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Adaptationism – How to Carry out an Exaptationist Program1 BEHAVIORAL AND BRAIN SCIENCES (2002) 25, 489–553 Printed in the United States of America Adaptationism – how to carry out an exaptationist program1 Paul W. Andrews, Steven W. Gangestad, and Dan Matthews Department of Psychology, University of New Mexico, Albuquerque, NM 87131. {pandrews; sgangest; danda}@unm.edu Abstract: Adaptationism is a research strategy that seeks to identify adaptations and the specific selective forces that drove their evolu- tion in past environments. Since the mid-1970s, paleontologist Stephen J. Gould and geneticist Richard Lewontin have been critical of adaptationism, especially as applied toward understanding human behavior and cognition. Perhaps the most prominent criticism they made was that adaptationist explanations were analogous to Rudyard Kipling’s Just So Stories (outlandish explanations for questions such as how the elephant got its trunk). Since storytelling (through the generation of hypotheses and the making of inferences) is an inherent part of science, the criticism refers to the acceptance of stories without sufficient empirical evidence. In particular, Gould, Lewontin, and their colleagues argue that adaptationists often use inappropriate evidentiary standards for identifying adaptations and their func- tions, and that they often fail to consider alternative hypotheses to adaptation. Playing prominently in both of these criticisms are the concepts of constraint, spandrel, and exaptation. In this article we discuss the standards of evidence that could be used to identify adap- tations and when and how they may be appropriately used. Moreover, building an empirical case that certain features of a trait are best explained by exaptation, spandrel, or constraint requires demonstrating that the trait’s features cannot be better accounted for by adap- tationist hypotheses. Thus, we argue that the testing of alternatives requires the consideration, testing, and systematic rejection of adap- tationist hypotheses. Where possible, we illustrate our points with examples taken from human behavior and cognition. Keywords: adaptation; ADHD; brain allometry; constraint; epistemology; evolutionary psychology; exaptation; female orgasm; opti- mization; special design; waist-hip ratio (WHR) 1. Introduction Jay Gould and geneticist Richard Lewontin (e.g., Gould & Lewontin 1979; Lewontin 1978; 1979). Perhaps the most In the past decade, evolutionary psychology has emerged as prominent criticism they made was that the explanations an important theoretical perspective in psychology. Evolu- that adaptationists gave for traits were analogous to Rud- tionary psychology is a methodologically rich field that could yard Kipling’s Just So Stories (outlandish explanations for be applied to a variety of interesting questions (e.g., phylo- questions such as how the elephant got its trunk). Of genetic analysis of psychological and behavioral traits). One course, the criticism is not against storytelling in science per approach receiving much attention in recent years pre- se. The generation of hypotheses and the making of infer- dominantly involves the application of adaptationism to ences is an inherent part of science. Rather, the criticism understanding the evolution and nature of human psycho- refers to the acceptance of stories without sufficient em- logical design (Barkow et al. 1992; Buss 1995; Ciba Foun- pirical evidence. Gould, Lewontin, and their colleagues dation 1997; Pinker 1997a). Adaptationism, as a research have made two important epistemological criticisms of the strategy, seeks to identify adaptations and to elucidate the story telling that adaptationists do. First, adaptationists of- specific selection pressures that forged them in an organ- ten use inappropriate evidentiary standards for identifying ism’s evolutionary past. It has a long history within evolu- adaptations and their functions. Second, adaptationists of- tionary biology that, in its current form, crystallized in the ten fail to consider alternative hypotheses to adaptation. 1960s and 1970s (particularly influenced by the writings of Many have responded to the criticisms of Gould and George Williams 1966) and now dominates the study of an- Lewontin (e.g., Alcock 1987; 1998; Alexander 1987; Borgia imal behavior in biology (e.g., Krebs & Davies 1993; 1997). 1994; Buss et al. 1998; Cronin 1993; Dawkins 1986; Dennett Adaptationists sometimes implement optimization models 1995; 1997; Houston 1997; Maynard Smith 1978; 1995; Mayr (formal mathematical theories of selection pressures) to de- 1983; Parker & Maynard Smith 1990; Pinker 1997b; Pinker cide whether a particular design serves some specific func- & Bloom 1992; Reeve & Sherman 1993; Sherman 1988; tion (e.g., Parker & Maynard Smith 1990). Perhaps as of- 1989; Thornhill 1990; Thornhill & Palmer 2000; Tooby & ten, however, they use intuitive arguments for how a Cosmides 1992; Wright 1997) and Gould has responded to particular feature must have served a goal responsible for at least some of these arguments (e.g., Gould 1997a; 1997b; its evolution (Williams 1966). 