Humans devote ample time to produce and perceive music. How and why this behavioral propensity originated in our species is unknown. For centuries, speculation dominated the study of the evolutionary origins of musicality. Following Darwin’s early intuitions, recent empirical research is opening a new chapter to tackle this mystery

Ravignani, A.

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to suggest an additional chapter, it wouldhave been on culture, the ‘secret of oursuccess’ [7]. One could have wonderedabout the importance of the culturalenvironment for selecting particularlearning abilities and cooperative behav-iours [8]. For now, I am grateful to Solo-mon for not suggesting that robots will killus all and pursuing a question no onewants to ask.Future Humans: Inside the Science of our ContinuingEvolution by Scott Solomon, Yale University Press, 2016.US$142.95, hbk (880 pp.) ISBN 978-0-047-17964-21School of Anthropology & Museum Ethnography, 51Banbury Road, University of Oxford, Oxford OX2 6PE, UK*Correspondence:alexandra.alvergne@anthro.ox.ac.uk (A. Alvergne).https://doi.org/10.1016/j.tree.2018.08.002References1. Goldacre, B. (2006) All men will have big willies. https://www.badscience.net/2006/10/%E2%80%9Call-men-will-have-big-willies%E2%80%9D/2. Nettle, D. and Pollet, T.V. (2008) Natural selection on malewealth in humans. Am. Nat. 172, 658–6663. O’Neil, E., Jr (2009) Poverty, structural violence, and racismin a world out of balance. Race Ethn. Multidiscip. Glob.Perspect. 3, 115–1384. Wilde, S. et al. (2014) Direct evidence for positive selectionof skin, hair, and eye pigmentation in Europeans during thelast 5,000 y. Proc. Natl. Acad. Sci. U. S. A. 111, 4832–48375. Ellison, P. (2009) On Fertile Ground: A Natural History ofHuman Reproduction, Harvard University Press6. Stinson, S. et al., eds (2012) Human Biology: An Evolution-ary and Biocultural Perspective (2nd edn), Wiley-Blackwell7. Henrich, J. (2017) The Secret of Our Success: How CultureIs Driving Human Evolution, Domesticating Our Species,and Making Us Smarter, Princeton University Press8. Laland, K.N. (2017) Darwin’s Unfinished Symphony: HowCulture Made the Human Mind, Princeton University PressForumDarwin, SexualSelection, and theOrigins of MusicAndrea Ravignani1,2,*,@Humans devote ample time to pro-duce and perceivemusic. How andwhy this behavioral propensityoriginated in our species isunknown. For centuries, specula-tion dominated the study of theevolutionary origins of musicality.Following Darwin’s early intuitions,recent empirical research is open-ing a new chapter to tackle thismystery.Darwin’s Early IntuitionsDarwinian thought applied to understand-ing howmusic originated in humans has aconflicted history. Darwin originally pro-posed to apply his sexual selection frame-work to music [1]. However, except for afew theoretical perspectives acknowledg-ing his contribution [2], it was commonlyassumed that Darwin had little to sayabout music, and music research littleto benefit from a Darwinian approach[1]. Recently, empirical research hastested Darwin’s intuitions laid out ashypotheses almost two decades ago[2]. This research deals with the ‘evolutionof musicality’, with musicality defined as ahuman biological predisposition to pro-cess music [3]. This is not to be confusedwith the study of the ‘cultural evolution ofmusic’, where music is seen as a culturalproduct varying over history (Box 1 andFigure 1).Old Hypotheses and NewEmpirical WorkTraditionally, hypotheses for the evolutionof humanmusicality focused on one over-arching question: why is music such awidespread behavior in our species if itdoes not seem to have an obvious adap-tive function? Formore than a century, therole of sexual selection in human musical-ity has been addressed from purely theo-retical and anecdotal perspectives. Bycontrast, the past decade has seen anumber of empirical, complementaryefforts to test whether musicality couldbe a sexually selected trait in humans.Discovering genes associated with musi-cal aptitude is a necessary prerequisitebefore any selective pressure (sexual ornatural) can be invoked. Molecular stud-ies have found a number of genetic cor-relates or expression patterns related tomusic processing, production, and per-ception [4]. In particular, alleles of thearginine vasopressin receptor genes areassociated with memory for, among otherthings, musical motifs. In addition, musiclistening and performance influence upre-gulation of many genes affecting motorbehavior, learning, memory, and dopami-nergic pathways. At the population level,a large study used twin modeling to testpredictions generated by the sexualselection hypothesis [5]. This study foundBox 1. Evolution of Music