The objects of selection

The proposal by Williams (7) to adopt the gene as the object of selection not only conformed to the prevailing reductionist spirit of the time but also fitted into the thinking of many geneticists who in the mathematical analyses of population genetics had adopted the gene as the principal entity of evolutionary change. Williams’s proposal was strongly endorsed by Dawkins (9). This idea of the gene as the target of selection was at first widely accepted, for instance by Lewontin (10). But eventually it was severely criticized (11, 12), and even its original supporters have now moderated their claims. The critics pointed out that “naked genes,” “not being independent objects” (9), are not “visible” to selection and therefore can never serve as the target. Furthermore, the same gene, for instance the human sickle cell gene, may be beneficial in heterozygous condition (in Plasmodium falciparum areas) but deleterious and often lethal in the homozygous state. Many genes have different fitness values when placed into different genotypes. Genic selectionism is also invalidated by the pleiotropy of many genes and the interaction of genes controlling polygenic components of the phenotype. On one occasion Dawkins (ref. 13, point 7) himself admits that the gene is not an object of selection: “. . . genetic replicators are selected not directly, but by proxy . . . [by] their phenotypic effects.” Precisely! Nor are combinations of genes, as for instance chromosomes, independent objects of selection; only their carriers are.

Since only a fraction of all eggs are fertilized and only an infinitesimal fraction of male gametes succeed in fertilizing an egg, gametes are obviously a category of entities subjected to intense selection. It is curious that this is virtually never mentioned in the literature dealing with selection, perhaps because we know so little about fitness differences among gametes. For instance, the success in terrestrial vertebrates of a spermatozoon in fertilizing an egg is presumably quite unrelated to the properties of its haploid genome that makes successful adults. Evidently, the ability to swim rapidly, to be able to sense unfertilized eggs, and to be able to penetrate the egg membrane are the properties of the spermatozoon that are most helpful in achieving success. However, these phenotypic properties of the spermatozoa are presumably produced by the paternal testis and are probably part of the extended phenotype of the male parent. They have nothing to do with the haploid genome of the gametes, which, so far as we can tell, has no influence whatsoever on the fertilizing capacity of these gametes. Chance is presumably the most overwhelmingly important factor at this level. But in other organisms gametes (e.g., plant pollen grains and free swimming gametes in aquatic organisms) seem to have gamete-specific properties influencing mating success. They may be genuine selectons.

From Darwin to the present day most evolutionists (1) have considered the individual organism to be the principal object of selection. Actually, it is the phenotype which is the part of the individual that is “visible” to selection (14). Every genotype, interacting with the environment, produces a range of phenotypes, called by Woltereck (15) the “norm of reaction.” Therefore, when an evolutionist says that the “genome is a program that directs development,” it would be wrong to think of it in a deterministic way. The development of the phenotype involves many stochastic processes which preclude a one-to-one relation between genotype and phenotype. This is, of course, precisely the reason why we must accept the phenotype as the object of selection rather than the genotype.

Different phenotypic expressions of the same genotype may differ considerably in their fitness value. What is visible to selection is the phenotype which “screens off” the underlying genotype (2). The term phenotype refers not only to structural characteristics but also to behavioral ones and to the products of such behavior such as bird nests and spider webs. Dawkins (13) refers to these as the extended phenotype. However, such species-specific behaviors are programmed in the neural system of these individuals and thus do not differ in principle from the morphological aspects of the phenotype.

In this account, when I refer to the term individual, I always mean what the word individual means in the daily language, that is, the individual organism. Philosophers have also applied the term to “particulars,” like the species. I have avoided this designation because it is apt to create confusion.

There has been a long and bitter controversy as to whether groups as cohesive wholes can serve as targets of selection. The answer is “it depends.” There are different kinds of assemblages of individuals (“groups”), some of which do and others which do not qualify as targets of selection. At one time I classified groups on the basis of size and geographical relationship (16), but this did not turn out to be a productive approach. However, there is another approach which usually produces clear-cut results. It is obvious that a group, the selective value of which is simply the arithmetic mean of the fitness values of the composing individuals (when in isolation), is not a target of selection. If such a group is particularly successful, it is due to the superior fitness of the composing individuals. This idea has often been included in theories of group selection. However, this false or soft group selection is not group selection at all. In contrast, if, owing to the interaction of the composing individuals or owing to a division of labor and other social actions, the fitness of the group is higher or lower than the arithmetic mean of the fitness values of the composing individuals, then the group as a whole can serve as an object of selection. I call this hard group selection. Interestingly, this was already appreciated by Darwin in a discussion of groups of primitive humans (4). Such hard group selection, a prerequisite for the explanation of human ethics, is still controversial.

It is sometimes difficult to decide whether the success of a particular group is due to soft or hard group selection. However, when a group of ground squirrels is particularly successful, because it has an efficient system of sentinels warning the group of approaching predators, it is clearly hard group selection. This is also the case when a pride of lionesses splits up to block the escape route of an intended victim. The success of surprise attacks by chimpanzees on members of neighboring troupes depends on the well organized strategy of the attackers. In all such cases the successful group acts as a unit and is as a whole the entity favored by selection.

There has been much argument about whether there is, or is not, such a phenomenon as species selection. In the early post-Darwinian period when thinking about selection was rather confused, it was often said that such and such a character had evolved because it was “good for the species.” This is quite misleading. The selected character had originated because it benefited certain individuals of a species and had gradually spread to all others. The species as an entity does not answer to selection.

