Eight Little Piggies (37 page)

3.
Channels versus one-way streets
. Whitman conceived his series of orthogenetic stages as a forced pathway—a one-way street with pigeons as the cars. He was clearly wrong in this vision, and two major errors invalidate his form of orthogenesis. First, the cars can go in either direction; Whitman’s series may carve a road into a complex landscape, but the traffic flows both ways. Pigeons can either gain or lose color. Second, I doubt that either the checkered or two-barred condition represents a primitive state for domestic pigeons. The ancestor of domestic races was a population, not an individual—and populations are variable. I suspect that the parental population included both checkered and two-barred birds within a spectrum of variation—and that the spectrum represents the ancestral condition.

But think about Whitman’s vision in a slightly modified form, and we encounter an idea that is not only valid, but also full of potential insight for correcting a major misconception and teaching a fundamental truth about evolution. Think of his one-way street as a channel instead—a favored pathway of evolutionary variation set by the inherited genetic and developmental programs of organisms.

If natural selection controlled evolution entirely, then no such limits and pathways would exist, and organisms would be like billiard balls, capable of movement in any direction and subject to any change in position induced by the pool cue of natural selection. But, to borrow an old metaphor from Francis Galton (see Essay 27 for a full explication), suppose that organisms are polyhedrons rather than billiard balls—and that they can only move by flipping from one side (on which they now rest) to an adjacent facet. They may need a push from natural selection to move at all, but internal limitations and possibilities set the direction of possible change. If inherited genetic and developmental programs build the facets of Galton’s polyhedron, then strong internal constraints upon evolutionary change must exist and Whitman’s insight is correct, so long as we convert his one-way streets into channels—that is, strong biases in the direction of variation available for evolutionary change. Moreover, Whitman probably identified the most important internal channel of all—the pathway of ontogeny, or the growth of individuals. Evolutionary change proceeds most readily in directions already established in growth—lengthening a bit here, cutting out a stage or two there, changing the relative timing of development among organs and parts.

The most serious of vernacular misconceptions views evolution as an inexorable machine, working to produce optimal adaptations as best solutions to problems posed by local environments and unconstrained by the whims and past histories of organisms. For example, I have monitored the “Ask the
Boston Globe
” science query column for years and have never seen anything but adaptationist answers to evolutionary questions. One correspondent asked, “Why do we have two breasts?” and the paper responded that the “right” number of nipples (for optimal adaptation) is one more than the usual complement of offspring, thus providing a margin of safety, but not so large a surplus to become a burden. Since human females almost always have but a single child, two become the right number of breasts by this argument rooted in natural selection. I couldn’t help but laugh when I read this conclusion. I do grasp the logic, but surely the primary channel of our anatomical design—bilateral symmetry—has some relevance to the solution. Most externalities come in twos on our bodies—eyes, nostrils, ears, arms, legs, etc.—and the reason cannot be singleton births. Isn’t this prior channel of architecture more likely to supply the primary reason for two breasts?

If the purely adaptationist vision were valid, we might gain the comfort of seeing ourselves, and all other creatures, as quintessentially “right,” at least for our local environments of natural selection. But evolution is the science of history and its influence. We come to our local environments with the baggage of eons; we are not machines newly constructed for our current realities. These historical baggages are expressed as the genetic and developmental channels that led Whitman too far. But these same channels, properly interpreted as strong biases in variation rather than one-way streets of change, would give us a much richer view of evolution as a subtle balance between constraints of history and reshapings by natural selection.

The power of these channels provides a key to understanding our bodies and our minds; we will never grasp the evolutionary contribution to our nature if we persist in the naive view that natural selection builds best solutions. We can accept the idea more readily for our bodies; hernias and lower back pain are the price we pay for walking upright with bodies evolved for quadrupedal life and not optimally redesigned. But how much of the quirkiness and limitations of our modes of thinking might also record a structure evolved during eons for other uses, and only recently adding the varied phenomena of higher consciousness and its primary tool of expression in language? Why are we so bad at so many mental operations? Why do we seem so singularly unable to grasp probability? Why do we classify by the painfully inadequate technique of dichotomy? Why can we not even conceive of infinity and eternity? Is the limit of current cosmological thinking a defect of data, or a property of mind that gives us no access to more fruitful kinds of answers?