versus MusicalityIn contrast to research about the evolution of human musicality [3], a second strand has investigated theevolution of music, intended as a cultural product of musicality. Darwin had a clear intuition that languageand birdsong are shaped by learning and transmission (see Figure 1A in main text), and this intuition canbe easily extended to music (see Figure 1B in main text). This second strand of empirical research tacklesthe question of how imitation, transmission, and ‘selection’ shape cultural and structural features of music(reviewed in [12]). Empirical, corpus-based research has shown how sets of musical behaviors are shapedby interindividual transmission across generations, display temporal trends and associations with othercultural variables, and are pruned via ‘cultural bottlenecks’ (reviewed in [12]). In addition, experimentalefforts have replicated in the laboratory how musical patterns and cultures ‘evolve’: by building artificialcultural strains of participants who imitate unstructured sounds from their predecessors (see Figure 1B inmain text), music-like patterns emerge (reviewed in [12]). Studying the evolution of both music andmusicality is equally important, especially in light of the increasing scientific synthesis of biology andculture. This work on cultural transmission provides both a link between music and musicality, and apossibility to perform cross-species research (Box 2) using comparable paradigms (see Figure 1A vs 1B inmain text).716 Trends in Ecology & Evolution, October 2018, Vol. 33, No. 10some, though weak, support that musi-cality is sexually selected for (see below).Another study found that during peak fer-tility, females preferred composers ofmore complex music as short-term part-ners [6]. These connections betweengenes, physiology, and behavior mightseem straightforward at first. However,they are the first empirical efforts in a fieldtraditionally dominated by ‘Just So Sto-ries’. A new chapter is being opened upby these recent empirical results.Breaking Down the Evolution ofMusicality into IndividuallyTestable HypothesesTheplurality of these empirical approachesand results suggests that the evolution ofmusicality shouldbebrokendown into indi-vidually testablesubhypotheses (H1–4 in Table 1), whichcan be tested to probe the sexual selectionframework. How do the empirical studiesdescribed above address the hypothesesin Table 1? There is ample evidence forH1:a number of genes are associated with,among other things, musical aptitude, cre-ativity, perception, and production [4,5].There is also some evidence for H2: musi-cality correlates with other measures ofreproductive success, although this corre-lation does not seem to derive from over-lapping genetic influences [5]. These firsttwo hypotheses are expected to hold truenotonly for thecaseofsexual selection,butalso for virtually any framework in whichevolution plays a role in shapingmusicality.Crucially, there is negative evidence forH3:musicality does not seem topredictmatingsuccess in a modern, Western society [5].However, this finding must be contrastedwith positive evidence for H4: women pre-fer more complex music and better per-formers. Women, more than men, wouldchoose higher-quality performers for long-term relationships [7], and – around ovula-tion – they would pick a composer of morecomplexmusic forshort-termrelationships[6].Notice that,whileH1–3wouldhold for ageneral natural selection framework, H4would provide evidence for sexual selec-tion in particular (but see [8,9]).A Complex Picture: MixedSupport for Sexual Selection onHuman MusicalityTogether, these works provide a multifac-eted picture: some data support whileother data refute the role of sexual selec-tion in human musicality; possiblybecause this evolutionary framework ismore complex than usually surmised.Some caveats apply, which can informand refine future research. First, sexualselection already displays nuances whenapplied to model organisms whose etho-gram is well known (e.g., Drosophila).Applying sexual selection to early stagesof human evolution is even trickier. Sec-ond, each one of the results above wasobtained from modern, Western socie-ties. Primordial conditions and selectiveCultural transmission of mofs in:(B) Scosh undergrads(A) Zebra finchesFigure 1. How Individual Learning and Interindividual Transmission across Generations ofLearners Can Shape (A) Birdsong and (B) Human Music. In iterated learning experiments with zebrafinches (A), a bird was raised in isolation and hence produced an aberrant song. This zebra finch (bird 1)constituted the only tutor for bird 2, which in turn tutored bird 3, etc. In the human iterated learning experiments,a non-musician (participant 