“… functional information does not ‘validate’ claims of selection. It mostly serves to provide a more interesting and entertaining story. In humans, where controlled experiments and measurements of fitness are difficult or impossible to obtain, the evidence for selection must come directly from the genetic data.”
— Nielsen (Reference Nielsen2009)
In their target article, Mehr et al. propose a theory of musical adaption as credible signaling, citing a breadth of evidence that spans the disciplines of anthropology, developmental psychology, and comparative psychology. Underlying their claim is the belief that establishing adaptations for music requires unequivocal evidence for the functional design of music. Writing on “what constitutes evidence for adaption” (sect. 2), the authors opine that “a successful account of music must provide evidence for the design of its principal features” (sect. 3, para. 1) and that “supporting a claim of adaptation therefore requires evidence for design.” (sect. 2, para. 8). Music, in their view, fulfills these criteria and “… exhibits design features consistent with adaptations for credible signaling, which give rise to a universal human psychology of music” (sect. 5.3, para. 2).
Although the authors put forth a well-reasoned perspective on the adaptive origins of music in credible signaling, we believe the authors err in presuming that evidence for design is a tenable basis upon which to infer adaptations for music. Criticisms regarding the inadequacy of appealing to design for adaptive theorizing are certainly not new and have historically been aimed at the adaptationist program, more generally (Gould & Lewontin, Reference Gould and Lewontin1979). These criticisms have highlighted that evolutionary theorists have a tendency to conflate design and adaptation (Nielsen, Reference Nielsen2009), while ignoring or underestimating the role of non-adaptive, evolutionary processes (Jensen et al., Reference Jensen, Payseur, Stephan, Aquadro, Lynch, Charlesworth and Charlesworth2019) that can produce organismal complexity (Lynch, Reference Lynch2007).
Alongside these criticisms against the adaptationist program and the growing appreciation of non-adaptive processes in evolution, methodological improvements in the evolutionary and biological sciences have helped move the scientific paradigm for identifying adaptations beyond simple appeals to design. Innovations in evolutionary biology, population genetics, and comparative genomics, for instance, have produced a systematic framework for testing for selection, and, by extension, for testing for adaptations by natural selection. Over several decades, quantitative approaches to evolutionary biology have yielded a suite of statistical tests that detect signatures of selection at the level of the genome (Nei, Suzuki, & Nozawa, Reference Nei, Suzuki and Nozawa2010; Nielsen, Reference Nielsen2005). Using these techniques, population-genetic and comparative-genomic analyses have successfully identified selection at the local and global levels. For example, local selection can be detected based on patterns of excessive population differentiation (e.g., Fst) or by patterns of haplotype structure and linkage disequilibrium (Nei et al., Reference Nei, Suzuki and Nozawa2010). Similarly, global selection is indicated by elevated rates of non-synonymous (Ka) substitutions compared to synonymous substitutions (Ks) (Clark et al., Reference Clark, Glanowski, Nielsen, Thomas, Kejariwal and Todd2003) or by a heighted ratio of non-synonymous and synonymous substitutions between species (Ka/Ks), relative to the ratio of non-synonymous and synonymous polymorphisms within a species (Pn/Ps) (McDonald & Kreitman, Reference McDonald and Kreitman1991). Moreover, lineage-specific gene duplications and expansions of gene families (Demuth & Hahn, Reference Demuth and Hahn2009) can be investigated in comparative frameworks to test for positive selection at the global level (Hahn, De Bie, Stajich, Nguyen, & Cristianini, Reference Hahn, De Bie, Stajich, Nguyen and Cristianini2005). These techniques can even be expanded to study the evolution of higher order features of the genome, such as changes in gene-coexpression networks (Oldham, Horvath, & Geschwind, Reference Oldham, Horvath and Geschwind2006).
Once identified, genomic signatures of selection can, then, be related to traits proposed to be functional, providing an initial foundation for identifying adaptations. However, simply associating molecular signals of selection with a trait posited to have adaptive origins can still produce erroneous conclusions about adaptation. Associations between genetic signals of selection, although possibly reflecting an adaptive effect, could also reflect pleiotropic effects (Nielsen, Reference Nielsen2009). To rule out pleiotropic effects, among other confounds, evolutionary biologists have developed an integrated framework that combines observational, field, and experimental methodologies to study adaptations in a number of organisms. It is only after arriving at a robust understanding of the underlying pathways between the genome, the phenotype, and fitness of the trait under question, using this integrated framework, can conclusions about adaptations confidently be drawn (Barrett & Hoekstra, Reference Barrett and Hoekstra2011).
