(This quotation illustrates a common source of misunderstanding. Darwin does often use such phrases as “advantageous to the community.” By our later linguistic conventions, such a statement might seem to signify a leaning to group selectionist arguments. But these conventions did not exist in Darwin's generation. Note how he uses this phrase only as a description of a result. Darwin identifies the causal process yielding this result, in this case and almost every other time he invokes such language, as selection on organisms, with benefit to communities as an epiphenomenal effect.)
The second challenge, the origin of sterility itself, seems more serious — for how could selection, especially in its necessarily gradualistic mode, promote the diminution of reproductive power in individuals? Clearly, the increasingly sterile workers cannot be promoting their own fitness; but their labor may aid their entire nest or hive. Must not the evolution of sterility therefore provide prima facie evidence for group selection, and for the failure of Darwin's argument about the exclusivity of selection on organisms?
Darwin does indeed refer to sterility as “one special difficulty, which at first appeared to me insuperable, and actually fatal to my whole theory” (p. 236). He then offers an explanation, based exclusively on organismal selection and similar to his argument about differences in form between workers and [Page 130] reproductives (p. 236): “How the workers have been rendered sterile is a difficulty; but not much greater than that of any other striking modification of structure; for it can be shown that some insects and other articulate animals in a state of nature occasionally become sterile; and if such insects had been social, and it had been profitable to the community that a number should have been annually born capable of work, but incapable of procreation, I can see no very great difficulty in this being effected by natural selection.”
The phrase “profitable to the community” seems to imply group selection but, as argued above, this modern interpretation need not reflect Darwin's intent. He did not, after all, know about haplodiploidy, different degrees of relatedness, or parent-offspring conflict. He does not argue here at the locus classicus for modern theories of group selection — altruism defined as the rendering of aid (at personal peril or expense) to non-relatives. Rather, he views the hive as a group of cooperating bodies, all tightly related and all generated by the queen. Anything beneficial to the hive fosters the reproductive success of the queen in ordinary natural selection upon her as an individual. The sterility of a worker does not differ in principle from the horns of an ox — a trait not found in parents, but produced by selection on parents. A queen that can generate more sterile workers might be favored by selection just as a breeder picks cows that yield castrated oxen with longer horns.
At most, one might hold that Darwin treats the entire hive as an entity — a statement about higher-level selection on the “superorganism” model (see D. S. Wilson and Sober, 1989, and Sober and Wilson, 1998). But here we meet an issue that must be regarded as more linguistic than substantive. Just as Janzen (1977) wishes to identify a clone as a single El (for “evolutionary individual”), and to treat single bodies of rotifers or aphids as parts, so too might Darwin view the bodies in a hive as iterated organs of the whole. Nonetheless, selection acts on the queen as an individual reproducer. The determinants of her success undoubtedly include the form and function of her sterile offspring. Natural selection can “get at” a beaver through the form of its dam, or at a bird through the shape of its nest — and we do not talk about selection on the higher-level entity of organism plus product. Why should selection not “get at” the queen ant or bee through the conformation of the hive and the function of its members? (See Ruse, 1980, for a parallel argument, in agreement with mine, on Darwin's explanation of hymenopteran castes by organismic selection.)
Darwin takes up a different challenge to the exclusivity of organismic selection in the next chapter on “Hybridism.” Crosses between varieties of a species are usually fertile, but crosses between species are generally sterile, or at least greatly impaired in fecundity. Under the guiding precepts of gradualism and uniformitarian methodology, we must view species as former varieties promoted by selection to the greater difference of true distinctness. But natural selection could not have built sterility in gradual degrees from an original fertility between parent and offspring — for sterility cannot benefit the hybrid individual: “On the theory of natural selection the case is especially important, inasmuch as the sterility of hybrids could not possibly be of any advantage [Page 131] to them, and therefore could not have been acquired by the continued preservation of successive profitable degrees of sterility. I hope, however, to be able to show that sterility is not a specially acquired or endowed quality but is incidental on other acquired differences” (p. 245).
Darwin considers two possible explanations. He constructs his entire chapter on hybridism as a defense of natural selection in its ordinary, organismal mode through the rejection of one explanation based on species selection and the advocacy of another rooted in selection on organisms with an interesting twist. Darwin admits that species selection, at first glance, seems to provide a simple and attractive solution: interspecific sterility must originate as an adaptation of species, built and promoted to preserve integrity by preventing introgression and subsequent dissolution. (A. R. Wallace strongly promoted this view. Darwin's firm rejection led to a protracted argument that strongly colored their relationship — see Kottler, 1985; Ruse, 1980.)
