantial the pressure of new mutational effects on affected traits—and many of them will be harmful. The awful ones will disappear as fast as a bandersnatch's prey. But we know that most mutational effects, positive or negative, are very small. Small fitness differences in relatively small populations are, like serving a snark with greens, the recipe for the advance of slightly harmful alleles. Since our genomes are of oceanic size and our evolution has been going on for millions of years, we must harbor much of this harmful variation. That's nonadaptive evolution, but we shouldn't outgrabe over it because the same process is also what enables variation for new adaptations to arise. An important kind of mutational change is the duplication of genes or chromosomal segments. Duplicate copies introduce functional redundancy. Future mutations can then modify the function of these duplicates, leading to new functions. DNA sequence analysis clearly shows that if genomes are anything, they are the spoor of duplication events. That, in turn, means that even functional evolution can be nonadaptive because some of this enabling duplication must have been neutral or even harmful. Our snarkish concept must be true. From the extensive recent data on genome structure and variation, we can see that a great deal of what happens in the genome is not just adaptive responses to environmental challenges. Rather than consistent survival of the fittest, a more apt phrase for what is going on would be “failure of the frail,” which I'll abbreviate as FOTF.6 When something more harmful than the bowsprit getting mixed with the rudder occurs, such as mutations producing proteins that no longer interact, nature can scuttle those mutations from the population. But, unlike the classical notion of purifying selection, things are not necessarily being “purified.” FOTF need not involve selection in the classical Darwinian sense of competition among organisms for limited resources.6 And while FOTF is clearly a form of selection, it is conservative, reflecting the failure of what has been working rather than serving as a main source of new adaptations or fine tuning. One may wonder whether similar principles work at the organismal as well as the genome level. Could selection, after all, not be such a fine-tuning determinant of who gets vaporized by a boojum? Is there phenotypic as well as genetic drift? Can biological traits evolve without the aid of selection? Phenotypic drift must occur. There is direct evidence in aspects of morphological evolution.7-12 If survival of the fittest were to apply to traits in the way that is so often repeated, their underlying genetic variation would quickly be washed away, but that is manifestly not the case. Instead, we know that most traits are affected by existing variation in large numbers, sometimes hundreds, of genes.13-15 Selection generally works most clearly at the extremes of a trait distribution, be it body size, behavior, or susceptibility to disease. Snaring the outliers is FOTF, which leaves a lot of variation in the acceptably fit middle. Success takes many forms. And that variation drifting around in the population makes it possible for individuals to succeed and hence for populations to absorb considerable deleterious variation. Species like humans use exploratory and modifying behavior to set sails for the winds of the day, buffering against threatening aspects of the environment. We pursue success in social groups that send out parties in many directions, finding ways to live that are viable and avoiding those that aren't. Unlike the Bellman, whose only notion was to tinkle his bell, there typically are many ways to succeed and new environments to explore further. The existence of options weakens the intensity of selection, implying that some “nonadaptive” phenotypes will succeed. But thinking that way leads to a semantic wild snark chase. The jubjub is a desperate bird that must be avoided at all cost. It's clearly identifiable by its song, which resembles the sound of a pencil squeaking on a slate. When the Butcher proclaimed, “Tis the voice of the Jubjub!” the Beaver turned pale to the tip of its tail and fairly lost heart, and outgrabe in despair when the Butcher repeated his proclamation for the third time. Repetition can be intimidating in the real world, too. The apparent paradox that much of what seems clearly adaptive must instead be nonadaptive or even harmful is not solely the result of thinking probabilistically rather than deterministically. More importantly, it shows how, if we're not careful, we can be misled by theory, even if the theory has been repeated more than three times. That's because the paradox is an artifact of the way evolutionary theory is usually conceived mathematically, essentially as a formalization of “survival of the fittest.” Selective values are assigned to each allele relative to the best-competing allele in the population, which, mathematically, is the fittest. But to think of all but one allele as deleterious is to speak in absolutist or essentialist, if not deterministic terms. Moreover, it does not present an accurate picture of the way real life works. Since, at any given time, most alleles have only slight, if any, effects on fitness, mischaracterizing them as “deleterious” does mischief to our understanding of evolution. Even if one allele is, on average, less positive than another, it is only in terms of relative fitness that the former is deleterious or nonadaptive. That doesn't mean that bearers of the allele stagger around like bowls of quivering curds, barely making ends meet. In