The Panda’s Thumb (7 page)

In reading Schweber's detailed account of the moments preceding Darwin's formulation of natural selection, I was particularly struck by the absence of deciding influence from his own field of biology. The immediate precipitators were a social scientist, an economist, and a statistician. If genius has any common denominator, I would propose breadth of interest and the ability to construct fruitful analogies between fields.

In fact, I believe that the theory of natural selection should be viewed as an extended analogy—whether conscious or unconscious on Darwin's part I do not know—to the laissez faire economics of Adam Smith. The essence of Smith's argument is a paradox of sorts: if you want an ordered economy providing maximal benefits to all, then let individuals compete and struggle for their own advantages. The result, after appropriate sorting and elimination of the inefficient, will be a stable and harmonious polity. Apparent order arises naturally from the struggle among individuals, not from predestined principles or higher control. Dugald Stewart epitomized Smith's system in the book Darwin read:

As Schweber states: “The Scottish analysis of society contends that the combined effect of individual actions results in the institutions upon which society is based, and that such a society is a stable and evolving one and functions without a designing and directing mind.”

We know that Darwin's uniqueness does not reside in his support for the idea of evolution—scores of scientists had preceded him in this. His special contribution rests upon his documentation and upon the novel character of his theory about how evolution operates. Previous evolutionists had proposed unworkable schemes based on internal perfecting tendencies and inherent directions. Darwin advocated a natural and testable theory based on immediate interaction among individuals (his opponents considered it heartlessly mechanistic). The theory of natural selection is a creative transfer to biology of Adam Smith's basic argument for a rational economy: the balance and order of nature does not arise from a higher, external (divine) control, or from the existence of laws operating directly upon the whole, but from struggle among individuals for their own benefits (in modern terms, for the transmission of their genes to future generations through differential success in reproduction).

Many people are distressed to hear such an argument. Does it not compromise the integrity of science if some of its primary conclusions originate by analogy from contemporary politics and culture rather than from data of the discipline itself? In a famous letter to Engels, Karl Marx identified the similarities between natural selection and the English social scene:

Yet Marx was a great admirer of Darwin—and in this apparent paradox lies resolution. For reasons involving all the themes I have emphasized here—that inductivism is inadequate, that creativity demands breadth, and that analogy is a profound source of insight—great thinkers cannot be divorced from their social background. But the source of an idea is one thing; its truth or fruitfulness is another. The psychology and utility of discovery are very different subjects indeed. Darwin may have cribbed the idea of natural selection from economics, but it may still be right. As the German socialist Karl Kautsky wrote in 1902: “The fact that an idea emanates from a particular class, or accords with their interests, of course proves nothing as to its truth or falsity.” In this case, it is ironic that Adam Smith's system of laissez faire does not work in his own domain of economics, for it leads to oligopoly and revolution, rather than to order and harmony. Struggle among individuals does, however, seem to be the law of nature.

Many people use such arguments about social context to ascribe great insights primarily to the indefinable phenomenon of good luck. Thus, Darwin was lucky to be born rich, lucky to be on the
Beagle
, lucky to live amidst the ideas of his age, lucky to trip over Parson Malthus—essentially little more than a man in the right place at the right time. Yet, when we read of his personal struggle to understand, the breadth of his concerns and study, and the directedness of his search for a mechanism of evolution, we understand why Pasteur made his famous quip that fortune favors the prepared mind.

CAN ANYTHING BE
more demoralizing than parental incompetence before the most obvious and innocent of children's questions: why is the sky blue, the grass green? Why does the moon have phases? Our embarrassment is all the more acute because we thought we knew the answer perfectly well, but hadn't rehearsed it since we ourselves had received a bumbled response in similar circumstances a generation earlier. It is the things we think we know—because they are so elementary, or because they surround us—that often present the greatest difficulties when we are actually challenged to explain them.