But Darwin rejected this explanation because he could not conceive how a species might act as an entity in this manner. Nonetheless, he could not possibly argue in response that hybrid sterility arose by direct selection for the trait itself. He therefore proposed a subtle argument, almost surely correct in our current judgment, for the origin of hybrid sterility as an incidental consequence of other differences established by organismal selection. A. R. Wallace, in striking contrast, remained so committed to viewing every natural phenomenon as a direct adaptation that he willingly roamed up and down among levels of selection (quite unaware of the logical difficulties thus entailed) until he found a locus that could support a direct adaptive explanation.
Darwin argued that any population, in diverging far enough from an ancestor to rank as a separate species, must undergo a series of changes (usually extensive), mediated by natural selection and leading to a set of unique features. Any two species will therefore come to differ in a series of traits directly built by natural selection. These disparities will probably render the two species sufficiently unlike, particularly in rates and modes of reproduction and development, that any hybrids between them will probably be stunted or infertile — not because selection acted directly for sterility, but only as an incidental effect of differences evolved by natural selection for other reasons. Although interspecific sterility cannot be built directly by selection for its advantages to organisms, this feature can and will originate as a consequence of ordinary selection on organisms. Darwin contrasts his proposal with Wallace's alternative based on direct adaptation via species selection:
Now do these complex and singular rules indicate that species have been endowed with sterility simply to prevent their becoming confounded in nature? I think not. For why should the sterility be so extremely different in degree, when various species are crossed, all of which we must suppose it would be equally important to keep from blending together? …The foregoing rules and facts, on the other hand, appear to me clearly to indicate that the sterility both of first crosses and of hybrids is simply [Page 132] incidental or dependent on unknown differences, chiefly in the reproductive systems, of the species which are crossed (p. 260).
In what I regard as Darwin's most brilliant use of his favorite device — argument by analogy — he then compares hybrid sterility with incompatibility in hybrid grafts (whereas grafts between varieties of the same species usually “take”). I find this comparison particularly compelling because we would not be te
mpted to construct an argument about species selection to explain the incompatibility of grafts — as no advantage for the integrity of species accrues thereby, especially since the “experiment” of grafting between two species almost never occurs in nature. Yet the logical structures of these two arguments about grafting and sterility, as well as the attendant results, share an identical logic — joining within species, and maintenance of separation between species, based upon incidental effects wrought by increasing degrees of difference evolved for other reasons:
It will be advisable to explain a little more fully by an example what I mean by sterility being incidental on other differences, and not a specially endowed quality. As the capacity of one plant to be grafted or budded on another is so entirely unimportant for its welfare in a state of nature, I presume that no one will suppose that this capacity is a specially endowed quality, but will admit that it is incidental on differences in the laws of growth of the two plants . . . The facts by no means seem to me to indicate that the greater or lesser difficulty of either grafting or crossing together various species has been a special endowment; although in the case of crossing, the difficulty is as important for the endurance and stability of specific forms, as in the case of grafting it is unimportant for their welfare (pp. 261-263).
Darwin then drives the point home with a lovely prose flourish (and a memorable visual image!) in explicitly rejecting an appeal to supraorganismal selection. Nature knows no explicit principle of higher-level order. “There is no more reason to think that species have been specially endowed with various degrees of sterility to prevent them crossing and blending in nature, than to think that trees have been specially endowed with various and somewhat analogous degrees of difficulty in being grafted together in order to prevent them becoming inarched in our forests” (p. 276).
The development of Darwin's views on organismic selection. If the first edition of the Origin only marked a waystation in fluctuation or degree of commitment, then Darwin's stand on organismic selection, however strongly expressed in this initiating volume, might not be deemed so central to his worldview. But Ruse (1980) has documented Darwin's continuing and increasing attention to this issue — particularly as he argued with Wallace (see also Kottler, 1985) about the principle of incidental effects to explain hybrid sterility as a side consequence of natural selection rather than a direct product of species selection. Ruse writes (1980, p. 620): “By the end of the decade [the 1860's] with respect to the animal and plant worlds, there was [Page 133] nothing implicit about Darwin's commitment to individual selection. He had looked long and hard at group selection and rejected it.”
How Darwin struggles with, and “walls off,” exceptions. The exegetical literature on Darwin usually states that he allowed only two exceptions, in the entire corpus of his writing, to the exclusivity of natural selection on organisms — first, in permitting some form of group selection for the neuter castes of social insects, and second, for the origin of human moral behavior. I agree with Ruse (see point 2 just above) that Darwin did not stray from his orthodoxy for social insects, though some of his terminological choices invite misinterpretation today. For human morality, on the other hand, Darwin did throw in the towel after long struggle — for he could not render altruism towards non-relatives by organismal selection. Nonetheless, a theory often becomes sharpened (not destroyed or even much compromised in a world of relative frequencies) by specifying a domain of exceptions — provided that the exceptions be rare in occurrence, and peculiar in form. As humans, we surely have a legitimate personal interest in our moral behavior, but we cannot enshrine this property as occupying more than a tiny corner of nature (whatever its eventual impact upon our planet, and whatever our parochial concern for its uniqueness).