I do not intend this list as a statement of despair about our mental midgetry. To recognize a potential limit is to think about tools of possible transcendence. Freedom, as Spinoza said, is the recognition of necessity. Let us return once again to the proper metaphor of channels and remember the finest statement in literature about emerging from ruts: “There is a tide in the affairs of men, which, taken at the flood, leads on to fortune.”

TENNYSON’S
In Memoriam
, published in 1850, was surely the most popular of Victorian poems. The good queen herself remarked to her poet laureate, following the death of her beloved husband, Prince Albert: “Next to the Bible,
In Memoriam
is my comfort.” As a paradoxical and ultimate testimony of success, many lines became so popular, so much a part of everyday speech, that their relatively recent source was forgotten and a false Shakespearian or biblical origin often assumed. Be honest now; didn’t you think that Shakespeare wrote:

(
In Memoriam
also gave us, nearly a decade before Darwin’s book, the classic metaphor for natural selection: “nature red in tooth and claw.”)

After loving and losing, the most famous misattributed line from
In Memoriam
must be:

Tennyson’s image provides an excellent epitome for that constant and unwelcome companion of intellectual life: frustration. I may be fascinated by big questions—the ultimate origin of the universe, for example—but I am not frustrated because I expect no near or immediate solution. Frustration lies just beyond the finger tip—the solution that is almost palpable, but for one little, stubborn obstacle.

Scientific frustration takes two primary forms. In the usual, empirical variety, deeply desired data lie just beyond our reach. Remember that we looked at the moon for millennia, but never knew the form of her back face (and couldn’t really develop a decent theory of origin and subsequent history without this information). So near (if we could only grab hold of the damned thing and turn it around)—and yet so far (a good quarter of a million miles). One space probe and a camera resolved this frustration of the ages.

A second species of frustration arises from logical problems, and these sometimes seem more intractable because solutions must come from inside our heads. Consider the classics, Zeno’s paradoxes, or the puzzles of our primers:

Again, the answers seem so close (after all, the arrow does move and Achilles does pass the tortoise), yet the structure of resolution eludes us.

Empirical frustrations are resolved by evidence; I don’t know that they present much of a general message beyond the obvious value of data over casuistry. Logical frustrations have more to teach us because solutions require a reorientation of mental habits (if only the minor realization that problems need not be viewed as external to their posers, and therefore “objective”: The man in the puzzling couplet is pointing to his own son).

The study of evolution is beset with frustration, most of the empirical variety (inadequacy of the fossil record, our inability to track and document enough members of a population). But the profession also features some persistent logical puzzles, most treated (and some resolved) by Darwin himself. Several take a similar form, roughly: “I can figure out why a particular feature is useful to an organism once it develops, but how could it arise in the first place?” I have treated one standard form of this puzzle in several essays—the “10 percent of a wing” problem, or how can wings evolve if tiny initial stages could confer no aerodynamic benefit? Darwin’s solution, now experimentally confirmed (see Essay 9 in
Bully for Brontosaurus
), argues that initial stages functioned in a different manner (perhaps for thermoregulation in the case of incipient wings), and were later coopted, when large enough, for their current use in flight.

A related and equally thorny problem asks why a useful evolutionary trend can begin in the first place and why one pathway is taken in a large potential field. The knee-jerk adaptationist answer—“because the evolved feature works so well (and must therefore, in some sense, have been prefavored as a solution)”—simply will not do, for current utility and historical origin are entirely separate issues. (What, in nature, works better than a wing?—and yet we all agree that benefit in flight did not initiate the trend).