One such question, with an obvious and incorrect answer, lies close to our biological lives: why, in humans (and in most species familiar to us), are males and females produced in approximately equal numbers? (Actually, males are more common than females at birth in humans, but differential mortality of males leads to a female majority in later life. Still, the departures from a one to one ratio are never great.) At first glance, the answer seems to be, as in Rabelais's motto, “plain as the nose on a man's face.” After all, sexual reproduction requires a mate; equal numbers imply universal mating—the happy Darwinian status of maximal reproductive capacity. At second glance, it isn't so clear at all, and we are drawn in confusion to Shakespeare's recasting of the simile: “A jest unseen, inscrutable, invisible, as a nose on a man's face.” If maximal reproductive capacity is the optimal state for a species, then why make equal numbers of males and females. Females, after all, set the limit upon numbers of offspring, since eggs are invariably so much larger and less abundant than sperm in species familiar to us—that is, each egg can make an offspring, each sperm cannot. A male can impregnate several females. If a male can mate with nine females and the population contains a hundred individuals, why not make ten males and ninety females? Reproductive capacity will certainly exceed that of a population composed of fifty males and fifty females. Populations made predominantly of females should, by their more rapid rates of reproduction, win any evolutionary race with populations that maintain equality in numbers between the sexes.

What appeared obvious is therefore rendered problematical and the question remains: why do most sexual species contain approximately equal numbers of males and females? The answer, according to most evolutionary biologists, lies in a recognition that Darwin's theory of natural selection speaks only of struggle among
individuals
for reproductive success. It contains no statement about the good of populations, species, or ecosystems. The argument for ninety females and ten males was framed in terms of advantages for populations as a whole—the usual, congenial, and dead wrong, way in which most people think of evolution. If evolution worked for the good of populations as a whole, then sexual species would contain relatively few males.

The observed equality of males and females, in the face of obvious advantages for female predominance if evolution worked upon groups, stands as one of our most elegant demonstrations that Darwin was right—natural selection works by the struggle of individuals to maximize their own reproductive success. The Darwinian argument was first framed by the great British mathematical biologist R.A. Fisher. Suppose, Fisher argued, that either sex began to predominate. Let us say, for example, that fewer males than females are born. Males now begin to leave more offspring than females since their opportunities for mating increase as they become rarer—that is, they impregnate more than one female on average. Thus, if any genetic factors influence the relative proportion of males born to a parent (and such factors do exist), then parents with a genetic inclination to produce males will gain a Darwinian advantage—they will produce more than an average number of grandchildren thanks to the superior reproductive success of their predominantly male offspring. Thus, genes that favor the production of males will spread and male births will rise in frequency. But, this advantage for males fades out as male births increase and it disappears entirely when males equal females in number. Since the same argument works in reverse to favor female births when females are rare, the sex ratio is driven by Darwinian processes to its equilibrium value of one to one.

But how would a biologist go about testing Fisher's theory of sex ratio? Ironically, the species that confirm its predictions are no great help beyond the initial observation. Once we frame the basic argument and determine that the species we know best have approximately equal numbers of males and females, what do we achieve by finding that the next thousand species are similarly ordered? Sure, it all fits, but we do not gain an equal amount of confidence each time we add a new species. Perhaps the one to one ratio exists for another reason?

To test Fisher's theory, we must look for exceptions. We must seek unusual situations in which the premises of Fisher's theory are not met—situations that lead to a specific prediction about how sex ratio should depart from one to one. If change of premises leads to a definite and successful prediction of altered outcome, then we have an independent test that strongly boosts our confidence. This method is embodied in the old proverb that “the exception proves the rule,” although many people misunderstand the proverb because it embodies the less common meaning of “prove.” Prove comes from the Latin
probare—
to test or to try. Its usual, modern meaning refers to final and convincing demonstration and the motto would seem to say that exceptions establish indubitable validity. But in another sense, closer to its root, “prove” (as in “proving ground” or printer's “proof”) is more like its cognate “probe”—a test or an exploration. It is the exception that probes the rule by testing and exploring its consequences in altered situations.

Here nature's rich diversity comes to our aid. The stereotyped image of a birder assiduously adding the rufous-crowned, peg-legged, speckle-backed, cross-billed and cross-eyed towhee to his life list gives, in unwarranted ridicule, a perverted twist to the actual use made by naturalists of life's diversity. It is nature's richness that permits us to establish a science of natural history in the first place—for the variety virtually guarantees that appropriate exceptions can be found to probe any rule. Oddities and weirdnesses are tests of generality, not mere peculiarities to describe and greet with awe or a chuckle.

Fortunately, nature has been profligate in providing species and modes of life that violate the premises of Fisher's argument. In 1967, British biologist W.D. Hamilton (now at the University of Michigan) gathered the cases and arguments into an article entitled “Extraordinary sex ratios.” I will discuss in this essay only the clearest and most important of these probing violations.

