In children experiencing pain, the study of the social context of facial expressions might help to evaluate evolutionary and conditioning hypotheses of behavioural development. Social motivations and influences may be complex, as seen in studies of children having their ears pierced, and in studies of everyday pain in children. A study of opposing predictions of the long-term effects of parental caregiving is suggested.

According to Williams, human facially expressed pain, and its perception by conspecifics, is generated by evolved mechanisms. We argue that a key variable – sex (male, female) – needs to be considered for a complete theory of pain expression and perception. To illustrate, we cite findings on sex differences in pain and pain perception, and in crying and crying responsiveness.

The experience of pain appears to be associated, from early infancy and across pain stimuli, with a consistent facial expression in humans. A social function is proposed for this: the communication of pain and the need for help to observers, to whom information about danger is of value, and who may provide help within a kin or cooperative relationship. Some commentators have asserted that the evidence is insufficient to account for the consistency of the face, as judged by technical means or in the perceptions of observers, or that facial expression is epiphenomenal to a gross behavioural defensive response to pain. The major criticism is that it is unnecessary to invoke evolutionary mechanisms beyond the emergence of an unconditioned facial response to pain in neonates, subsequently shaped and maintained by instrumental and social reinforcement throughout life. These criticisms are addressed, acknowledging the need for further data to address some, and elaborating the areas in which evolutionary and operant mechanisms would predict different behavioural interactions, rather than acting synergistically. Several supportive commentaries propose extending evolutionarily-based hypotheses to sex differences, the complexities of others' responses within the social relationship, and the role of empathy. A number of commentators provided valuable suggestions for experimental paradigms or methodological issues. Overall, addressing these issues indicates the need for further conceptual development and for collection of data specifically in relation to these hypotheses.

The authors contributed equally to this paper. Order of authorship was determined alphabetically. Correspondence may be addressed to any of the authors.Adaptationism is a research strategy that seeks to identify adaptations and the specific selective forces that drove their evolution 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 functions, 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 adaptations 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 adaptationist hypotheses. Thus, we argue that the testing of alternatives requires the consideration, testing, and systematic rejection of adaptationist hypotheses. Where possible, we illustrate our points with examples taken from human behavior and cognition.

Strong adaptationists would explain complex organic designs as specific adaptations to particular ancestral environments. Weak adaptationists don't assume that complex organic functioning represents evolutionary design in the sense of niche-specific adaptation. For some domain-specific competencies (folkbiology) strong adaptationism is useful, not necessary. With group-level belief systems (religion), strong adaptationism can become spurious pseudo-adaptationism. In other cases (language), weak adaptationism proves productive.

In addition to ensuring that appropriate standards of evidence are employed when attempting to identify adaptations, researchers should investigate all nonevolutionary factors that could potentially explain their results. Evolutionary analyses may be undermined by alternative, non-evolutionary explanations either because not all relevant information is included in an evolutionary analysis, or because inappropriate methods incapable of detecting an adaptation are employed.

One important difference between adaptive and nonadaptive explanations can be found in the evolutionary sequence of structural and functional modifications. Phylogenetic analysis (cladistics) provides a powerful methodology for distinguishing exaptation from adaptation, by indicating whether character traits have predated, accompanied, or followed evolution of particular functions. Such analysis yields falsifiable hypotheses that can help to distinguish causal relationships from mere correlation.

Special design criteria are largely unable to discriminate between claims that specific competencies in judgements under uncertainty are a result of an adaptation for representing naturally sampled frequencies, or due only to inherent properties of such a format. Because divisions between these perspectives are thin, evidence via additional criteria are persuasive only in combination, using inference to the best available explanation.

To understand adaptation (and exaptation), a more comprehensive view of development is required: one beyond a constraining force. Developmental plasticity may be an adaptation by natural selection simultaneously favored (or sometimes in conflict) at multiple levels of biological organization (e.g., cells, individuals, groups, etc.). To understand the interrelationships between developmental plasticity and adaptive evolution I borrow heavily from West-Eberhard (2003) and Frank (1995; 1997). Developmental plasticity facilitates evolution, results in particular patterns of evolutionary change, and may produce exaptations by design rather than by chance.

There are two kinds of useful traits: adaptations, and all the others. Exaptations are just all the others. Exaptations are not for anything. Because there is such diversity in all the others, exaptation is not an explanatory concept. Its only real use is to block adaptationist excesses.

I claim that our desire to be special motivates us to suppose that if we were not God created, we must be self-created. I also claim that Stephen J Gould's claims about punctuated equilibrium, the absence of directional selection, and exaptations, when taken together, lead to kind of secular creationism. I introduce the notion of “adaptive effects” and argue that a focus on the actual physiological and psychological mechanisms that produce adaptations provides a way out of the exaptation dilemma.

Andrews et al. criticize Gould and colleagues for (1) failing to provide evidentiary criteria for accepting exaptationist alternatives to adaptationist explanations, and (2) seeing exaptations and spandrels as being far more frequent than adaptations in the evolutionary history of modern humans. I argue that the first of these criticisms is wrong, and the second reflects a bias for the classical version of Darwinian evolutionary theory, which Gould was trying to expand by proposing concepts like exaptation and spandrels.

Andrews et al. subscribe to the view that distinguishing selectionist from nonselectionist hypotheses – or, distinguishing adaptations from mere spandrels or exaptations – is important to the study of psychology. I offer three reasons for thinking that this view is false; that considerations of past selective efficacy have little to contribute to inquiry in psychology.

The aptationist program includes attempts at sorting adaptations from exaptations, and therefore requires knowledge of historical changes in biological character states (traits) and their effects or functions, particularly for nonoptimal aptations. Phylogenetic inference is a key approach for historical aspects of evolutionary hypotheses, particularly testing evolutionary scenarios, and such “tree-thinking” investigation is directly relevant to the aptationist program.

Andrews et al. present a form of instrumental adaptationism that is designed to test the hypothesis that a given trait is an adaptation. This epistemological commitment aims to make clear statements about behavioural natural kinds. The instrumental logic is sound, but it is the limits of our empirical imagination that can cause problems for theory construction.

Andrews et al. claim that Gould and Lewontin's critique of adaptationism is largely epistemological rather than ontological. In this commentary I argue that, on the contrary, the deepest part of their critique is ontological, raising concerns about the existence of the traits that are the subjects of adaptationist theorising. Andrews et al.'s failure to address this problem undermines their defence of adaptationism.

It is anthropomorphic to speak of Nature designing adaptations for a specific function, as if with conscious intent. Any effect constitutes an adaptive function if it contributes to survival and to reproduction. Natural selection is blind to what might have been the original function. Mutations arise by purest accident and are selected based on whatever fortuitous effects they might produce.

The adaptationist and exaptationist programs overlap in their need for a pluralistic approach to understanding evolutionary change, and Andrews et al. effectively illustrate the methodological confounds of these approaches. However, the current critique of adaptationism, especially in the arena of human behavior, rests on the tendency to rapidly reify adaptationist hypotheses prior to broad evidentiary consensus across relevant disciplines.

The fitness maximization standard incorrectly assumes that most adaptations have high heritablility, and it imposes the difficult requirement that correlated phenotypic and environmental contributors to reproduction be controlled for. Despite infrequently recognized problems, the special design standard is the foundation of the spectacular successes of modern medicine. It also suggests that the ancestral environment provides a window into the functioning of the brain.

Andrews et al. effectively argue that, despite prominent criticism, adaptationism can be a viable research strategy. We agree. In our complementary commentary, we discuss the neglected method of inference to the best explanation and argue that it is a valuable addition to the adaptationist's methodological practice.