Thus, even with the remarkable methodological progress in the evolutionary and biological sciences, producing unequivocal evidence of selection, and further, adaptation, is extremely difficult, as it requires a mechanistic understanding of the functional links between the genome, the phenotype, and the fitness of the trait under study (Barrett & Hoekstra, Reference Barrett and Hoekstra2011). To this end, unraveling the evolution of music may seem like an insurmountable undertaking. Already, however, the methods described above have helped illuminate the evolution of language in humans (Fisher, Reference Fisher2017; Fitch, Huber, & Bugnyar, Reference Fitch, Huber and Bugnyar2010), echolocation in bats (Zhang et al., Reference Zhang, Cowled, Shi, Huang, Bishop-Lilly, Fang and Wang2013), and the evolution of song and vocal learning in birds (Zhang et al., Reference Zhang, Li, Li, Li, Larkin, Lee and Wang2014). A similar framework could be adopted to probe adaptive hypotheses of music, particularly at the global level, as music is considered a human universal (Mehr et al., Reference Mehr, Singh, Knox, Ketter, Pickens-Jones, Atwood and Glowacki2019). For example, comparative studies could investigate selection related to music by studying the evolution of genes associated with music and musical ability across the mammalian phylogeny. Candidates for this analysis could include genes associated with music-related disorders (e.g., Angelman and Prader–Willi syndromes as discussed in the target article, congenital amusia; Peretz, Cummings, & Dubé, Reference Peretz, Cummings and Dubé2007) and human genes orthologous to those involved in auditory traits in songbirds, which have convergent patterns to humans (Pfenning et al., Reference Pfenning, Hara, Whitney, Rivas, Wang, Roulhac and Jarvis2014). Moreover, candidate genes for musical aptitude (Järvelä, Reference Järvelä, Thaut and Hodges2019) could be investigated for molecular signals of selection in a comparative framework or could be checked for their overlap with gene families experiencing expansion. Findings from such genomic studies would lend more credibility to adaptive theories of music, complement the existing anthropological–psychological data on music, and move the evolutionary science of music toward a more rigorous framework, similar to the one that is currently employed in other evolutionary and biological sciences to identify adaptations. Finally, directly testing for selection using genomic data could motivate future anthropological and psychological research by identifying possible biological pathways and traits of musicality, which could be used to generate novel, testable hypotheses about the evolution of music.
“… functional information does not ‘validate’ claims of selection. It mostly serves to provide a more interesting and entertaining story. In humans, where controlled experiments and measurements of fitness are difficult or impossible to obtain, the evidence for selection must come directly from the genetic data.”
— Nielsen (Reference Nielsen2009)In their target article, Mehr et al. propose a theory of musical adaption as credible signaling, citing a breadth of evidence that spans the disciplines of anthropology, developmental psychology, and comparative psychology. Underlying their claim is the belief that establishing adaptations for music requires unequivocal evidence for the functional design of music. Writing on “what constitutes evidence for adaption” (sect. 2), the authors opine that “a successful account of music must provide evidence for the design of its principal features” (sect. 3, para. 1) and that “supporting a claim of adaptation therefore requires evidence for design.” (sect. 2, para. 8). Music, in their view, fulfills these criteria and “… exhibits design features consistent with adaptations for credible signaling, which give rise to a universal human psychology of music” (sect. 5.3, para. 2).
Although the authors put forth a well-reasoned perspective on the adaptive origins of music in credible signaling, we believe the authors err in presuming that evidence for design is a tenable basis upon which to infer adaptations for music. Criticisms regarding the inadequacy of appealing to design for adaptive theorizing are certainly not new and have historically been aimed at the adaptationist program, more generally (Gould & Lewontin, Reference Gould and Lewontin1979). These criticisms have highlighted that evolutionary theorists have a tendency to conflate design and adaptation (Nielsen, Reference Nielsen2009), while ignoring or underestimating the role of non-adaptive, evolutionary processes (Jensen et al., Reference Jensen, Payseur, Stephan, Aquadro, Lynch, Charlesworth and Charlesworth2019) that can produce organismal complexity (Lynch, Reference Lynch2007).
