Abstract
Biological adaptations appear designed for a purpose, and so they result from a “creative process” almost by definition. Traditional evolutionary theory assigns a special role in this process to natural selection, with theorists invoking selection both to explain the appearance of purpose, and to predict what the purpose of adaptations will be. At the same time, traditional theory recognizes that many other factors might influence the evolution of adaptations. These factors might, for example, increase evolvability and accelerate adaptation, or bias evolution towards a subset of the possible adaptive outcomes. Such factors are also creative in a sense, but not in the same sense as natural selection. Challenges to traditional theory have sometimes championed organisms as a neglected source of creativity in evolution. This could be interpreted as the radical claim that non-human organisms—like people—are novel sources of purpose in nature, generating apparently designed outcomes that are not directed at reproductive success. But it might also be interpreted as the uncontroversial claim that organisms—like many other things—sometimes act in a way that accelerates adaptation or makes some adaptive outcomes more probable than others. Ambiguity about their claims has led to theories attracting unwarranted enthusiasm and unwarranted scepticism, and distracts us from the criteria by which the theories should be judged.
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Notes
- 1.
The main alternative topic would be speciation, such that “creative factors” lead to the origin of new species. But this cannot be natural selection’s uniquely creative role, because biologists have long recognized that speciation can occur in lots of different ways (see, e.g., Mayr 2001). With speciation, as with evolvability (§5.3.1.1), a major challenge is to determine the relative importance of the different factors; and as with evolvability too, another major challenge may be to explain why speciation is so slow (e.g., Felsenstein 1981; Barton 2020; §5.3.1.2).
- 2.
This is why “traditional thinking” will not be identified with any single historical period. “The Modern Synthesis” is, moreover, very variously and often unhelpfully characterized, sometimes as a quasi-mythical event, like the Dissociation of Sensibility, and sometimes as a shorthand for a strict set of tenets, difficult to identify with any actual scientists. These are historical idealizations as bold as any found in population genetics.
- 3.
Darwin, for example, found it “difficult to imagine that eyes, although useless, could be in any way injurious to animals living in darkness” (1859: 137; see also Weismann 1889: 86), and the fitness benefits of eye loss remain hypothetical. Anderson (1893) speculated that eyes might be “exposed to injury, destructive inflammation, and the attacks of parasites”, while Protas et al. (2007) called attention to the metabolic and energetic cost of eye maintenance (Young 1971; Linsenmeier and Braun 1992); these costs increase in perpetual darkness (Kimble et al. 1980; Wangsa-Wirawan and Linsenmeier 2003), and may be at a particular premium for teleost fish (Damsgaard et al. 2020), and in caves (Simon et al. 2017).
- 4.
Of course, much scientific effort has been devoted to refining and formalizing Darwin’s claim (e.g., Hamilton 1964), and the version quoted is potentially misleading (oak galls, for example, are part of oaks, but form for the exclusive good of wasps).
- 5.
The role of drift in quantitative genetics is easy to miss because the modelling tracks phenotypic distributions instead of allele frequencies (e.g., Walsh and Lynch 2018), but when the genotype-to-phenotype map is sufficiently complex, selection on single alleles will often be weak, so that many allelic substitutions are driven by drift (Frank 2013: 55; Barton 2017: 98, 104). Quantitative genetic theory allows us to model evolution when the map is arbitrarily complex (Fisher 1918; Barton 2017: 96; Barton et al. 2017), although this point is also obscured when the theory is identified with its first-order approximations like the Breeder’s Equation.
- 6.
Bergson, for example, proposed his theory of “Creative Evolution” because “adaptation explains the sinuosities of the movement of evolution, but not its general directions” (Bergson 1907/1998: 102). Simpson (1949, Ch. 11) argued that most of the non-illusory trends were adaptive; although for Simpson this implied that “orientation in evolution is not determined solely by some characteristic within the evolving organisms or solely by external factors in their environments, but by both and by interplay between the two” (1949: 142; see also 149–50).
- 7.
Note that Wright himself, unlike the authors cited, did not call drift creative (e.g., Wright 1980), confirming that the word is used in different ways.
- 8.