In the Descent of Man, Darwin presents his most interesting and extensive discussion of supraorganismal selection. As an example of his clarity on the issue of levels of selection, consider the following passage on why natural selection could not foster altruistic behavior within a tribe — with an explicit final statement that differential success among distinct tribes should not be called natural selection:
But it may be asked, how within the limits of the same tribe did a large number of members first become endowed with these social and moral qualities, and how was the standard of excellence raised? It is extremely doubtful whether the offspring of the more sympathetic and benevolent parents, or of those who were the most faithful to their comrades, would be reared in greater number than the children of selfish and treacherous parents of the same tribe. He who was ready to sacrifice his life, as many a savage has been, rather than betray his comrades, would often leave no offspring to inherit his noble nature ... Therefore it seems scarcely possible (bearing in mind that we are not here speaking of one tribe being victorious over another) that the number of men gifted with such virtues, or that the standard of their excellence, would be increased through natural selection, that is, by the survival of the fittest (1871, vol. 1, p. 163).
In the light of this conundrum, and as part of his resolution, Darwin does allow for selection at the tribal level defined as differential success of groups with more altruists: “It must not be forgotten that although a high standard of morality gives but a slight or no advantage to each individual man and his children over the other men of the same tribe, yet that an advancement in the standard of morality, and an increase in the number of well-endowed men [Page 134] will certainly give an immense advantage to one tribe over another” (1871, p. 166).
This passage has often been quoted, but without its surrounding context of contrary alternatives and restrictive caveats, as a clean example of Darwin's move to a higher level of selection when required. But such an interpretation seriously misrepresents Darwin's motives and logic. He did make the move, but only as one factor in a surrounding context of mitigation. I regard these mitigations and restrictions to hold the line of organismal selection (expressed in three distinct arguments, discussed below) as far more interesting than the move itself, for Darwin's extreme reluctance to address selection at any level other than the organismic lies so well exposed in the totality.
1. The Descent, as a whole, rests upon the strongest mode of argument for organismal selection. Darwin did not write a separate book on human evolution; his ideas (mostly speculative) on this subject occupy the first, and shorter, part of a two volume treatise entitled, in full: The Descent of Man, and Selection in Relation to Sex. In other words, Darwin wrote the Descent as an introduction to his general exposition of sexual selection. We might regard the two parts as oddly juxtaposed until we realize that many of Darwin's major arguments about human evolution — in the establishment of secondary sexual characters, and in differentiation among races, for example — invoke sexual selection by intraspecific competition, rather than ordinary natural selection as adaptation to external environments. As Ruse (1980) notes, Darwin viewed sexual selection as the strongest general argument against group selection, for its theme of relentless struggle in mating among members of a population guarantees that individualism must reign, largely by precluding the formation of alliances that higher-level selection could exploit. (Modern notions of sexual selection do envision the formation of such alliances, so the argument may strike us as incorrect today — but Darwin conceived sexual selection as a hyperindividual mode.)
2. Darwin does not present his argument for tribal selection as a happy solution to the problem of morality, but only as one potential factor among others. He also devises an argument based on organismal selection — in the form that would be called “reciprocal altruism” today: “As the reasoning powers and foresight of the members became improved, each man would soon learn from experience that if he aided his fellow-men, he would commonly receive aid in return. From this low motive he might acquire the habit of aiding his fellows” (1871, p. 163).
3. Darwin presents tribal selection as a peculiarity based on the uniqueness of h
uman consciousness, and thus as a strictly circumscribed exception to the generality of organismal selection throughout living nature. As conscious beings, we become especially sensitive to the “praise and blame” of our fellows. If altruistic behavior gains a status as virtuous, then we might be persuaded — against our deeper biological drive for seeking personal advantage — to engage in such behaviors in order to foster praise or avoid calumny. In other words, a form of “cultural evolution,” rooted in our unique level of consciousness, could overcome the behaviors driven by organismal selection, and [Page 135] could establish a preference for altruistic acts that might then serve as a basis for tribal selection. But such an argument cannot enjoy wide application in nature, as all other species lack this special mental mechanism for spreading abstract ideas against the thrust of natural selection:
We may therefore conclude that primeval man, at a very remote period, would have been influenced by the praise and blame of his fellows. It is obvious, that the members of the same tribe would approve of conduct, which appeared to them to be for the general good, and would reprobate that which appeared evil... A man who was not impelled by any deep, instinctive feeling, to sacrifice his life for the good of others, yet was roused to such actions by a sense of glory, would by his example excite the same wish for glory in other men, and would strengthen by exercise the noble feeling of admiration. He might thus do far more good to his tribe than by begetting offspring with a tendency to inherit his own high character (1871, p. 165).
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