the real world, fitness differences in the effects of alleles are not inherent in themselves. Rather, these differences are often so slight that they literally are inestimable, heavily dependent on their ecological and population context at any given time, and surely not, as a rule, persistent or inherent. In fact, it appears that about 10% of the seriously harmful alleles known in humans are normal alleles in other species.16-18 This is not just because the context may differ between species, but also because allelic effects depend on other factors even among individuals within a species. A survival-of-the-fittest world view was inadvertently reinforced by the way Mendel's work on peas was perceived. It entrenched the idea that traits were determined by single genes, each with two states (for example, green and yellow, smooth and wrinkled). Mendel carefully chose to study traits in which that model proved effectively true, but he knew very well that not all traits behaved that way.19 Knowledgeable geneticists have stated that clearly almost from the moment Mendel was rediscovered in 1900. What we are today is not the best that nature threw up for evolutionary consideration, even if we accept that “best”is a meaningful concept. Instead, we are what worked well enough not to have been hunted out of existence. That is the sense in which FOTF is a better metaphor for evolution. Such a view removes any need to wrestle with the snarkish concept of nonadaptive adaptation. Instead, we can see the grandeur of life as the result of what worked in the physical world, if not in an inherently fanciful mathematical formulation. Because selection typically is weak and most traits are affected by many genes, fitness differences are distributed across these genes, and are thus very slight at most individual genes. That explains why finding evidence of genetic signatures of positive adaptive selection in our own geographically diverse, recently evolved species is as hard as hunting snarks with forks and hope (Fig. 3).20 “You may hunt it with forks and hope.” Drawing by Henry Holiday, public domain. Population genetics has too readily presented evolution as a winner-take-all survival of the fittest phenomenon. Evolution is far messier than any mathematical theory. Chance events are unavoidable, and there's more than one way to chase the evolutionary snark. The “best” is often so little different from much of the rest that it's misleading to think it must win out and that the rest is meaningfully inferior. Population geneticists know,of course, that their models are practical guides for understanding aspects of the evolutionary process and evaluating empirical data. The thoughts expressed here are consistent with, because they are from, that theory. But if people really know that survival of the fittest is a problematic catch-phrase, and if they don't really mean it, why do they keep saying it, as if that made it true? The conclusion that much of evolution is nonadaptive may seem highly heretical. However, it's a false controversy because the pervasive idea that anything here today must have been specifically selected for, whether that idea is repeated in textbooks or not, is a disservice to how evolution works. In a profound sense, except in the current generation that has yet to reproduce, there is no such thing as a nonadaptive trait in living species. What's here today has sailed through an adaptive history, but that does not mean that it was the best available choice at any given time, much less every given time in the past. What we can more safely say is that since at any time, in most times, there are various ways to sail life's quest successfully, the trait was not strongly selected against. This view shouldn't sound strange because, in terms of properly applied evolutionary theory, it's as sound as a bell. It is neither mystic nor fanciful but is, instead, wholly realistic. It resembles everyday experience, which, unlike the evolutionary past or snarks, is open to everyone to observe. And nothing I've said implies that selection cannot sometimes be strong or rapid in the usually conceived way. The eons of time and the generally undetectably slow nature of evolution relative to the limits of human experience and imagination make it possible for harmful or selectively neutral variation to be assembled into highly organized traits. Differential proliferation is always involved, as adaptations gently meander between what won't work and what can. Darwin need not turn uffishly in his grave about this because even FOTF alone is a kind of selection that keeps things within the range of viability. In his preface to Snark, Carroll rebuffed the “wildly possible…charge of writing nonsense” that might be made against him, by pointing (nonsensically) to the “arithmetical principles so cautiously inculcated [in the poem]…or to its noble teachings in Natural History.”1 Perhaps the arithmetical teachings of real natural history will help us navigate the semantic nonsense of the controversy over selection versus non-selection and gain a better understanding of the ways in which we may be adrift in the evolutionary sea. Readers having vocabulary difficulties can consult the appropriate dictionary: Wikipedia, Hunting of the Snark. I welcome comments on this column: kenweiss@psu.edu. Anne Buchanan and I have a blog that deals with relevant subjects, at ecodevoevo.blogspot.com. I thank Anne, Nathaniel Cannon, Jen Wagner, and John Fleagle for critically reading this manuscript. This column is written with financial assistance from funds provided to Penn State Evan Pugh professors.