A variety of results have questioned whether drift is required for peak shifts—especially when selection pressures vary in space and time (Wright 1931: 167; Fisher and Ford 1950; Weatherhead 1986; Williams 1992, Ch. 4; Price et al. 1993; Whitlock 1997; Weinreich and Chao 2005; Whibley et al. 2006; Bell 2010). And while many populations are spatially subdivided (Provine 1986: 270; Harrison and Taylor 1997; Yang et al. 2019), there is no evidence that levels of drift match the “sweet spot” required to maximize evolvability (Coyne et al. 1997; Barton 2017), or have any tendency to evolve in that direction (e.g., Peck 1992). Nor is there evidence that large well-mixed populations are conspicuously maladapted. Regarding mutational biases, a range of different results suggest that adaptation might not be limited by the rate of beneficial mutation (e.g. because frequent beneficial substitutions can interfere with one another; Weissman and Barton 2012; but see also Wright 1932; Maynard Smith 1976; Maynard Smith et al. 1991; Arnold 1996; Schluter 2000; Welch and Jiggins 2014; Rousselle et al. 2020; Barton 2020). Other work has shown that decreasing the severity of deleterious mutations might lead to extinction, because weakly deleterious mutations persist for longer (Gabriel et al. 1993; see also Kondrashov 1988). Biases that make beneficial mutations more likely, or deleterious mutations less severe, need not, therefore, lead to substantial increases in evolvability. It is important to note that none of these arguments is conclusive. The decisive measurements—on real-world fitness landscapes, or levels of maladaptation relative to some hypothetical optimal kind—remain very difficult (Maynard Smith 1978; Williams 1992, Chs. 4, 9 and 10; Crespi 2000; Hereford et al. 2004; Kaznatcheev 2019); and there is still no consensus about the relative contributions to adaptation of large- and small-effect mutations (Simpson 1947: 494-5; Bell 2010; Rockman 2012; Boyle et al. 2017; Barton 2017: 105-6; Barghi et al. 2020). In addition, some developmental biases are difficult to quantify, while others, like “key innovations”, evolved only once (Williams 1992: 35); so unlike with sex and recombination, we cannot use natural or induced variation to perform tests.
- 9.
- 10.
Overall mutation rates, like recombination rates, are the subject of a generalised reduction principle (e.g., Altenberg et al. 2017), but unlike recombination rates, there is no evidence that mutation rates can be reduced to zero, especially in stressful conditions, when all sorts of biological functions are poorly performed.
- 11.
Of the four bases in DNA, C and T are pyrimidines with a single ring, while A and G are purines with two rings. Transition substitutions are pyrimidine-to-pyrimidine or purine-to-purine, and so conserve the number of rings, while transversions change the number of rings. There are twice as many possible transversions as transitions, allowing us to define a “surprising” overrepresentation of transitions.
- 12.
Note, however, that the controls used by Payne et al. (2019), involving neutral sites and the redundancy of the genetic code, are rarely available for other types of mutational or developmental bias.
- 13.
This view is culturally specific (e.g., Niu and Sternberg 2006), but it does seem to be the relevant one for debates about evolutionary theory.
- 14.
Waddington’s major complaint about population genetics seems to have been its failure to mention things explicitly (so there is “no explicit mention of the phenotype”, “no hint that phenotypes can be affected by environments”, and “no mention of the fact that the effect of a given gene is influenced by the rest of the genotype” 1969/2008: 259). Of course, mentioning things explicitly is not always a theoretical virtue (Gilbert 1994: 153; Strevens 2008) and in any case, all these things are mentioned explicitly in standard quantitative genetics (Fisher 1918; Hill and Kirkpatrick 2010; Walsh and Lynch 2018).
- 15.
Assessing the importance of plasticity to evolvability is difficult for some unique reasons (e.g. Lewontin 1985). How should the benefits of plasticity in a given trait be weighed against the benefits arising from most other traits being stably expressed? And how should we deal with the fact that much adaptive plasticity aims precisely at stabilizing other aspects of the phenotype?
- 16.
Waddington also claimed that his theory—like sexual selection before and kin selection after—explained a whole new class of adaptations; but these were “pseudo-exogenous adaptations”—which look like physiological adaptations but aren’t—and so are not distinguished by a characteristic type of function (Waddington 1953b: 134; Simpson 1953: 113).
- 17.
- 18.
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Acknowledgments
I am very grateful to Tom and Ben Dickins for giving me the excuse and space to think about this topic. I am very grateful too for helpful comments on earlier drafts, including from Ben Dickins, Mitchell Distin, David Haig, Hilde Schneemann, Raphael Scholl, and Lucy Weinert. Special thanks are due to Tobias Uller, whose detailed comments tidied up some of the sloppiest thinking, and to Jean-Baptiste Grodwohl, who would be co-author were he not so fastidious. Finally, I am grateful in a deeper way to Alain Welch, to whose memory I dedicate this chapter.
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Welch, J.J. (2023). The Creativity of Natural Selection and the Creativity of Organisms: Their Roles in Traditional Evolutionary Theory and Some Proposed Extensions. In: Dickins, T.E., Dickins, B.J. (eds) Evolutionary Biology: Contemporary and Historical Reflections Upon Core Theory. Evolutionary Biology – New Perspectives on Its Development, vol 6. Springer, Cham. https://doi.org/10.1007/978-3-031-22028-9_5
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