In principle the application of evolutionary theory to psychological processes and behavior is not controversial; Darwin’s own writings contain speculation about the role of evolution in shaping “mental faculties.” However, the field of Evolutionary Psychology has been fiercely debated since its creation at the end of the 1980s, with criticisms ranging from methodological to ideological. It is my goal to update some conceptual and methodological criticisms of many branches of Evolutionary Psychology in light of the last few years of development in the post-genomic age of evolutionary biology and my position as an evolutionary genomicist. They are that 1. Evolutionary Psychology has an impoverished view of evolutionary biology, and 2. Evolutionary Psychology is using insufficient methodology to answer its questions (for criticisms similar to the one presented here see Lloyd & Feldman 2002 and Bolhuis et al. 2011). My hope is by shedding light on these perceived deficiencies that the field can move forward with a more solid foundation.
Understanding the logic of Evolutionary Psychology
The core principles of Evolutionary Psychology were laid out by Leda Cosmides and John Tooby most prominently in 1992, they are:
1. The brain is a physical system. It functions as a computer. Its circuits are designed to generate behavior that is appropriate to your environmental circumstances.
2. Our neural circuits were designed by natural selection to solve problems that our ancestors faced during our species’ evolutionary history.
3. Consciousness is just the tip of the iceberg; most of what goes on in your mind is hidden from you. As a result, your conscious experience can mislead you into thinking that our circuitry is simpler that it really is. Most problems that you experience as easy to solve are very difficult to solve – they require very complicated neural circuitry
4. Different neural circuits are specialized for solving different adaptive problems.
5. Our modern skulls house a stone age mind.
Evolutionary Psychologists may argue that these principles have been modified or adapted as the field progressed. I will leave that discussion aside for now and focus this critique on the second principle because I believe it has largely been left unchanged since first laid out by Cosmides and Tooby. Starting from the second principle, Evolutionary Psychology turns evidence for design and/or function into evidence of adaptation and directional natural selection.
“The concept of good design for solving an adaptive problem is important because it allows researchers to discover new mechanisms within the human mind. There is a systematic method for using theories of adaptive function and principles of good design for discovering new programs” (Tooby & Cosmides, 2005)
This logic is justified because:
“Natural selection is the only component of the evolutionary process that can introduce complex functional organization in to a species’ phenotype” (Cosmides and Tooby, 1997)
The most well known criticism of the Evolutionary Psychology program actually predates the formal explication of Evolutionary Psychology. In 1978, Harvard paleontologist Stephen J. Gould and geneticist Richard Lewontin in “The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme”. In it they argue that many evolutionary biologists were being led astray trying to explain observed functions of traits without employing all the various mechanisms of evolution and instead resorting to providing hypotheses with little evidence beyond simply being “consistent” with natural selection; more akin to storytelling than science. When an adaptive hypothesis was shown to be false it was simply replaced with another adaptive hypothesis or a claim that an adaptive explanation must exist but we don’t know it yet. Gould and Lewontin express concern that non-adaptive explanations were being ignored that could explain traits just as well, if not better, such as: genetic drift; developmental and phylogenetic constraints; non-genetic adaptations like phenotypic plasticity, or cultural practices; functions being due to how a trait is correlated with another trait that was the real target of selection; or functions of a structure that was selected for entirely different purposes.
Responses to Gould and Lewontin have been varied, but generally challenge the accusation that Evolutionary Psychology is predominately or exclusionary adaptationist and to insist the adaptive hypotheses are carefully tested and considered when studied, and often are genuinely preferable to non-adaptive explanations. Below we will explore some deficiencies in these rebuttals, especially in light of recent developments in evolutionary genomics.
