The assumption that Darwin’s principle of natural selection is free of empirical content is not very plausible. I reconstruct his claim about natural selection from the first edition of the Origin (Darwin 1859) and thus from the argument as he gave it before Spencer’s phrase was coined. His claim differs drastically from the reading of Spencer’s phrase that became usual within the MS framework: It has strong empirical content. Although also a notion close to fitness as understood in MS and in population genetics can be found in Darwin, this notion is not even closely related to what he means when using the term “the fittest.” As can be expected from a ground-breaking insight within empirical science, his claim is not tautological but refutable and in need of empirical support. This might be one reason why the Origin is so rich in reported observations and discussion of analogies.
Darwin’s notion of natural selection is the basis for his argument about the generation of biological species (Darwin 1859, 1876). This notion combines three ideasFootnote 1: first, the general observation that individuals differ, and that this holds for all species; second Darwin’s empirical finding that, in the wild, most individuals die at early developmental stages or at a young age; and third, the theoretical insight that in populations of biological individuals of which each produces more than one offspring during its lifetime, not all offspring can possibly survive in the long run. Let me first recapitulate this tripartite point of departure, which provides the basis for Darwin’s empirical claim about evolutionary change, in reverse order.
The theoretical insight at the basis of the argument is that unrestricted populations increase at a geometrical ratio, i.e., they grow exponentially (Darwin 1859, pp. 47–49, 58, 79, 332), and that, because the food supply cannot grow exponentially forever, not all individuals can possibly survive. Darwin borrows this idea from the economist Robert Malthus (1798, pp. 4, 6, 7). In the third chapter of the Origin, he transfers the “doctrine of Malthus” from human social systems to “the whole animal and vegetable kingdoms” and stresses that there can be neither an artificial increase of food, nor “prudential restraint from marriage” in these kingdoms (Darwin 1859, p. 47). The situation therefore is that not all animals and plants can and will survive.Footnote 2
This theoretical result is confirmed by Darwin’s observation that plants and animals living under unfavorable circumstances leave fewer offspring (cf. next paragraph but one) and specified by the empirical finding that most individuals die at early developmental stages or at a young age and thus do not leave any offspring at all. Darwin (1859, pp. 47, 48 et pass.) points out several times that many seeds and seedlings, eggs and young are “destroyed”.Footnote 3 Food shortage is not the only reason for these deaths, although he counts it as important at least in the context of climate and seasonal changes; it is also relevant that many young individuals serve other animals as prey (p. 50).
Consequently, Darwin considers it inevitable that, in each species, many individuals die before their time—in particular, before they had a chance to propagate. This does not, however, say anything about which individuals among the young ones die and which ones survive. Survival could be a matter of chance, of intrinsic properties like body mass, strength or locomotive capability, of being the first or last born, or of any other account. Darwin prepares his answer to this question (which he does not ask explicitly) by referring to the general observation that individuals differ and that this holds for all species. Reference to variation is so important for his argument that he commences his Origin with two chapters on differences between individuals. In the first chapter, he describes variability as a phenomenon that allows breeders to form varieties of a species by selecting individuals for breeding that have traits deviating in the desired direction from other individuals. In the second chapter, he states that variation also occurs in the wild and is thus not an artifact of domestication. Darwin does not have a satisfying explanation of variation, but he tries to make its occurrence as plausible as he could by providing examples, both domesticated and in the wild. He discusses the proposals of other authors as to how variation comes about, namely that variation was induced by light, excess food, or other external factors. Darwin (1859, p. 10) himself is cautious in ascribing these factors more than a minor influence, but he considers variation, whatever its origin might be, as a matter of fact and most variation as being heritable.
The theoretical result about the overproduction of offspring, confirmed by the empirical result that there is indeed overproduction of offspring regulated by the death mainly of young individuals, leads in combination with the observation of heritable individual differences (however induced) to Darwin’s central claim that exactly those inheritable individual differences will make the difference in survival:
[A]ny variation, however slight and from whatever cause proceeding, if it be in any degree profitable to an individual of any species, in its infinitely complex relations to other organic beings and to external nature, will tend to the preservation of that individual, and will generally be inherited by its offspring. The offspring, also, will thus have a better chance of surviving. (Darwin 1859, p. 46, emphasis added)
So Darwin does not consider the inheritable difference as such as making the difference in survival. Relevant is whether a variation is profitable for the individual in how it can deal with the external world. (Eyes do not help very much in the dark, and a high body mass not on an island with restricted food supply in absence of predators.)
The quote given above is followed by the introduction of the term ‘natural selection’: “I have called this principle, by which each slight variation, if useful, is preserved, by the term of Natural Selection, in order to mark its relation to man’s power of selection” (p. 46). Darwin conceives this process as being burdened with uncertainty:
[I]f variations useful to any organic being do occur, assuredly individuals thus characterised will have the best chance of being preserved […] and […] tend to produce offspring similarly characterised. (Darwin 1859, p. 92, emphasis added)
Which individuals survive is essentially the outcome of a causal process. Unknown causal factors and/or chance merely impose a (probabilistic) weakening on the causal connection between survival and the “profitability” or “usefulness” of a certain variation in a particular environment.Footnote 4
The persuasiveness of Darwin’s claim depends on how convincingly individual differences are demonstrated to be linked to survival. Darwin conceives the link as consisting in the effects of a varying match between the individual’s traits and its environment, framed in terms of an economy of nature (Ospovat 1979; Hodge 2009)Footnote 5: Survival is supported by those variations of traits that are, as quoted above, “profitable” for the individual “in its infinitely complex relations to other organic beings and to external nature”—that is, by variations that allow the individual to cope better with its biotic and abiotic environment. In the definition, this is abridged as “being useful.” Stripping the economic metaphor of its teleological content, Haeckel introduced the concept of ecology (Haeckel 1866); sometimes he explicitly took up the concept of an economy of organisms (vol. 1, p. 8) or of nature in his definition (Haeckel 1868, p. 539). So, from the present point of view, natural selection and its reference to the biotic and abiotic environment, which is understood as being more or less constant, can be seen as an ecological concept (cf. Bouchard 2011).