1) was given random drumming patterns to imitate, and the imitated patterns weregiven to participant 2, again to copy. In both cases, signals became more structured over experimentalgenerations: bird vocalizations converged towards wild-type songs, and drumming patterns convergedtowards rhythmic features found in most world musical cultures (see also universals and comparative methodin Box 2). Both studies are reviewed in [12].Table 1. Subhypotheses Supporting Hypotheses of Musicality as a Naturally Selected, Sexually Selected, or Nonadaptive, Purely Esthetical TraitaHypotheses Refs NaturalselectionSexualselectionNonadaptiveesthetic traitH1 Genes that code for abilities related to music perception and production. Reviewed in [4] + + +H2 Population-wide associations between increased musicality and traits related to higher fitness. [5] + + H3 Greater mating success in musically skilled individuals – as long as this leads to increased fitness.Notice, however, that mating success does not always coincide with reproductive success, namelythe number of surviving, second-generation offspring, or fertilization success.[5]   H4 Sexual dimorphism in preference, operationalized as one sex preferentially choosing mates whoshow a particular musical trait, such as mates who produce more complex or conspicuous music,or are better performers.[6,7] 0 + +aH1, H2, and H4 are mostly supported by the reviewed literature, while H3 is not. +, positive evidence; , negative evidence; 0, neutral evidence.Trends in Ecology & Evolution, October 2018, Vol. 33, No. 10 717forces might be removed or reversed inpresent-day humans (e.g., contraceptionand relaxed selection), making conceptslike fitness and mating advantage difficultto test reliably. Third, across animal spe-cies, females can be either the choosingor the chosen sex [8]: if musicality weresexually selected for in our lineage, malesshould not be assumed as those system-atically engaging in displays. Fourth, sexdifferences in human cognition are some-times attributable to culture, rather thanpurely biological sexual dimorphism. Thesame might hold for musicality. Finally,sexual selection is only one of the manyhypotheses suggested for how musicmight have originated in humans. Somealternative hypotheses invoke, for exam-ple, kin selection, group bonding, or coor-dinated behavior [2,7,9]. Otherhypotheses seek less functionally drivenexplanations [10], or propose that musi-cality would not have evolved under func-tional selective pressures, but rather be abyproduct of other traits such as lan-guage [7,11,12]. In support of thishypothesis, most genes related to musicprocessing [4] are equally related to pho-nological processing. In such cases, it isimpossible to know whether music,speech, or both influenced the prevalenceof a particular gene.Human Sensory Biases andAlternative EvolutionaryHypothesesA possible solution to this riddle could beoffered by the biological framework ofsensory biases [2,10]. This frameworksuggests that not all traits and perceptualpreferences are amenable to selectivepressures. Preference for some patternsis a mere byproduct of sensory biases,and production of specific patterns is away of exploiting those biases. In particu-lar, the idea from avian vision that evolu-tion can be driven by esthetics, ratherthan functionality [10], is readily extend-able to other species (humans) anddomains (musicality). Empiricalevidence for sensory biases that lack astraightforward function [10] should besought for human musicality. Forinstance, the small-integer ratio bias inrhythm processing is a potentialcandidate for nonfunctional sensorybiases. When humans perceive or imitatemusical rhythms, they tend to alter noteonsets in a way that interonset durationsare integer multiples of each other’s(Figure 1B and references in [12]). Thisapproach seems particularly worthy ofmore investigation in humans; alsobecause a substrate of sensory biases(Box 1) could fit most evolutionary frame-works, and link behavioral predispositionswith culturally transmitted behaviors(Figure 1).A Multicomponent Approach toEmpirically Test the Origins ofHuman MusicalityIn brief, it remains unclear whether sexualselection might have shaped musicality inour ancestors [3,8,9]. What appears clearis that several strands of research arestarting to actively test evolutionaryhypotheses empirically. Armchairspeculation is finally turning into data-driven debate. Methods used includecomparative experiments on precursorsto musicality in other species (Box 2),genetics of human populations, andpaleo-anthropology reconstructing earlyhominid behavior. An empirical approachto Darwin’s longstanding intuitions(Box 2) should allow testing whether