There is, of course, no question that one species can cause the extinction of another species. The introduction of the Nile perch into Lake Victoria in Africa has resulted in the extinction of several hundred endemic species of cichlid fishes. The parasitic cowbird almost exterminated the Kirtland’s warbler in northern Michigan until drastic cowbird eradication procedures in the breeding range of Kirtland’s warbler were adopted. Darwin (3) described in 1859 the extermination of many native New Zealand species of animals and plants by the introduction of competing species from England. The competitors were by no means always close relatives. In spite of all these examples I hesitate to use the term species selection and prefer to call such events species turnover or species replacement because the actual selection takes place at the level of competing individuals of the two species. It is individual selection discriminating against the individuals of the losing species that causes the extinction.

Some authors have also attempted to recognize even higher levels such as family selection or clade selection, but in no case are these entities as such the object of selection. Selection in these cases always takes place at the level of individuals.

This term was introduced by Lewontin (10) to designate the object of selection. In science as well as in daily life the term unit usually means some measurable entity. We have units of length, weight, and time, and we have electrical units like volt, watt, ohm, etc. Clearly, unit of selection does not refer to this kind of unit. Occasionally, we also use the word unit for concrete entities, for example, “The president sent several units of marines to the area of the disturbances.” The term unit of selection was adopted by many authors, but many others found it so unsuitable that they introduced new terms. Owing to its ambiguity, the term unit has been used less and less frequently in recent years.

Dawkins, the author of this term, states, “We may define a replicator as any entity in the universe which interacts with its world, including other replicators in such a way that copies of itself are made” (17). He also states that “a DNA molecule is the obvious replicator.” In other words, replicator selection is essentially a new word for gene selection. One of the advantages of his term, says Dawkins, is that it automatically preadapts our language to deal “with non-DNA forms of evolution such as may be encountered on other planets.” This strikes me as a rather curious excuse for introducing a new term into science. With the phenotype of the individual rather than the gene being the target of selection, the term replicator becomes irrelevant.

The term is, of course, in complete conflict with the basic Darwinian thought. What is important in selection is the abundant production of new phenotypes to permit the species to keep up with possible changes in the environment. This is made possible by meiosis and sexual reproduction. The replication of DNA has nothing to do with this. To be sure, Mendel’s discovery of the constancy of genes, confirmed by all the subsequent work in genetics and molecular biology, is a very efficient way to achieve rapid and unambiguous evolutionary change, and it refuted the inheritance of acquired characters. But such constancy is not a necessity for selection. For Darwin inheritance of acquired characters and a direct effect of the environment were compatible with natural selection. He did not demand complete constancy of the genetic material. Since the gene is not an object of selection (there are no naked genes), any emphasis on precise replication is irrelevant. Evolution is not a change in gene frequencies, as is claimed so often, but the maintenance (or improvement) of adaptedness and the origin of diversity. Changes in gene frequency are a result of such evolution, not its cause. The claim of gene selection is a typical case of reduction beyond the level where analysis is useful.

In due time Dawkins (17) realized that the individual reproducing organism did have a role in the selection process. But being a gene selectionist, he saw this role only as the function to serve as a transport mechanism for the genes. He therefore introduced for individuals the terms “vehicle.” Doing so, he missed the decisive point that the phenotype is far more than a vehicle for the genotype. The term vehicle altogether fails to bring out the important role of the phenotype in the process of selection.

Hull (18) realized the unsuitability of the term vehicle because he appreciated that the object of selection acts “as a cohesive whole with its environment.” To stress this interaction he proposed the term interactor “as an entity that directly interacts as a cohesive whole with its environment in such a way that replication is differential.” The term interactor has a number of weaknesses. One is the stress on replication while omitting any reference to the production of variation during meiosis and reproduction. More serious is the fact that interactor is not a specific term for the object of selection. Every cell is an interactor; every organ of an organism interacts with the other organs, species interact, and so do classes of individuals such as the two sexes. Also, interacting is not conspicuous during the process of elimination that results in natural selection. In biology interaction is far more pertinent to functional than to evolutionary biology. When one hears the word interactor, one’s first thought would never be natural selection. What is needed is a more specific term.

For many years I used the term target of selection for the object of selection. The more I realized, however, that natural selection is an elimination process, the more I realized that the eliminated individuals were the real target of the selection process and that it was rather misleading to call the “leftovers” the target of selection.

Dawkins (19) has introduced the term “meme” for the entities subject to selection in cultural evolution. It seems to me that this word is nothing but an unnecessary synonym of the term “concept.” Dawkins apparently liked the word meme owing to its similarity to the word gene. In neither his definition nor the examples illustrating what memes are does Dawkins mention anything that would distinguish memes from concepts. Concepts are not restricted to an individual or to a generation, and they may persist for long periods of time. They are able to evolve.

Since all the previously used technical names for the object of selection are unsuitable for one reason or another, I am herewith proposing a new term, “selecton.” A selecton is a discrete entity and a cohesive whole, an individual or a social group, the survival and successful reproduction of which is favored by selection owing to its possession of certain properties. The selecton is the answer to Sober’s question “selection of?” (see above). This still leaves us with Sober’s other question.