1997c; 1997d). Most recently, the debate between Gould and Everyone agrees that organisms have adaptations. Yet, adaptationists has been carried to outlets intended for the lay adaptationism as a research strategy has not enjoyed con- public, including exchanges about evolutionary psychology in sensual affection within evolutionary biology. In the 1970s, the New York Review of Books (Dennett 1997; Gould 1997a; it became the target of criticisms by paleontologist Stephen 1997b; 1997c; 1997d; Pinker 1997b; Wright 1997). Despite Downloaded© 2002 from https://www.cambridge.org/coreCambridge University Press. University 0140-525X/02 of Minnesota $12.50 Libraries, on 27 Nov 2018 at 03:01:10, subject to the Cambridge Core terms of use, available at 489 https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0140525X02520094 Andrews et al.: Adaptationism – how to carry out an exaptationist program emerging nearly a quarter-century ago, these debates persist selection that it is difficult to infer selective history with the with no consensual resolution (though each side appears to use of traditional adaptionist tools. Thus, we also discuss the think matters have resolved in their favor). Few debates are ways in which even the best adaptationist evidentiary stan- more central to evolutionary biology and, in particular, evo- dards can fail to identify adaptation (sect. 4). In the last ma- lutionary psychology – the arena in which skirmishes have jor section (sect. 5), we note that problems with storytelling most recently been staged. Our purpose is not to review the are not unique to adaptationism. Gould and Lewontin in- entire literature on this debate. Rather, some confusion sist that adaptationists consider alternative hypotheses, but about the nature of the debate persists, and we attempt to they have not provided any evidentiary criteria for accept- clarify the major issues. In particular, the major criticisms of ing the alternatives that they ask adaptationists to consider. adaptationism advanced by Gould and Lewontin have been In the absence of rigorous evidentiary standards, exapta- largely epistemological in nature, rather than ontological; a tionist story telling is “Just So” storytelling. We argue that point not always appreciated. an adaptationist approach is crucial to providing empirical By way of background, we first discuss traits and how support for the alternative hypotheses about trait design they evolve (sect. 2). Next, we discuss the primary goal of that Gould, Lewontin, and their colleagues insist should be adaptationism – to determine whether traits are adapta- considered. Where possible, we illustrate our points with tions; and, if so, to determine the specific selection pres- examples about human behavior and cognition. sures that shaped them (sect. 3). In this section we also dis- cuss problems with different standards that adaptationists 2. The effects of traits and how they influence could use (and sometimes have used) to classify traits as trait evolution adaptations and make inferences about the specific selec- tive forces that shaped them, especially in light of the crit- Biologists use the term “trait” to refer to aspects of organ- icisms made by Gould and Lewontin. Playing prominently isms’ phenotypes. The question of what qualifies as a trait is in these criticisms, are the concepts of constraint and exap- not so straightforwardly answered as it might seem, a point tation. A constraint opposes the modifying influence of se- emphasized by Gould and Lewontin (1979). Because all as- lection on the phenotype, whereas an exaptation is a pre- pects of the organism’s phenotype are integrated with one existing trait that acquires a new beneficial effect without another, organisms are “not collections of discrete objects” modification to the phenotype by selection. To Gould and (Gould & Lewontin 1979). Genes often have pleio-tropic ef- his colleagues, constraint and exaptation are so prevalent in fects (i.e., a single gene may influence many aspects of the organism’s phenotype) and they often epistatically interact with each other (i.e., an allele at one locus may influence the phenotypic expression of an allele at another locus). Paul W. Andrews is currently a post-doctoral fellow in Nevertheless, biologists interested in how an organism’s the Department of Psychology at the University of New phenotype evolved are forced to discriminate between as- Mexico. He received a B.S. (Aerospace Engineering)
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