sex-ual selection, or other evolutionary mech-anisms instead, drove the emergenceof musicality. Crucially, musicalityshould be deconstructed in its con-stituent components, for example, theneurobiological bases for preferring con-sonant intervals, processing temporallystructured rhythmic sequences, orsynchronizing to a beat (Box 1) [12],and each tested independently. Severalcomplex behaviors in animals can bedissected into simpler unrelated mecha-nisms, each with a distinct evolutionarypath. Likewise, distinct evolutionary pathsmight underlie different components ofhuman musicality.AcknowledgmentsThe author is sincerely grateful to Ben Charlton,Cinzia Chiandetti, Piera Filippi, Tecumseh Fitch,Maxime Garcia, Irma Järvelä, Massimo Lumaca,Guy Madison, Margarita Mendez Arostegui, Ales-sandro Miani, John O’Connor, Ruth Sonnweber,Charlie Stuijt, the editor, and two anonymous refer-ees for invaluable comments on earlier manuscriptversions of this paper. This project has receivedfunding from the European Union’s Horizon 2020Research and Innovation Programme under theMarie Skłodowska-Curie grant agreement No.665501 with the research Foundation Flanders(FWO) (Pegasus2 Marie Curie fellowship12N5517Nto A.R.), a visiting fellowship in Language Evolutionfrom the Max Planck Society, and ERC grant 283435ABACUS (to Bart de Boer).1Research Department, Sealcentre Pieterburen,Hoofdstraat 94a, 9968 AG Pieterburen, The Netherlands2Artificial Intelligence Laboratory, Vrije Universiteit Brussel,Pleinlaan 2, 1050 Brussels, Belgium*Correspondence:andrea.ravignani@gmail.com (A. Ravignani).https://doi.org/10.1016/j.tree.2018.07.006Box 2. Darwin’s Legacy beyond Sexual SelectionGoing beyond sexual selection, researchers have tested three of Darwin’s ideas that are indirectly linked,though clearly connected, to the evolution of musicality. One concept relates to the universality of music andmusical skills. The biological predispositions of a species define the set of behaviors and behavioral artifactsthey produce, and musicality is no exception [3,11,12]. This concept was subtly introduced by Darwin butneeded to develop in the 20th century before being tackled empirically [1,12]. A second concept is thecomparative method [2,3]: looking for homologies and analogies of traits underpinning human musicality inother animal species. This has proved a fruitful strand of research [12]. Third, a recurrent theme in Darwin’swork is the association between vocal modulation and emotions [11]: this concept has been empiricallytackled via prosody. Perceptual experiments have tested how this musical aspect of human language linksspeech, emotions, and referential meaning [11].718 Trends in Ecology & Evolution, October 2018, Vol. 33, No. 10References1. Bannan, N. (2016) Darwin, music and evolution: newinsights from family correspondence on The Descent ofMan. Music. Sci. 21, 3–252. Miller, G. et al. (2000) Evolution of human music throughsexual selection. In The Origins of Music (Wallin, N., ed.),pp. 329–360, MIT Press3. Honing, H. (2018) On the biological basis of musicality.Ann. N. Y. Acad. Sci. 1423, 51–564. Järvelä, I. (2018) Genomics studies on musical aptitude,music perception, and practice. Ann. N. Y. Acad. Sci.1423, 82–915. Mosing, M.A. et al. (2015) Did sexual selection shapehuman music? Testing predictions from the sexualselection hypothesis of music evolution using a largegenetically informative sample of over 10,000 twins. Evol.Hum. Behav. 36, 359–3666. Charlton, B.D. (2014) Menstrual cycle phase alters wom-en’s sexual preferences for composers of more complexmusic. Proc. R. Soc. B 281, 201404037. Madison, G. et al. (2018) Musical improvisation skill in aprospective partner is associated with mate value andpreferences, consistent with sexual selection and parentalinvestment theory: implications for the origin of music.Evol. Hum. Behav. 39, 120–1298. Odom, K.J. et al. (2014) Female song is widespread andancestral in songbirds. Nat. Commun. 5, 33799. Merker, B. et al. (2000) Synchronous chorusing andhuman origins. In The Origins of Music (Wallin, N., ed.),MIT Press10. Prum, R.O. (2017) The Evolution of Beauty: How Darwin’sForgotten Theory of Mate Choice Shapes the AnimalWorld-and Us, pp. 315–327, Doubleday11. Filippi, P. et al. (2017) Humans recognize emotionalarousal in vocalizations across all classes of terrestrialvertebrates: evidence for acoustic universals. Proc. R.Soc. B 284, 2017099012. Ravignani, A. et al. (2017) The evolution of rhythm cogni-tion: timing in music and speech. Front. Hum. Neurosci.11, 303Trends in Ecology & Evolution, October 2018, Vol. 33, No. 10 719

Darwin, sexual selection, and the origins of music

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