Abstract
Complex vocal learning, the capacity to imitate new sounds, underpins the evolution of animal vocal cultures and song dialects and is a key prerequisite for human speech and song. Due to its relevance for the understanding of cultural evolution and the biology and evolution of language and music, the trait has gained much scholarly attention. However, while we have seen tremendous progress with respect to our understanding of its morphological, neurological and genetic aspects, its peculiar phylogenetic distribution has remained elusive. Intriguingly, animals as distinct as hummingbirds and humpback whales share well-developed vocal learning capacity in common with humans, while this ability is quite limited in nonhuman primates. Yet, solving this ‘vocal learning conundrum’ may shed light on the constraints ancestral humans overcame to unleash their vocal capacities. To this end I consider major constraints and functions that have been proposed. I highlight an especially promising ecological constraint, namely the spatial dimensionality of the environment. Based on an informal comparative review, I suggest that complex vocal learning is associated with three-dimensional habitats such as air and water. I argue that this is consistent with recent theoretical advances—i.e., the coercion-avoidance and dimensionality hypotheses—and with the long-standing hypothesis that mate choice is a major driver of the evolution and origin of complex vocal learning. However, I stress that multiple functions may apply and that quantitative phylogenetic comparative methods should be employed to finally resolve the issue.
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Abramson JZ, Hernández-Lloreda MV, García L, Colmenares F, Aboitiz F, Call J (2018) Imitation of novel conspecific and human speech sounds in the killer whale (Orcinus orca). Proc R Soc B Biol Sci 285(1871):20172171. https://doi.org/10.1098/rspb.2017.2171
Altringham JD (1996) Bats : biology and behaviour. Oxford University Press, Oxford
Amorim MCP, Vasconcelos RO, Fonseca PJ (2015) Fish Sounds and Mate Choice. In: Ladich F (ed) Sound communication in fishes. Springer, Vienna . https://doi.org/10.1007/978-3-7091-1846-7
Andersson MB (1994) Sexual selection. Princeton University Press, Princeton
Araya-Salas M, Gonzalez-Gomez P, Wojczulanis-Jakubas K, López V, Wright TF (2018) Spatial memory is as important as weapon and body size for territorial ownership in a lekking hummingbird. Sci Rep 8(1):1–11. https://doi.org/10.1038/s41598-018-20441-x
Araya-Salas M, Wright T (2013) Open-ended song learning in a hummingbird. Biol Let 9(5):20130625. https://doi.org/10.1098/rsbl.2013.0625
Arriaga G, Jarvis ED (2013) Mouse vocal communication system: are ultrasounds learned or innate? Brain Lang 124(1):96–116. https://doi.org/10.1016/j.bandl.2012.10.002
Bass AH, Chagnaud BP, Feng NY (2015) Comparative Neurobiology of Sound Production in Fishes. In: Ladich F (ed) Sound communication in fishes. Springer, Vienna . https://doi.org/10.1007/978-3-7091-1846-7
Bass AH, Mckibben JR (2003) Neural mechanisms and behaviors for acoustic communication in teleost fish. Prog Neurobiol 69:1–26. https://doi.org/10.1016/S0301-0082(03)00004-2
Beecher MD, Brenowitz EA (2005) Functional aspects of song learning in songbirds. Trends Ecol Evol 20(3):143–149. https://doi.org/10.1016/j.tree.2005.01.004
Behr O, Von Helversen O (2004) Bat serenades: complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behav Ecol Sociobiol 56:106–115. https://doi.org/10.1007/s00265-004-0768-7