Nature rarely heeds our homilies in all cases. We are told, and with good reason, that mating of brothers and sisters should be avoided, lest too many unfavorable recessive genes gain an opportunity to express themselves in double dose. (Such genes tend to be rare, and chances are small that two unrelated parents will both carry them. But the probability that two sibs carry the same gene is usually fifty percent.) Nonetheless, some animals never heard the rule and indulge, perhaps exclusively, in sib mating.

Exclusive sib mating destroys the major premise of Fisher's argument for one to one sex ratios. If females are always fertilized by their brothers, then the same parents manufacture both partners of any mating. Fisher assumed that the males had different parents and that an undersupply of males awarded genetic advantages to those parents that could produce males preferentially. But if the same parents produce
both
the mothers and fathers of their grandchildren, then they have an equal genetic investment in each grandchild, no matter what percentage of males and females they produce among their children. In this case, the reason for an equal balance of males and females disappears and the previous argument for female predominance reasserts itself. If each pair of grandparents has a limited store of energy to invest in offspring, and if grandparents producing more offspring gain a Darwinian edge, then grandparents should make as many daughters as possible, and produce only enough sons to ensure that all their daughters will be fertilized. In fact, if their sons can muster sufficient sexual prowess, then parents should make just one son and use every bit of remaining energy to produce as many daughters as they can. As usual, bountiful nature comes to our aid with numerous exceptions to probe Fisher's rule: indeed, species with sib mating also tend to produce a minimal number of males.

Consider the curious life of a male mite in the genus
Adactylidium
, as described by E.A. Albadry and M.S.F. Tawfik in 1966. It emerges from its mother's body and promptly dies within a few hours, having done apparently nothing during its brief life. It attempts, while outside its mother, neither to feed nor to mate. We know about creatures with short adult lives—the mayfly's single day after a much lengthier larval life, for example. But the mayfly mates and insures the continuity of its kind during these few precious hours. The males of
Adactylidium
seem to do nothing at all but emerge and die.

To solve the mystery, we must study the entire life cycle and look inside the mother's body. The impregnated female of
Adactylidium
attaches to the egg of a thrips. That single egg provides the only source of nutrition for rearing all her offspring—for she will feed on nothing else before her death. This mite, so far as we know, engages exclusively in sib mating; thus, it should produce a minimal number of males. Moreover, since total reproductive energy is so strongly constrained by the nutritional resources of a single thrips' egg, progeny are strictly limited, and the more females the better. Indeed,
Adactylidium
matches our prediction by raising a brood of five to eight sisters accompanied by a single male who will serve as both brother and husband to them all. But producing a single male is chancy; if it dies, all sisters will remain virgins and their mother's evolutionary life is over.

If the mite takes a chance on producing but a single male, thus maximizing its potential brood of fertile females, two other adaptations might lessen the risk—providing both protection for the male and guaranteed proximity to his sisters. What better than to rear the brood entirely within a mother's body, feeding both larvae and adults within her, and even allowing copulation to occur inside her protective shell. Indeed, about forty-eight hours after she attaches to the thrips' egg, six to nine eggs hatch within the body of a female
Adactylidium
. The larvae feed on their mother's body, literally devouring her from inside. Two days later, the offspring reach maturity, and the single male copulates with all his sisters. By this time, the mother's tissues have disintegrated, and her body space is a mass of adult mites, their feces, and their discarded larval and nymphal skeletons. The offspring then cut holes through their mother's body wall and emerge. The females must now find a thrips' egg and begin the process again, but the males have already fulfilled their evolutionary role before “birth.” They emerge, react however a mite does to the glories of the outside world, and promptly die.

But why not carry the process one stage further? Why should the male be born at all? After copulating with its sisters, its work is done. It is ready to chant the acarine version of Simeon's prayer,
Nunc dimittis—
Oh Lord, now lettest thou thy servant depart in peace. Indeed, since everything that is possible tends to occur at least once in the multifarious world of life, a close relative of
Adactylidium
does just this.
Acarophenax tribolii
also indulges exclusively in sib mating. Fifteen eggs, including but a single male, develop within the mother's body. The male emerges within his mother's shell, copulates with all his sisters and dies before birth. It may not sound like much of a life, but the male
Acarophenax
does as much for its evolutionary continuity as Abraham did in fathering children into his tenth decade.

Nature's oddities are more than good stories. They are material for probing the limits of interesting theories about life's history and meaning.