Evolutionary psychology has an impoverished view of evolution
In Spandrels we can already see claims that non-adaptive processes in evolution were being de-emphasized and their capacity for design and function were overlooked around the same time that Evolutionary Psychology was being developed. This is reflected in the conceptual foundation and practice of Evolutionary Psychology. Only adaptation is mentioned in the 5 principles of Evolutionary Psychology and Cosmides and Tooby explicitly say that only natural selection can produce complex design. While the claim about adaptation and complex design is an empirical question, it is often simply taken as true by Evolutionary Psychologists. If an evolutionary psychologist wants to show that, for example, postpartum depression is an adaptation they can posit that it’s function is to inform mothers “that they are suffering or have suffered a fitness cost, which motivates them to reduce or eliminate investment in offspring under certain circumstances, and that may help them negotiate greater levels of investment from others” (Hagen 1999) or they may show preference against fluctuating facial asymmetry may have evolved because it “may signal psychological, emotional, and physiological distress” that harms fitness (Shackelford and Larsen 1997). Women wear high heels because it “alters their lumbar curvature to be closer to an evolutionarily optimal angle” (Lewis et al. 2017) supposedly increasing fitness, music evolved by sexual selection as an indicator of fitness (Miller 2000), Gossip and “negative information sharing” functions as a form of evolved intrasexual competition and mating strategy (Wyckoff et al. 2019) and men insulting their romantic partner was “designed to retain their long-term mate” (McKibbon et al. 2007). Some in the field may occasionally venture away from exclusively adaptive explanations, but it clearly seems that Evolutionary Psychology is predominately about adaptations and considers adaptations central to cognitive functions. However, in the time since Spandrels was published the appreciation of the role of non-adaptive processes has only expanded in evolutionary biology.
Work from Michael Lynch (2007) directly challenges the view that complexity requires adaptive explanations in no uncertain terms “There is no evidence at any level of biological organization that natural selection is a directional force encouraging complexity. In contrast, substantial evidence exists that a reduction in the efficiency of selection drives the evolution of genomic complexity.” Reviewing several years of his work and the work of others, Lynch describes how several aspects of genome complexity, gene structure, and genetic network interactions are largely explainable by accounting for non-adaptive processes, especially related to duplicate gene evolution, and the small effective population size in eukaryotes and the low selective cost of increased mutational target size (Lynch and Conery, 2003; Lynch 2006; 2007).
Similarly Freeling and Thomas (2006) argue that many aspects of genomic and morphological complexity arise through the biased retention of duplicate genes that is driven by a biochemical constraint to maintain stoichiometric balance of gene products from macromolecular complexes or genetic networks. The remnant duplicate genes create functional modules that can be acted upon later by adaptive or non-adaptive evolutionary processes. They describe this process as being a spandrel of changes in purifying selection and degenerative mutations. Furthermore my own work has highlighted that the biased expression, silencing, and retention of genes from one parental genome of a hybrid or polyploid is largely the result of the biochemical and biophysical consequences of pre-existing parental differences rather than adaptive processes (Bird et al. 2018;2019).
Additionally through large scale genomic datasets in humans we’ve learned much about the role of non-adaptive evolutionary processes. Jensen et al. (2018) point out that neutral processes like drift can induce complex patterns in the genome that can resemble the effects of selection when populations leave equilibrium and undergo drastic changes in size (Jensen et al. 2018). These neutral processes have been invoked to explain many genetic differences between continental populations (Hofer et al. 2009) and the prevalence of diseases in Ashkenazi Jewish populations (Risch et al. 2003; Bray et al. 2010). Morphological analysis has also found that many aspects of human phenotypic diversity in crania reflect neutral evolutionary processes (Roseman and Weaver, 2007) and even many differences between human and neanderthal crania are likely due to neutral evolutionary divergence (Weaver et al. 2007).
These results are just a small sample of the role of non-adaptive processes in the generation of genetic and phenotypic complexity and diversity. They are also in no way meant to undercut the role of adaptive evolution, often the above features interact with adaptive and non-adaptive processes to generate complex phenotypes. While they are not strictly related to behavior or psychological processes there is no reason given (in principle) why these particular phenotypes would be different. In fact many arguments against skepticism of Evolutionary Psychology insist that the brain is no different than any other biological phenotype subject to evolution. By not updating their understanding of evolutionary processes to incorporate non-adaptive sources of complexity, many in Evolutionary Psychology are overlooking important potential explanations for psychological and behavioral phenomena. It is no longer empirically tenable to insist that only selection can produce complex functional design, and to continue to do so only weakens Evolutionary Psychology.
Evolutionary psychology is methodologically insufficient to answer evolutionary questions
The methodological shortcomings of evolutionary psychology are best understood by seeing it’s divergence from evolutionary biology. With the expanded understanding of the capacity of non-adaptive evolutionary processes from Spandrels a commitment to more methodological rigor and attention to adaptationist pitfalls took place in evolutionary biology (Nielsen, 2009). In the following years several methods were developed to measure direct and indirect selection on traits (Lande, 1979; Lande and Arnold, 1983; Arnold and Wade 1984a,1984b). Lande and Arnold (1983) explicitly mention the criticisms of Lewontin and Gould as motivation for a quantitative approach to empirically studying natural selection. This practice of quantifying and modeling natural selection became widespread in evolutionary studies and enhanced our understanding of the pattern and strength of selection in the wild (Kingsolver and Hoekstra, 2001), though these methods are not without their issues (Pujol et al. 2018).