Natural selection on the basis of the match of the organism with the environment gains its evolutionary relevance only under two assumptions: first, the assumption of the heritability of variation, which is supported in later chapters of the Origin with a plethora of empirical examples, and second, the idea that the range of variation is not fixed, but always centered at the actual parameter value so that the limits of variability also grow or shift with each new variant. This shift allows for organisms departing further and further from the original type, as Wallace puts it in his version of a selection theory (Wallace 1858, p. 54).
Within the framework of his economic metaphor, Darwin speaks about the profitability or usefulness of certain variations for the individual’s coping with its living conditions, which I have characterized above as the quality of the match of the individual and its environment. However, he speaks neither about a match (he uses this word only in a different sense in the context of breeding), nor does he use the term ‘environment’. Sometimes he writes about the individual or its trait as being adapted, in particular when the stabile traits of a species are at stake (Darwin 1859, pp. 2, 45, 57 et pass.). But in general, and also with respect to new variations, he speaks of the fit between an individual and other beings or external nature. He also refers to an individual or a character as being fitted to, or being fitted for, certain ends: The flying lemur’s wings are “fitted for gliding through the air” (p. 130); Darwin admires “how infinitely complex and close-fitting […] the mutual relations of all organic beings to each other and to their physical conditions of life” are (p. 59). The fitting-relation is graded, so, for example, seeds are better or less well fitted for dispersal (p. 106). Better fit, Darwin claims, gives the individual that produces these seeds an advantage over other individuals (p. 106).
Darwin uses the metaphor of being fitted already in his essays from 1842 to 1844, respectively, where he speaks about recent and fossil organisms as being “fitted to wholely different ends” (Darwin 1842/1844, p. 30) and, referring to Rhinoceroses in former times, that “some of these ancient animals were fitted to very different stations” (p. 37). He writes about species being fitted to diversified means of subsistence (p. 146), “best fitted to its new habits and station” (p. 156), and for being “fitted to widely different ends in the economy of nature” (p. 160). He uses also negations and speaks of organisms being unfit for a new climate regime (p. 173) or being ill-fitted (Darwin 1859, p. 261).
To stay close to the terms Darwin uses and at the same time to disambiguate his use of “being fitted,” I call the degree of match, of being fitted to the biotic and abiotic environment, the fittedness of an individual.Footnote 6 Darwin’s notion of a trait being fitted to ends or to habits, on the other hand, refers to how well the trait under consideration can perform its task. Such tasks are mirrored by the functional organization of an organism and their performance depends also on the environment. A trait being fitted in this other sense is thus a matter of its functioning. The fittedness of an organism obviously depends, though in a non-trivial way, on how well its traits are fitted; on how well it’s whole set of traits performs in the actual environment.Footnote 7
Focusing fittedness is very much in line with Stephen Jay Gould’s claim that “criteria of fitness independent of survival can be applied to nature and have been used consistently by biologists” (Gould 1976, p. 100). It disentangles the two components intermingled in his somehow misleading reference to “criteria of fitness”: the smoothness of the interaction of the organism with its environment (fittedness), which belongs to what Gould calls ‘design’, and their claimed connection to fitness (see below “The two faces of fitness proxies” Section).
A change in fittedness has consequences. Darwin (1859, p. 67) points out that an increase of fit increases the “chance of surviving and of leaving offspring”. So, having “fitted” traits is what makes the difference with respect to survival. The better fitting individual (or, analogously, species) has greater chances of leaving offspring than the less well-fitted individual (or species), which runs a greater risk of dying too early in life to leave progeny. Under the presupposed heritability of variation—and when above the inherited characteristics also new variation occurs in the offspring—natural selection leads to a gradual improvement of fittedness in a given environment and to regaining fittedness after a change in the environment. So fittedness has an important explanatory role: differences in fittedness explain differences of (the chance of) leaving offspring.
According to this reconstruction, we have a two-step mechanism that leads from variation to the number of progeny and, consequently, a two-step explanation. Step one: Variation of traits modifies the capabilities and thus the fittedness of an organism. Step two: the individual with higher fittedness leaves more surviving offspring. Under the empirically supported assumption that, by and large, the progeny inherits the traits of the ancestors, re-iteration of these two steps yields the evolutionary result of natural selection.
That fittedness of the individual is a cause of, or at least a predictor for, differences in the survival of its lineage and the basis for gradual changes of a species is a strong empirical claim. It could easily turn out to be empirically wrong, either generally or for some species, and in the latter case, either in all settings or in some particular situations only. It might well be that, in some species, individuals that fit physiologically almost perfectly into their environment have fewer offspring than individuals with lower fittedness. One can think of manifold reasons in behavior and in physiology. The individuals might, for example, be too lazy or too busy to build nests, not engage in brood care, be unattractive to possible mates, be themselves too picky in choosing mates, or they might have a less functional reproductive system or even be sterile.Footnote 8 It is also not very likely that fittedness, which depends on a large set of parameters (of which many will be quite unstable), is a parameter that could be determined with such high precision that one could indeed order individuals unambiguously according to their fittedness. Anyway, the estimation of fittedness needs to take into account that there is a sophisticated interaction between different traits (Pistón et al. 2019). Nevertheless, Darwin has developed a highly plausible explanatory scheme and shows that it can be applied fruitfully in many cases.