Darwin also thought about this issue and proposed a solution. His argument features a trio of important properties: it is interesting, probably correct, and largely unappreciated. Darwin considered the classic case of mimicry in butterflies—the convergence of a tasty species on the pattern of a noxious form, all the better to fool predators (viceroy on monarch, for example). A potential mimic may share an environment with one hundred other butterfly species. Why converge upon one, rather than any of the ninety-nine others? And why initiate such a trend at all among so many other evolutionary possibilities? Darwin argued that the inception must reside in accident, whatever the predictable character of the trend once it starts, and whatever the resulting benefit. The mimic’s ancestor must begin with a slight and fortuitous resemblance to the species eventually copied. Such predispositions can only be chancy, for a species cannot know its complex future. A beginning “leg up” can nudge the trend into a particular path. The path itself will be carved by the deterministic force of natural selection, but the push into the path requires a bit of luck. Without an initiation in nonadaptive good fortune, the final and stunning adaptation could never evolve.

I am tempted to call this logical solution the “great seal principle,” to honor the motto of our national emblem (engraved on the flip side of a dollar bill)—
annuit coeptis
. The agent is usually construed as God and the line, following our gender-biased tradition, therefore translated as “he smiles on our beginnings.” But the Latin third-person singular is androgynous, and I prefer to think of the agent as Lady Luck—therefore, “she smiles on the initiations.”

Darwin’s argument is theoretically sound as an abstract resolution of a conceptual puzzle—one of the logical frustrations of my introduction. But have we any evidence that nature actually bows to the reason of our arguments? This issue is particularly important in evolutionary biology because we so often make the mistake of assuming that we understand the origin of a feature just because it now works so well. Consider, for example, the large set of “showy” male organs—from peacocks’ tails to deer antlers to elaborate behavioral displays in birds-of-paradise—that presumably evolved in the process identified by Darwin as “sexual selection.” In one category of sexual selection, called “female choice” by Darwin, these elaborate structures (encumbrances in any other context) develop and enlarge because females prefer the bigger or more decorated males. Female choice may explain the extensive and gaudy patterning, but why tail feathers in the first place? Why not one of a hundred alternatives—head plumes, elaborate calls, or the more common mammalian analog of old-fashioned male bullying?

Several evolutionists, in the past few years, have thought more deeply about the difference between origins and later pathways and have taken Darwin’s problem and solution more seriously. They have realized that the pathways set by female choice must often involve an important initiating component of preexisting bias in sensory and cognitive systems. Females, after all, perceive and process information in a limited number of ways based on broad features of brain and sense organs that obviously did not evolve in order to prefer showy tail feathers in some unspecified future. Relative to tail feathers, or antlers, or complex behavioral displays, these biases are components of good fortune that permit the initiation of a particular trend. Two recent studies have provided excellent evidence for the great seal principle by combining experimental data on female choice, with a documentation of preexisting sensory biases in a genealogical context that validates an evolutionary argument.

Fish tails
. When we think of the conjunction of weaponry and fishes, we usually picture a large and graceful marine species with a sword for a snout and a lovely name of classical redundancy—
Xiphias gladius
, the swordfish (
xiphias
is a Greek sword;
gladius
, a Latin counterpart, as in the gladiator who wields it in combat). But a much smaller, Central American, fresh-water relative of the guppy, also bears a sword—this time at the rear end, formed after sexual maturity, and only in males, by an elongation of rays at the base of the caudal (tail) fin.

Alexandra Basolo of the University of California at Santa Barbara performed behavioral experiments on the swordtail,
Xiphophorus helleri
, and proved that females do prefer males with longer swords, thus establishing the efficacy of female choice in maintaining and enlarging the male sword. But such information tells us very little about the origin of swords. These projections do males a world of Darwinian good, but why swords, rather than big eyeballs, funny fins, or elaborate swimming displays? Fortunately, we have enough information about the genealogy of swordtails to reconstruct a historical sequence, and to recognize an important component of preexisting female sensory bias in the evolution of swords.

The close relatives of
X. helleri
are all swordless, and we may conclude that ordinary swordless tails represent the original state of this lineage. In particular,
Xiphophorus maculatus
, the closest living relative of the swordtail, lacks a rear projection (despite its taxonomic residence in the same genus, with its etymology of “sword bearer”). Basolo therefore performed a series of ingenious and elegant experiments on the swordless
X. maculatus
.