With the rapid expansion of DNA sequence data, new possibilities of testing selective hypotheses have further advanced the field of evolutionary biology (Nielsen 2005). These methods exploit the fact that selection leaves certain predictable signals in the genome like decreased genetic diversity around the selected locus, higher genetic divergence between populations that experience selection and those that didn’t, and changes in allele frequency distributions in the selected region (Barrett and Hoekstra, 2011). Other methods try to identify subtle shifts in allele frequency that reflect polygenic selection, like a positive relationship between effect size of an allele on a trait of interest and that alleles frequency (Barrett and Hoekstra, 2011). Finding regions potentially under selection requires looking for regions showing some combination of these patterns in a genome. Similarly comparative genomics approaches can aid in inferring selection between species or clades in a phylogeny, for example, by looking at shifts in the ratio of non-synonymous and synonymous substitutions (dn/ds) in orthologous genes, with ratios > 1 potentially suggestive of positive selection (Enard and Paabo, 2004; Mikkelsen et al. 2005; Ellegren, 2008). Even with these powerful methods the risk of falsely inferring selection, and especially adaptation is possible. The community has cautioned researchers that false positives for selection are possible in the presence of complex evolutionary or demographic scenarios and that claims of adaptation are best reserved for cases where connections between genotype, phenotype, and fitness have been well empirically established (Nielsen 2009; Barrett and Hoekstra, 2011). Beyond work in humans, these DNA sequence based methods and the modeling framework they allow for have revolutionised the study of domestication in plants and animals, greatly expanding our understanding of evolution and natural selection (Gerbault et al. 2014).
Evolutionary biology has spent decades since Spandrels developing and enhancing methods to model and measure natural selection, recently looking at allele frequencies directly with DNA sequencing technology. Inferring selection, let alone adaptation, from tenuous logical inferences based on circumstantial evidence for function, is far beyond the pale of what kinds of work would be publishable in mainstream evolutionary biology journals. However, much of the work in Evolutionary Psychology still follows this strategy. Very rarely if ever is selection actually measured or any genetic association to the trait of interest identified. Additionally sex differences are often attributed to sexual selection, but again empirical work is typically not done to demonstrate selection has occurred for a particular trait even though this is an open frontier in evolutionary genomics and one which may challenge assumptions about sexual selection in humans (Kasimatis et al. 2020). Likewise mate choice decisions are often discussed in terms of fitness indicators and genetic quality, though the empirical coupling is something is recognized as needing thorough and careful investigation in the animal literature (Achorn and Rosenthal. 2019)
Importantly this second criticism is independent of whether Evolutionary Psychology is exclusively or predominantly adaptationist. Even if Evolutionary Psychology regularly considers non-adaptive explanations it still needs a robust methodology to test for adaptation. Considering the extent to which we now know non-adaptive processes can produce phenotypic complexity it is important that we explicitly test for selection. Evolutionary Psychology can continue with its current methodology but this would require much more caution and humility in the kinds of conclusions drawn from data, and a recognition that the evidence present is more relevant to the nature of behaviors and their fitness consequences rather than the presence and purpose of adaptations. To speak about adaptation more refined methods that identify and measure selection are necessary. If Evolutionary Psychology wants to be an evolutionary science it is important that it meet the standards of the broader field of evolutionary biology otherwise its claims will continue to justifiably be viewed with skepticism.
Conclusion
Used properly evolutionary theory is likely to greatly aid our understanding of human behavior and psychological processes, like it has for countless other biological questions. However, this means understanding the variety of evolutionary processes that can generate genetic and phenotypic diversity be they adaptive or non-adaptive. It also means applying proper methods to the evolutionary questions. By engaging more with past and current critiques and increased collaboration and interaction with evolutionary biology, genuine progress can be made in Evolutionary Psychology to better identify adaptations or to shift attention to more likely non-adaptive causes. The goals of Evolutionary Psychology aren’t served by clinging to outdated conceptions of evolution or by resisting methodological advances in other evolutionary sciences.
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