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How ubiquitous is adaptation? A critique of the epiphenomenist program

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Abstract

It is important to distinguish adaptation per se (adaptedness, or being adapted) from the more specific concept of adaptation for some function. Commonly used criteria for adaptation in either sense have limited applicability. There are, however, a number of widely applicable criteria for adaptation per se, such as several kinds of cost, low variation, the maintenance of integration, and the fitness distribution of mutations. Application of these criteria leads to the conclusion that adaptation is overwhelmingly prevalent for features of organisms. Neither the presence nor the absence of adaptation has a privileged status in inference. Effectively neutral evolution can occur on adaptive buttes while maintaining the same degree of adaptation, but it is likely to be relatively minor.

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Notes

  1. The word ‘organism’ is unfortunately ambiguous. It sometimes refers to a particular kind (not necessarily species) of living creature. I am using it in this sense. It also can refer to an entire single individual. But the word ‘individual’ is also ambiguous, even apart from many biological problems such as clones or mosaicism. Philosophers appropriated it from biology and modified its meaning. Then, remarkably, some biologists re-imported the philosophers’ concept, with as yet unresolved confusion as a consequence. It would seem preferable for philosophers to use another word, such as ‘unit’.

  2. ‘Fitness’ is an even more ambiguous word, but any concept to which it has referred can be used here. This results in some consequent marginal ambiguity of ‘adaptation’ per se, but less so, and the arguments in the paper are robust to such variants.

  3. Consider a highly entrenched feature, say gill slits in tetrapod embryos or number of segments in the thorax of insects. Possibly such a feature’s entrenchment sometimes prevents evolution of a different and much better organism. The entrenchment with which the organism is stuck prevents access to other parts of the state space. Because of this lack of evolutionary access, the feature can not be said to be adaptive now, although it may once have been.

  4. If one nevertheless prefers to use some other terminology, my arguments can be translated into that terminology. Terms are unimportant so long as they do not mislead. Rose and Lauder (1996) and Reeve and Sherman (1993) review concepts of adaptation from different perspectives.

  5. Actually there are degrees of adaptedness, and the space of neutrality depends on effective population size, so the hypotheses are not fully disjoint. Even if they were, though, estimation is to be preferred to decision theory. Say we are seeing if we can detect selection in a particular case and we find a negative result. This does not mean that selection is absent, as per the usual interpretation, but that with some specified confidence it is not stronger than the confidence limit. It could be absent, but our evidence does not show this. Repeated negative results, as with Avery’s progressive purification of the transforming factor of ‘Pneumococcus’ to try to eliminate protein from the DNA, can give a stronger conclusion for which one’s prior expectation becomes a relatively greater factor, as generated controversy then.

  6. Parallelism is evolution in the same direction from similar and closely related species; the tendency to produce such evolution is a homologous partial constraint. Convergence is evolution to similar phenotypes from more different ancestors; it is a triumph of selection over ancestry.

  7. A coefficient of variation (standard deviation as a percent of mean) less than about ten, or perhaps even eight, is a reasonable if fuzzy threshold. Like other criteria, though, it is not perfect. For instance, the number of oocytes in mammals of the same prenatal or postnatal age is highly variable, with a coefficient of variation usually greater than 50 (Van Valen 2003). Because there is evidence in this case that the number is nontrivial selectively, with respect to both number and quality of offspring, its high variation is puzzling unless, as may be the case, most of the variation in the data comes from error of estimation.

  8. Biologists sometimes use allometric relations as evidence of nonadaptation. (‘Nonadaptive’ includes neutrality; ‘inadaptive’ does not.) But such relations are easily modified by selection, even though change may be easier along the allometric path because of developmental conservatism. For instance, the well-known allometry of brain size and body size among mammals is formed from intraspecific allometries that at least usually have lower slopes.

  9. Although the standard equation for allometry uses the slope and Y intercept as parameters, selection clearly occurs on the centroid of the distribution rather than on the intercept.

  10. Hawks et al. (2007) have found a large acceleration in human adaptive evolution, at the DNA level, in the past 50,000 years or so, including geographic differentiation. A greatly increasing number of Homo sapiens produce a greatly increasing absolute number of potentially favorable mutations. However, their methods permit only rather weak inference as to most of the specific phenotypic causes.

  11. Not all the general criteria apply in potential cases of phenotypic adaptive buttes. However, variation and integration are still useful. Because the top of an adaptive butte has the same fitness everywhere, there is no selection against variants that remain on the butte. Therefore there is no selective resistance to the variation of each population expanding until it occupies more or less the whole surface of the butte. The means of the populations may still differ, but their distributions have about the same limits. Even if this does not happen, perhaps because of constraints, the distributions can be expected to have greater than usual variation.

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Acknowledgments

This paper is a revision of a talk I gave in 2003 at a symposium on the spandrels, at Duke University. I thank Dan McShea for the invitation, and the participants (especially Dan) and two referees for their comments.

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  1. Department of Ecology and Evolution, University of Chicago, 1101 E. 57 St., Chicago, Illinois, 60637, USA

    Leigh Van Valen

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Van Valen, L. How ubiquitous is adaptation? A critique of the epiphenomenist program. Biol Philos 24, 267–280 (2009). https://doi.org/10.1007/s10539-008-9142-x

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