In her basic procedure, she placed a female in the center section of an aquarium constructed with two side compartments of equal volume. She then put a single male into each of the side compartments and noted female preference by time spent in the vicinity of males, and by performance of courtship behaviors. In these particular experiments, she surgically implanted, into the tail of swordless
X. maculatus
males, swords of the same relative length and form as in
X. helleri
. In some males, the swords had the same distinctive yellow color and bold black border as in
X. helleri
; in others, the swords were transparent (and shown in behavioral experiments to be invisible to females).

Basolo placed a male with a colored tail into one side compartment and a male with an invisible tail into the other chamber. (She followed this elaborate procedure of implanting invisible tails, rather than simply using ordinary tailless males, because she needed to control for the results of surgery and the effect of a tail upon swimming and other male behaviors. If females just reacted differently to an ordinary, unoperated male, than to a male with an experimentally implanted tail, we would not know whether this disparity recorded the tail’s presence or the results of surgical intervention.)

Basolo used six pairs of males, each containing one fish with a visible and the other with a transparent sword. She tested each pair with nine to sixteen female fishes. Invariably, females preferred males with visible swords—even though males of this species have no swords at all in nature. As in all good experiments, Basolo then performed a variety of additional tests to eliminate other interpretations. She changed sides for males with visible and invisible swords—just in case females were choosing left or right sides of the aquarium, rather than visible or invisible swords. The females preferred the visible sword, regardless of position in the aquarium. She even performed a second operation and switched swords—placing the transparent sword into the fish that previously carried the colored version, and implanting the colored sword into the fish that had borne the invisible addition. The fish that had previously been shunned (presumably for its invisible sword) was now favored when bearing the sword with the prominent black border. Basolo concludes: “These data suggest that the females were basing their choice on sword preference and not other traits.”

The title of Basolo’s article says it all—“Female preference predates the evolution of the sword in swordtail fish” (see bibliography). Something in the sensory system of ancestral fishes evidently predisposed females of the
X. helleri
line to prefer males with swords. Since no previous member of this large and successful group of fishes possessed swords (so far as we know), this sensory and cognitive bias exists for other reasons, and must be regarded as fortuitous with respect to the evolution of swords. Male
Xiphophorus helleri
must, in this sense, thank Lady Luck for their graceful extensions.

Frog calls
. So much of what we view as most aesthetic and charming in nature—the singing and plumage of birds, as a prime example—actually functions as part of the great Darwinian struggle for reproductive success. Chorusing of males in crickets, frogs, or birds, is no paean of praise to the night, no hosanna to the joys of life, but a complex tapestry of challenge (to other males) or advertisement (to females).

In many frogs, the female choice model of sexual selection seems to apply, and males call to win the sexual attention of females—all in the service of the great Darwinian attempt to avoid croaking (vernacular sense) of family lines. Michael J. Ryan and colleagues at the University of Texas in Austin have applied the preexisting bias model (“sexual selection for sensory exploitation” in their terms) to the complex call of the Tungara frog,
Physalaemus pustulosus
(see bibliography).

This Panamanian frog has an unusually complex call, consisting of two sequential components with expressive names: a whine and a chuck. The call begins with the longer whine, about 350 milliseconds in duration, that gradually decreases in fundamental frequency from 900 to 400 Hertz. Although the whine contains up to three harmonics, most energy resides in the fundamental. (Harmonics are overtones generated from the fundamental and having higher frequencies at integral multiples of the fundamental. If that sounds like a mouthful, the first harmonic of a 220 Hz fundamental frequency is 440 Hz, the second 660 Hz, the third 880 Hz, etc.). The whine is followed by a series of one to six chucks. These chucks are much shorter in duration (about 40 milliseconds) and have a lower fundamental frequency of about 220 Hz. But, unlike the whine, chucks have much higher energy in the fifteen harmonics above the fundamental. In fact, some 90 percent of the energy resides in harmonics above 1500 Hz, with the peak frequency above 2000 Hz.