Belyk M, Brown S (2017) The origins of the vocal brain in humans. Neurosci Biobehav Rev 77:177–193. https://doi.org/10.1016/j.neubiorev.2017.03.014
Berg D, S., Cortopassi, K. A., Beissinger, S. R., and Bradbury, J. W. (2012) Vertical transmission of learned signatures in a wild parrot. Proc R Soc B Biol Sci 279(1728):585–591. https://doi.org/10.1098/rspb.2011.0932
Blumstein DT, Armitage KB (1997) Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls. Am Nat 150(2):179–200. https://doi.org/10.1086/286062
Boncoraglio G, Saino N (2007) Habitat structure and the evolution of bird song: a meta-analysis of the evidence for the acoustic adaptation hypothesis. Funct Ecol 21(1):134–142. https://doi.org/10.1111/j.1365-2435.2006.01207.x
Bradbury JW, Vehrencamp L (2011) Principles of animal communication, 2nd edn. Oxford University Press, Oxford
Brockelman WY, Schilling D (1984) Inheritance of stereotyped gibbon calls. Nature 312(5995):634–636. https://doi.org/10.1038/312634a0
Buzatto BA, Roberts JD, Simmons LW (2015) Sperm competition and the evolution of precopulatory weapons: Increasing male density promotes sperm competition and reduces selection on arm strength in a chorusing frog. Evolution 69(10):2613–2624. https://doi.org/10.1111/evo.12766
Charlton BD (2014) Menstrual cycle phase alters women’s sexual preferences for composers of more complex music. Proc R Soc B Biol Sci 281(1784):20140403–20140403. https://doi.org/10.1098/rspb.2014.0403
Charlton BD, Filippi P, Fitch WT (2012) Do women prefer more complex music around ovulation? PLoS ONE 7(4):e35626. https://doi.org/10.1371/journal.pone.0035626
Charlton BD, Reby D (2016) The evolution of acoustic size exaggeration in terrestrial mammals. Nat Commun 7(1):12739. https://doi.org/10.1038/ncomms12739
Clutton-Brock TH, Harvey PH, Rudder B (1977) Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature 269(5631):797–800. https://doi.org/10.1038/269797a0
Cockburn A (2006) Prevalence of different modes of parental care in birds. Proc Biol Sci 273(1592):1375–1383. https://doi.org/10.1098/rspb.2005.3458
Coleman SW, Patricelli GL, Coyle B, Siani J, Borgia G (2007) Female preferences drive the evolution of mimetic accuracy in male sexual displays. Biol Lett 3(5):463–466. https://doi.org/10.1098/rsbl.2007.0234
Condro MC, White SA (2014) Recent Advances in the Genetics of Vocal Learning. Compar Cognit Behav Rev 9:75–98. https://doi.org/10.3819/ccbr.2014.90003
Cook P, Rouse A, Wilson M, Reichmuth C (2013) A California sea lion (Zalophus californianus) can keep the beat: Motor entrainment to rhythmic auditory stimuli in a non vocal mimic. J Comp Psychol 127(4):412–427. https://doi.org/10.1037/a0032345
Courtiol A, Etienne L, Feron R, Godelle B, Rousset F (2016) The Evolution of Mutual Mate Choice under Direct Benefits. Am Nat 188(5):521–538. https://doi.org/10.1086/688658
Couzin ID, Laidre ME (2009) Fission-fusion populations. Curr Biol 19(15):R633–R635. https://doi.org/10.1016/j.cub.2009.05.034
Cowlishaw G (1996) Sexual selection and information content in gibbon song bouts. Ethology 102(2):272–284. https://doi.org/10.1111/j.1439-0310.1996.tb01125.x
Darwin C (1871) The descent of man, and selection in relation to sex. John Murray, London
Dunn JC, Halenar LB, Davies TG, Cristobal-Azkarate J, Reby D, Sykes D, Dengg S, Fitch WT, Knapp LA, Cristobal-Azkarate J, Reby D, Sykes D (2015) Evolutionary trade-off between vocal tract and testes dimensions in Howler Monkeys. Curr Biol 25(21):2839–2844. https://doi.org/10.1016/j.cub.2015.09.029
Ekstrom JMM, Burke T, Randrianaina L, Birkhead TR (2007) Unusual sex roles in a highly promiscuous parrot: the Greater Vasa Parrot Caracopsis vasa. Ibis 149(2):313–320. https://doi.org/10.1111/j.1474-919X.2006.00632.x
Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197(4300):215–223. https://doi.org/10.1126/science.327542
Evans JP (2010) Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies. Proc R Soc B Biol Sci 277(1697):3195–3201. https://doi.org/10.1098/rspb.2010.0826
Everett C, Blasí DE, Roberts SG (2016) Language evolution and climate: the case of desiccation and tone. J Lang Evol 1(1):33–46. https://doi.org/10.1093/JOLE/LZV004
Feenders G, Liedvogel M, Rivas M, Zapka M, Horita H, Hara E, Wada K, Mouritsen H, Jarvis ED, Clayton NS (2008) Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLoS ONE 3(3):e1768. https://doi.org/10.1371/journal.pone.0001768
Fine ML (1978) Seasonal and geographical variation of the mating call of the oyster toadfish Opsanus tau L. Oecologia 36(1):45–57. https://doi.org/10.1007/BF00344570
Fine ML, Parmentier E (2015) Mechanisms of Fish Sound Production. In: Ladich F (ed) Sound Communication in Fishes. Springer, Vienna, pp 77–126. https://doi.org/10.1007/978-3-7091-1846-7_3
Finlayson C (2014) The improbable primate: how water shaped human evolution. Oxford University Press, Oxford
Fitch WT (2000) The evolution of speech: A comparative review. Trends Cognit Sci 4:258–267
Fitch WT (2004) Kin selection and “mother tongues”: a neglected component in language evolution”. In: Oller K, Griebel U (eds) Evolution of communication systems: a comparative approach. MIT Press, Cambridge, pp 275–296
Fitch WT (2005) The evolution of language: A comparative review. Biol Philos 20(2–3):193–203. https://doi.org/10.1007/s10539-005-5597-1
Fitch WT (2006) The biology and evolution of music: A comparative perspective. Cognition 100(1):173–215. https://doi.org/10.1016/j.cognition.2005.11.009
Fitch WT (2010) The Evolution of language. Cambridge University Press, Cambridge
Fitch WT (2017) Empirical approaches to the study of language evolution. Psychon Bull Rev 24(1):3–33. https://doi.org/10.3758/s13423-017-1236-5
Fitch WT (2018) The biology and evolution of speech: a comparative analysis. Ann Rev Linguist 4(1):255–279. https://doi.org/10.1146/annurev-linguistics-011817-045748
Fitch WT, De Boer B, Mathur N, Ghazanfar AA (2016) Monkey vocal tracts are speech-ready. Sci Adv 2(12):e1600723. https://doi.org/10.1126/sciadv.1600723
Freeberg TM (2006) Social complexity can drive vocal complexity: group size influences vocal information in Carolina chickadees. Psychol Sci 17(7):557–561. https://doi.org/10.1111/j.1467-9280.2006.01743.x
Fuhrmann D, Ravignani A, Marshall-Pescini S, Whiten A (2014) Synchrony and motor mimicking in chimpanzee observational learning. Sci Rep. https://doi.org/10.1038/srep05283
Gaeth AP, Short RV, Renfree MB (1999) The developing renal, reproductive, and respiratory systems of the African elephant suggest an aquatic ancestry. Proc Natl Acad Sci USA 96:5555–5558
Garamszegi LZ, Pavlova DZ, Eens M, Møller AP (2007) The evolution of song in female birds in Europe. Behav Ecol 18(1):86–96. https://doi.org/10.1093/beheco/arl047
Garcia SM, Kopuchian C, Mindlin GB, Fuxjager MJ, Tubaro PL, Goller F (2017) Evolution of vocal diversity through morphological adaptation without vocal learning or complex neural control. Curr Biol 27(17):2677-2683.e3. https://doi.org/10.1016/j.cub.2017.07.059
Geissmann T (2000) Gibbon songs and human music from an evolutionary perspective. In: Wallin N, Merker B, Brown S (eds) Origins of music. MIT Press, Cambridge, pp 103–123
Gould SJ (1991) Exaptation: A Crucial Tool for an Evolutionary Psychology. J Social Issues 47(3):43–65. https://doi.org/10.1111/j.1540-4560.1991.tb01822.x
Hansen P (1979) Vocal learning: its role in adapting sound structures to long-distance propagation, and a hypothesis on its evolution. Anim Behav 27:1270–1271. https://doi.org/10.1016/0003-3472(79)90073-3
Harcourt AH, Harvey PH, Larson SG, Short RV (1981) Testes weight, body weight and breeding system in primates. Nature 293:55–57
Harvey PP, Pagel MD (1998) The comparative method in evolutionary biology. Oxford University Press, Oxford
Hayes KJ, Hayes C (1952) Imitation in a home-raised chimpanzee. J Comparat Physiol Psychol 45(5):450–459. https://doi.org/10.1037/h0053609
Herman LM (2017) The multiple functions of male song within the humpback whale (Megaptera novaeangliae) mating system: Review, evaluation, and synthesis. Biol Rev 92:1795–1818. https://doi.org/10.1111/brv.12309
Hindmarsh AM (1984) Vocal mimicry in starlings. Behaviour 90:302–324. https://doi.org/10.1163/156853984X00182
Jackendoff R (1999) Possible stages in the evolution of the language capacity. Trends Cognit Sci 3(7):272–279. https://doi.org/10.1016/S1364-6613(99)01333-9
Janik VM (2014) Cetacean vocal learning and communication. Curr Opin Neurobiol 28:60–65. https://doi.org/10.1016/j.conb.2014.06.010
Janik VM, Slater PJB (1997) Vocal Learning in Mammals. Adv Study Behav 26:59–99. https://doi.org/10.1016/S0065-3454(08)60377-0
Janik VM, Slater PJB (2000) The different roles of social learning in vocal communication. Anim Behav 60(1):1–11. https://doi.org/10.1006/ANBE.2000.1410
Jarvis E (2006) Selection for and against vocal learning in birds and mammals. Ornithol Sci 5(1):5–14. https://doi.org/10.2326/osj.5.5
Jarvis ED (2009) Bird song systems: Evolution. Encycl Neurosci. https://doi.org/10.1016/B978-008045046-9.00935-9
Jarvis ED (2019) Evolution of vocal learning and spoken language. Science 366(6461):50–54. https://doi.org/10.1126/science.aax0287
Johnston CE, Buchanan HM (2007) Learned or innate production of acoustic signals in fishes: a test using a cyprinid. Environ Biol Fishes 78(2):183–187. https://doi.org/10.1007/s10641-006-9087-3
Kappelman J, Ketcham RA, Pearce S, Todd L, Akins W, Colbert MW, Feseha M, Maisano JA, Witzel A (2016) Perimortem fractures in Lucy suggest mortality from fall out of tall tree. Nature 537(7621):503–507. https://doi.org/10.1038/nature19332
Kelley JL, Morrell LJ, Inskip C, Krause J, Croft DP (2011) Predation risk shapes social networks in fission-fusion populations. PLoS ONE 6(8):24280. https://doi.org/10.1371/journal.pone.0024280
Kellogg ME, Burkett S, Dennis TR, Stone G, Gray BA, McGuire PM, Zori RT, Stanyon R (2007) Chromosome painting in the manatee supports Afrotheria and Paenungulata. BMC Evol Biol 7:6. https://doi.org/10.1186/1471-2148-7-6
Kershenbaum A, Ilany A, Blaustein L, Geffen E (2012) Syntactic structure and geographical dialects in the songs of male rock hyraxes. Proc R Soc B Biol Sci 279(1740):2974–2981. https://doi.org/10.1098/rspb.2012.0322
Killin A (2016) Reflections on imitation, vocal mimicry, and entrainment. Aisthesis Pratiche, Linguaggi e Saperi Dell’estetico 9(2):81–87. https://doi.org/10.13128/AISTHESIS-19418
King SL, Janik VM (2013) Bottlenose dolphins can use learned vocal labels to address each other. Proc Natl Acad Sci 110(32):13216–13221. https://doi.org/10.1073/pnas.1304459110
Knörnschild M (2014) Vocal production learning in bats. Curr Opin Neurobiol 28:80–85. https://doi.org/10.1016/j.conb.2014.06.014
Knörnschild M, Nagy M, Metz M, Mayer F, Von Helversen O (2010) Complex vocal imitation during ontogeny in a bat. Biol Let 6(2):156–159. https://doi.org/10.1098/rsbl.2009.0685
Kokko H, Johnstone RA (2002) Why is mutual mate choice not the norm? Operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signalling. Philos Trans R Soc B Biol Sci 357(1419):319–330. https://doi.org/10.1098/rstb.2001.0926
Kondo N, Watanabe S (2009) Contact calls: Information and social function. Jpn Psychol Res 51(3):197–208. https://doi.org/10.1111/j.1468-5884.2009.00399.x
Lack D (1968) Ecological adaptations for breeding in birds. Princeton University Press, Methuen
Ladich F (2014) Fish bioacoustics. Curr Opin Neurobiol 28:121–127. https://doi.org/10.1016/j.conb.2014.06.013
Laland KN, Janik VM (2006) The animal cultures debate. Trends Ecol Evol 21(10):542–547. https://doi.org/10.1016/j.tree.2006.06.005
Langmore NE, Davies NB, Hatchwell BJ, Hartley IR (1996) Female song attracts males in the alpine accentor Prunella collaris. Proc R Soc B Biol Sci 263(1367):141–146. https://doi.org/10.1098/rspb.1996.0022
Larsson M, Abbott BW (2018) Is the capacity for vocal learning in vertebrates rooted in fish schooling behavior? Evol Biol 45(4):359–373. https://doi.org/10.1007/s11692-018-9457-8
Lattenkamp EZ, Vernes SC (2018) Vocal learning: a language-relevant trait in need of a broad cross-species approach. Curr Opin Behav Sci 21:209–215. https://doi.org/10.1016/j.cobeha.2018.04.007
Leutenegger W, Cheverud J (1982) Correlates of sexual dimorphism in primates: Ecological and size variables. Int J Primatol 3(4):387–402. https://doi.org/10.1007/BF02693740
Liu AGSC, Seiffert ER, Simons EL (2008) Stable isotope evidence for an amphibious phase in early proboscidean evolution. Proc Natl Acad Sci 105(15):5786–5791. https://doi.org/10.1073/pnas.0800884105
Longrie N, Fine ML, Parmentier E (2008) Innate sound production in the cichlid Oreochromis niloticus. J Zool 275(4):413–417. https://doi.org/10.1111/j.1469-7998.2008.00457.x
Lopez PT, Narins PM, Lewis ER, Moore SW (1988) Acoustically induced call modification in the white-lipped frog, Leptodactylus albilabris. Anim Behav 36(5):1295–1308. https://doi.org/10.1016/S0003-3472(88)80198-2
Lovejoy CO (2009) Reexamining human origins in light of Ardipithecus ramidus. Science 326(5949):74-74e8. https://doi.org/10.1126/science.1175834
Lupyan G, Dale R (2016) Why Are There Different Languages? The Role of Adaptation in Linguistic Diversity. Trends Cognit Sci 20(9):649–660. https://doi.org/10.1016/j.tics.2016.07.005
Maddieson I, Bhattacharya T, Smith DE, Croft W (2011) Geographical distribution of phonological complexity. Linguist Typol 15(2):267–279. https://doi.org/10.1515/LITY.2011.020
Marlowe FW (2005) Hunter-gatherers and human evolution. Evol Anthropol 14(2):54–67. https://doi.org/10.1002/evan.20046
McComb K, Semple S (2005) Coevolution of vocal communication and sociality in primates. Biol Let 1(4):381–385. https://doi.org/10.1098/rsbl.2005.0366
Mehr S, Krasnow M, Bryant G, Hagen E (2020) Origins of music in credible signaling. Behav Brain Sci. https://doi.org/10.31234/osf.io/nrqb3
Meyer J (2004) Bioacoustics of human whistled languages: an alternative approach to the cognitive processes of language. Anais Da Academia Brasileira de Ciencias 76(2):405–412. https://doi.org/10.1590/s0001-37652004000200033
Miller GF (2000a) Evolution of Human Music through Sexual Selection. In: Wallin NL, Merker B, Brown S (eds) The origins of music. MIT Press, Cambridge, pp 329–360. https://doi.org/10.7551/mitpress/5190.003.0025
Miller GF (2000b) The mating mind: how sexual choice shaped the evolution of the human nature. Doubleday, New York
Mirceta, S., Signore, A. V., Burns, J. M., Cossins, A. R., Campbell, K. L., and Berenbrink, M. (2013). Evolution of mammalian diving capacity traced by myoglobin net surface charge. Science, 340(6138). https://doi.org/https://doi.org/10.1126/science.1234192
Mitani JC, Rodman PS (1979) Territoriality: the relation of ranging pattern and home range size to defendability, with an analysis of territoriality among primate species. Behav Ecol Sociobiol 5(3):241–251. https://doi.org/10.1007/BF00293673
Mithen S (2007) The singing neanderthals: The origins of music, Language. Mind and Body, Weidenfeld and Nicolson
Mizuno A, Soma M (2020) Potential role of sensory bias in plumage pattern evolution: termite-eating and polka-dots in estrildid finches. Ethol Ecol Evol. https://doi.org/10.1080/03949370.2020.1803414
Moravec ML, Striedter GF, Burley NT (2006) Assortative Pairing Based on Contact Call Similarity in Budgerigars. Melopsittacus undulatus Ethology 112(11):1108–1116. https://doi.org/10.1111/j.1439-0310.2006.01267.x
Morgan E (1997) The aquatic ape hypothesis: the most credible theory of human evolution. Souvenir Press, London
Mosing MA, Verweij KJH, Madison G, Pedersen NL, Zietsch BP, Ullén F (2014) Did sexual selection shape human music? Testing predictions from the sexual selection hypothesis of music evolution using a large genetically informative sample of over 10,000 twins. Evol Human Behav 36(5):359–366. https://doi.org/10.1016/j.evolhumbehav.2015.02.004
Münkemüller T, Lavergne S, Bzeznik B, Dray S, Jombart T, Schiffers K, Thuiller W (2012) How to measure and test phylogenetic signal. Methods Ecol Evol 3(4):743–756. https://doi.org/10.1111/j.2041-210X.2012.00196.x
Niemitz C (2010) The evolution of the upright posture and gait: a review and a new synthesis. Naturwissenschaften 97(3):241–263. https://doi.org/10.1007/s00114-009-0637-3
Noad MJ, Cato DH, Bryden MM, Jenner MN, Jenner KCS (2000) Cultural revolution in whale songs: humpbacks have picked up a catchy tune sung by immigrants from a distant ocean. Nature 408(6812):537. https://doi.org/10.1038/35046199
Nottebohm F (1972) The Origins of Vocal Learning. Am Nat 106(947):116–140. https://doi.org/10.1086/282756
Nowicki S, Searcy WA (2014) The evolution of vocal learning. Curr Opin Neurobiol 28:48–53. https://doi.org/10.1016/j.conb.2014.06.007
Odom KJ, Hall ML, Riebel K, Omland KE, Langmore NE (2014) Female song is widespread and ancestral in songbirds. Nat Commun. https://doi.org/10.1038/ncomms4379
Okanoya K (2002) Sexual display as a syntactic vehicle: the evolution of syntax in birdsong and human language through sexual selection. In: Wray A (ed) The transition to language. Oxford University Press, Oxford, pp 46–63
Parker GA (1998) Sperm Competition and the Evolution of Ejaculates: Towards a Theory base. In: Birkhead T, Møller AP (eds) Sperm competition and sexual selection. Academic Press, Cambridge, pp 3–54. https://doi.org/10.1016/b978-012100543-6/50026-x
Payne RB (1984) Sexual selection, lek and arena behavior, and sexual size dimorphism in birds. Ornithol Monogr 33:iii–52. https://doi.org/10.2307/40166729
Payne RB, Payne LL, Woods JL (1998) Song learning in brood-parasitic indigobirds Vidua chalybeata: Song mimicry of the host species. Anim Behav 55:1537–1553
Payne RB, Payne LL, Woods JL, Sorenson MD (2000) Imprinting and the origin of parasite-host species associations in brood-parasitic indigo-birds, Vidua chalybeata. Anim Behav 59:69–81
Peters S, Derryberry EP, Nowicki S (2012) