The precise characterization of adaptation has been the focus of a large controversy in biology, and the philosophy of biology, about what exactly is likely to be adapted. Wynne-Edwards (1962) claimed that groups and populations were sometimes adapted. This meant that natural selection worked in favor of groups or populations, which sounds contradictory to the fact that individuals are the entities subsisting and spreading through selection. Williams (1966) gave a forceful defense of selection and hence adaptation as bearing exclusively on individuals. And, since the determinants of hereditary variations that are selected are genes, he concluded that selection acts primarily at the level of the genes. It is to be remarked, however, that he did not refute the logical possibility of adapted groups and then group selection, but proved that the alleged cases of group selection were explainable by natural selection at the level of genes, which is somehow more theoretically parsimonious.15 Along those lines, Dawkins (1976, 1982) elaborated his view of genic selectionism (or the "gene's eye view'' of evolution), trying to account for all manifestations of selection.16 One must here distinguish genic selectionism, which is an assertion about processes of selection and selectionist explanation, from genic determinism, which means that all phenotypic traits are wholly caused by genes with no impinging of environment or learning. One could perfectly subscribe to genic selectionism without genic determinism, as did Dawkins himself, and Dennett (1995) or Rosenberg (1985). Some practitioners or propagandists of sociobiology did make this confusion, which bore some hazardous moral and political consequences that in turn proved quite damaging for serious research conducted in those fields. But the genic selectionist's concept of gene only requires that the presence of a gene in a genotype in an environment makes a difference relative to the lack of this gene in the same context; the weaker requisite is that genes be "difference makers'' (Sterelny and Kitcher 1988), and here there is no commitment to any assumption about what genes determine and through which channels. This idea is the meaning of the locution "gene for'' which unhappily has been read in a deterministic sense. Genic selectionism does not prevent an environment from being as much a determinant as genes in the success of a trait (Gray 2001).
15 In fact, Williams (1992) elaborated and defended the concept of clade selection, added to gene selection.
16 On the differences between Williams' conception and Dawkins' gene's eye view, see Kenneth Waters (1991).
One of Dawkins' major arguments was the concept of inclusive fitness developed by Hamilton through his research on kin selection. Here, turning to the level of genes within selective explanation appeared fruitful in studying such features as cooperation or altruism that sounded at first glance contradictory to natural selection as enhancing the individual's fitness. The question, then, was to determine a level at which natural selection could explain the fact of altruism such as sterility of males in some hymenoptera species. Altruism has been selected because, although it decreases the fitness of the altruistic individual, it increases the representation ofits genes in the next generation, provided that the individual is closely enough related genetically to individuals benefiting from this altruism. This is the case in insect societies that are essentially kin societies.
Genic selectionism has been challenged in several ways by Gould, Lewontin, Sober, and Brandon. One main argument is that selection acts only on pheno-types hence is blind to genotypes. Therefore, the level of genes is not relevant for understanding selection. Many genotypes, hence many genes, are identical selectively provided that they are "genes for'' the same phenotypic trait. Using a notion elaborated by Reichenbach and Salmon in a philosophical debate about probabilities, the argument states that phenotypic interactions screen off the efficiency of genotypes and their relationships with environment. It does not deny that together with environments genotypes cause the phenotypes, but rather that this kind of causation does not explain the outcome of selection since it is necessary and sufficient for this purpose to consider the effects of the interaction of phenotype with its biotic and abiotic environments.17
The other line of defense, stated by Lewontin and Sober (1981), is the context-sensitivity principle, which claims that, since the phenotypic effects of a gene depend on the environmental and genetical context of its expression, a single allele cannot be the bearer of the selective causal process. The authors' example is then the case of heterozygote superiority, since in this case the diploid genotype (e.g., AA, or Aa or aa) and not the single allele (e.g., A or a), is the genuine entity supporting the selection process. One can surely mathematically describe what happens to the single allele, but this gene's eye view account is not causally explanatory.
Although biological evolution has been theoretically defined as a change in gene frequencies, the fact that the general model of the process of selection is not committed to any determination of the entities undergoing natural selection
17 A screens off B as a cause of C iff Pr (C/A&B) = Pr (C/A) / Pr (C/B). Sober (1992) contested that "screening off'' can yield a rebuttal of genic selectionism, since the argument is open to an almost infinite regress within which sometimes the most important explanatory cause is not the one which screens off all others.
implies that they are not necessarily "genes." Hull gave a formulation in terms of replicators (hereditarily reproducing entities) and interactors (entities whose causal relationships affected the hereditary success of the replicators they are associated with).18 In most classical cases of natural selection, replicators are genes and interactors organisms. The gene's eye view, then, says that since genes are the replicators, they are the units of selection. But of course this formal definition could be applied to other cases, in which replicators could be species or clades, or interactors could be genes themselves or groups. A more fine-grained approach of the various processes of selection is, thus, allowed by this formal characterization. For example, in the case of meiotic drive or segregation distorters—cases important to Dawkins' argument—genes are themselves the inter-actors. But the "replication" idea faces some specific problems since it mixes the idea of reproducing, and the idea of copying (Godfrey-Smith 2000a). Only genes replicate since organisms reproduce but they do not copy themselves; yet, unlike organisms, genes are not alone in the replication process, they are involved in a whole machinery (ribosomes, enzymes, proteins, etc.). However, this machinery allows the differential expression of genes in the genome through regulation of their transcription into mRNA and proteins. This transcription might be thought of as a copying of the gene, but it is not really a reproduction, since it is a process distinct from the replication of the cell in mitosis or inheritance through meiosis. Moreover, this copying process is submitted to the regulation of gene expression, contrary to the replication in mitosis. The general conclusion is that in no case are "copy" and "reproduce" synonymic or correlative notions, which weakens the very notion of "replication."
One point of interest of such a formulation is nevertheless that it can handle selection even outside biology, for instance, when we talk about cultural entities.19 The theoretical problem that faces this vision is to define a form of heredity in order to pick out the replicators. Hull thought that his formal characterization of selection was quite a logical one and embraced all possible cases. Giving the counterfactual example of the "protein world'' that has no replication of entities, Godfrey-Smith (2000a) showed that the interactor-replicator couple is not necessary to the selection process as such; however, in our world, almost any selective process does rely on these elements.
18 Dawkins coined "replicators" but opposed it to ''vehicles''; this word is too bound to the intuitive organism-genes difference.
19 For a general abstract account of theories using the concept of selection, such as immunology or evolutionary theory (''selection type theories''), see Darden and Cain (1988). For a theory of selection forged to address both evolution, immunology, and operant behavior, see Hull et al. (2001).
Easily expressible in this context, another argument against genic selection-ism rests on the "parity thesis'' (Sterelny, Griffiths), stating that all elements of the replication process are on a par (Griffiths and Gray 1994; Griffiths and Knight 1998; Oyama 2000), since environments as well as cytoplasmic elements or learned traits are "difference-makers" in the phenotypic outcome, exactly like genes.20 This thesis challenges both genic selectionism and genic determinism. Moreover, proponents of this theoretical alternative sometimes called Developmental System Theory contend that there exist kinds of heredity other than genetic inheritance, for example, nest styles, bird songs, or methylation patterns (Gray 2001; Jablonka 2001; Neumann-Held 2001). This challenge to gene's eye view, consisting in a multiplication of the replicators, is more radical than the other critiques because the whole concept of the selective process has to be transformed.21 However, while accepting several kinds of replicators, Maynard-Smith and Szathmary (1995) trace a line between "limited" and "unlimited'' inheritance, the latter allowing a quite infinite range of creation and transmission of elements. Only genes—and language—provide such an inheritance, which accounts for the extreme diversity and creativity of biological and cultural evolution.22
The thesis of genic selectionism has been undoubtedly stimulating in compelling people to clarify their concepts and presuppositions. In fact, reacting to Dawkins' extreme positions, some biologists did conceive of cases and mechanisms of group selection that could escape Williams' critique. Nunney (1999) tried to define lineage selection, an idea that was suggested by Hull (1980), whereas Gould invoked a species selection (for properties, such as size, sex, etc.) that Williams (1992) refuted, although admitting and defending a clade selection above the level of genic selection.23 D. S. Wilson and Sober provided theoretical grounds for the use of group selection (Sober 1988a; Wilson 1992; Sober and Wilson 1994, 1998), and, especially in Unto others, designed a pathway from evolutionary altruism to psychological altruism. Their argument first relies on
20 The gene's eye view defense has been the notion of information, in order to qualify the specificity of the genes' role against other factors. Information should be semantically defined. It is not a simple usual correlation (fire-smoke) that is always reversible. Maynard-Smith (2000) elaborated this option, but difficulties raised by Godfrey-Smith (2000b) are numerous and go against a univocal notion of biological information.
21 Clear formulations of the DST program are given by Gray (2001) and Oyama (Oyama, Gray, Griffith 2001). On the developmentalist challenge and its integration into evolutionary theories, see later.
22 Gray (2001) provides a critique of the distinction.
23 Williams' argument is that only a set of gene pools can behave in the same way as a gene pool when it comes to natural selection. Hence, there is only clade selection above the level of gene selection.
distinguishing and comparing within-group and between-group selection processes. Wilson and Sober's argument invokes a "common fate'' (Sober 1988a) of individuals in a group selection process, which implies that the selection process is compelled to act on all those individuals as a whole; then, secondary selective processes maintain this common fate, and selection can act at the level of the group. One consequence is that even kin selection appears as a form of group selection, rather than being genic selection's underpinning of an apparently altruistic phenomenon. Group selection, however, is not exclusive of genic selectionism, since its point is that groups are vehicles; it is yet another question to decide whether or not genes are the only replicators involved.
Concerning genic selectionism, two strong positions are opposed nowadays among philosophers of biology. The first one, formulated by Brandon (1988) is pluralism: it states that there are several levels of selection and several units of selection. It is then an empirical question to know in any given case which are the actual forms of natural selection, but most empirical evidence is in favor of selection above the level of organisms in some cases, added to selection at the level of genes. The opposing position is defended by Sterelny and Kitcher (1988), who claim that there is always a genic selectionism which operates together with any kind of selection, even if we cannot have empirical access to this level, and even if it is pragmatically more interesting for biologists to recognize supraorga-nismic selection processes and treat them as such. The genic level is always the "maximally informative'' one.24
Those philosophical considerations do not, in fact, impinge on biological investigations. It seems that biologists are in practice mostly pluralist on this issue (for example, Williams 1992), but it is not clear whether the decision between the two contrasting positions could be settled by the results of empirical inquiry. Some biologists, in fact, ignore those considerations and take for granted, since it is required by their practice, that there are several levels of selection (Keller and Reeve 1999) that have to be studied for themselves. But the recognition of the plurality of levels—notwithstanding the question of its ultimate theoretical reducibility to a genic one—gave rise to the important biological issue of their articulation. Michod (1999) elaborated the schema of a Darwinian dynamics, which accounts for the progressive emergence of new kinds of units of fitness: macromolecules, genes, cells, organisms, etc. The process relies widely on tradeoffs between decrease in fitness in lower levels (for example, association of
24 Lewontin and Godfrey-Smith (1993) showed that even if an allelic descriptive and predictive model is always possible in cases classically opposed to genic selectionism, provided that one in some case enriches the model with conditional probabilities of alleles, however, those formal questions of adequate models do not decide the point of what is the causally relevant level.
individuals creating a common interest, which hurts the interest of the individual) and increase in fitness at the higher level (for example, the level of the association itself), and this trade-off is exemplarily a case of multilevel selection. The recurrent problem is then to find models that show how, in each case, the prime for defection (e.g., breaking the association), which is available each time there is a "common good'' (Leigh 1999), can be overcome through this multilevel selection.
Although developed at a rather conceptual level, and mostly by philosophers, such controversies bear important consequences for the general meaning of the theory of evolution. What is at stake with altruism is the possibility of extending selectionist explanations in order to understand phenomena in the human domain. If altruism is explainable either by kin selection theory, or by Trivers' reciprocal altruism (1971), which holds for populations of nonrelated organisms and is now derived from Game theory, particularly from the results of the study of the Prisoners Dilemma by Axelrod, then the issue of levels and units of selection is at the same time the issue of the foundation of an evolutionary approach, not only of the emergence of man and human societies but also of the current human psyche and societies through a selectionist framework, a research program now called "evolutionary psychology'' (see below 3.2). Of course, altruism as studied by biologists is not what vernacular language calls altruism. For example, some very "egoistic" fellow (in ordinary language) would be biologically altruistic if he also wanted to leave no offspring; in contrast, a mother who sacrificed an entire life to her children, even if the perfect model of "altruism", would from a biological point of view be typically selfish since she is entirely devoted to entities, which share 50% of her genes.25 So, no matter what the conclusion of the units of selection debate, all the lessons that might be taken from evolutionary biology into psychology have to be checked regarding whether they use vernacular or technical concepts and whether they do or do not carry illegitimate confusions between those two meanings.
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