Alongside these criticisms against the adaptationist program and the growing appreciation of non-adaptive processes in evolution, methodological improvements in the evolutionary and biological sciences have helped move the scientific paradigm for identifying adaptations beyond simple appeals to design. Innovations in evolutionary biology, population genetics, and comparative genomics, for instance, have produced a systematic framework for testing for selection, and, by extension, for testing for adaptations by natural selection. Over several decades, quantitative approaches to evolutionary biology have yielded a suite of statistical tests that detect signatures of selection at the level of the genome (Nei, Suzuki, & Nozawa, Reference Nei, Suzuki and Nozawa2010; Nielsen, Reference Nielsen2005). Using these techniques, population-genetic and comparative-genomic analyses have successfully identified selection at the local and global levels. For example, local selection can be detected based on patterns of excessive population differentiation (e.g., Fst) or by patterns of haplotype structure and linkage disequilibrium (Nei et al., Reference Nei, Suzuki and Nozawa2010). Similarly, global selection is indicated by elevated rates of non-synonymous (Ka) substitutions compared to synonymous substitutions (Ks) (Clark et al., Reference Clark, Glanowski, Nielsen, Thomas, Kejariwal and Todd2003) or by a heighted ratio of non-synonymous and synonymous substitutions between species (Ka/Ks), relative to the ratio of non-synonymous and synonymous polymorphisms within a species (Pn/Ps) (McDonald & Kreitman, Reference McDonald and Kreitman1991). Moreover, lineage-specific gene duplications and expansions of gene families (Demuth & Hahn, Reference Demuth and Hahn2009) can be investigated in comparative frameworks to test for positive selection at the global level (Hahn, De Bie, Stajich, Nguyen, & Cristianini, Reference Hahn, De Bie, Stajich, Nguyen and Cristianini2005). These techniques can even be expanded to study the evolution of higher order features of the genome, such as changes in gene-coexpression networks (Oldham, Horvath, & Geschwind, Reference Oldham, Horvath and Geschwind2006).
Once identified, genomic signatures of selection can, then, be related to traits proposed to be functional, providing an initial foundation for identifying adaptations. However, simply associating molecular signals of selection with a trait posited to have adaptive origins can still produce erroneous conclusions about adaptation. Associations between genetic signals of selection, although possibly reflecting an adaptive effect, could also reflect pleiotropic effects (Nielsen, Reference Nielsen2009). To rule out pleiotropic effects, among other confounds, evolutionary biologists have developed an integrated framework that combines observational, field, and experimental methodologies to study adaptations in a number of organisms. It is only after arriving at a robust understanding of the underlying pathways between the genome, the phenotype, and fitness of the trait under question, using this integrated framework, can conclusions about adaptations confidently be drawn (Barrett & Hoekstra, Reference Barrett and Hoekstra2011).
Thus, even with the remarkable methodological progress in the evolutionary and biological sciences, producing unequivocal evidence of selection, and further, adaptation, is extremely difficult, as it requires a mechanistic understanding of the functional links between the genome, the phenotype, and the fitness of the trait under study (Barrett & Hoekstra, Reference Barrett and Hoekstra2011). To this end, unraveling the evolution of music may seem like an insurmountable undertaking. Already, however, the methods described above have helped illuminate the evolution of language in humans (Fisher, Reference Fisher2017; Fitch, Huber, & Bugnyar, Reference Fitch, Huber and Bugnyar2010), echolocation in bats (Zhang et al., Reference Zhang, Cowled, Shi, Huang, Bishop-Lilly, Fang and Wang2013), and the evolution of song and vocal learning in birds (Zhang et al., Reference Zhang, Li, Li, Li, Larkin, Lee and Wang2014). A similar framework could be adopted to probe adaptive hypotheses of music, particularly at the global level, as music is considered a human universal (Mehr et al., Reference Mehr, Singh, Knox, Ketter, Pickens-Jones, Atwood and Glowacki2019). For example, comparative studies could investigate selection related to music by studying the evolution of genes associated with music and musical ability across the mammalian phylogeny. Candidates for this analysis could include genes associated with music-related disorders (e.g., Angelman and Prader–Willi syndromes as discussed in the target article, congenital amusia; Peretz, Cummings, & Dubé, Reference Peretz, Cummings and Dubé2007) and human genes orthologous to those involved in auditory traits in songbirds, which have convergent patterns to humans (Pfenning et al., Reference Pfenning, Hara, Whitney, Rivas, Wang, Roulhac and Jarvis2014). Moreover, candidate genes for musical aptitude (Järvelä, Reference Järvelä, Thaut and Hodges2019) could be investigated for molecular signals of selection in a comparative framework or could be checked for their overlap with gene families experiencing expansion. Findings from such genomic studies would lend more credibility to adaptive theories of music, complement the existing anthropological–psychological data on music, and move the evolutionary science of music toward a more rigorous framework, similar to the one that is currently employed in other evolutionary and biological sciences to identify adaptations. Finally, directly testing for selection using genomic data could motivate future anthropological and psychological research by identifying possible biological pathways and traits of musicality, which could be used to generate novel, testable hypotheses about the evolution of music.
Financial support
This study was supported by the National Science Foundation (KAB, NSF-GRFP DGE-142487.1).
Conflict of interest
None.