The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme

Abstract

An adaptationist programme has dominated evolutionary thought in England and the United States during the past 40 years. It is based on faith in the power of natural selection as an optimizing agent. It proceeds by breaking an organism into unitary ‘traits’ and proposing an adaptive story for each considered separately. Trade-offs among competing selective demands exert the only brake upon perfection; non-optimality is thereby rendered as a result of adaptation as well. We criticize this approach and attempt to reassert a competing notion (long popular in continental Europe) that organisms must be analysed as integrated wholes, with Baupläne so constrained by phyletic heritage, pathways of development and general architecture that the constraints themselves become more interesting and more important in delimiting pathways of change than the selective force that may mediate change when it occurs. We fault the adaptationist programme for its failure to distinguish current utility from reasons for origin (male tyrannosaurs may have used their diminutive front legs to titillate female partners, but this will not explain why they got so small); for its unwillingness to consider alternatives to adaptive stories; for its reliance upon plausibility alone as a criterion for accepting speculative tales; and for its failure to consider adequately such competing themes as random fixation of alleles, production of non-adaptive structures by developmental correlation with selected features (allometry, pleiotropy, material compensation, mechanically forced correlation), the separability of adaptation and selection, multiple adaptive peaks, and current utility as an epiphenomenon of non-adaptive structures. We support Darwin’s own pluralistic approach to identifying the agents of evolutionary change.

The biology and evolution of music: A comparative perspective

“…As stressed by (Williams, 1966) in his foundational work, adaptation is an ''onerous concept'' to be demonstrated, not assumed. Despite the caricature of ''Panglossian adaptationists'' painted by Gould and Lewontin (1979), evolutionary biologists since Darwin have recognized that there are always some traits in any species that are non-adaptive (the vestigial appendix of humans being one classic example). Similarly, one answer to DarwinÕs quandary about the value of music may be that music is a byproduct of some other capacity such as language, but is not specifically adaptive in itself.…”

“…Similarly, one answer to DarwinÕs quandary about the value of music may be that music is a byproduct of some other capacity such as language, but is not specifically adaptive in itself. Such traits have been dubbed ''spandrels'' (Gould & Lewontin, 1979), borrowing an architectural term for a necessary but non-functional concomitant of a primary load-bearing function. Given the negative character of this hypothesis, if musical is a spandrel, the fastest way to find out is by positing adaptive hypotheses and then rejecting them one by one.…”

The capacity for music: What is it, and what’s special about it?

“…But whatever one may imagine about language, by comparison we find far less compelling the imaginable pressures that would favor the evolution of a narrow musical capacity (not that the literature lacks hypotheses, e.g., Cross, 2003;Huron, 2003; many papers in Wallin, Merker, & Brown, 2000). All else being equal, it is desirable, because it assumes less, to explain as much of the musical capacity as possible in terms of broader capacities, i.e., to treat the music capacity as an only slightly elaborated ''spandrel'' in the sense of Gould and Lewontin (1979). The difficulty is: a ''spandrel '' of what? However, the issue is not purely the desirability of accounting for the musical capacity in terms of other, more evolutionarily plausible components of cognition.…”

On the Possibility of Constructive Neutral Evolution

“…In some cases it may seem more felicitous to refer to "buffering," "tolerance," or "unrealized potential" than to "excess capacity," but the choice of words is not as important as the concept (as defined generically above), which is widely invoked in discussions of evolutionary novelty, as by Galis (1996), who refers to "excess structural capacity" in describing the evolution of musculoskeletal systems (see also Frazetta 1975), and by Gould and Lewontin (1979) in the concept of "spandrel" or Gould and Vrba (1982) in the concept of "preaptation," and in the "tolerance" invoked by Dover (1992). Multiple examples of innovations based on the coopting of "spandrels" or "preaptations" have been given recently (Armbruster 1996;Gould 1997).…”

“…Attributes Y and Z, considered in isolation, may be neutral sensu stricto or deleterious (though any deleterious effect of Y and Z will not have outweighed the advantage of X). The concepts of allometry and "spandrels" (Gould and Lewontin 1979), as well as many invocations of "developmental constraints" (Maynard Smith et al 1985), are based on this implication of pleiotropy, which might be thought of as "developmental hitchhiking." Occasionally, pleiotropic effects are seen explicitly as an alternative to random fixation as a mechanism of "neutral" change (e.g., as discussed by Nei 1987, p 387).…”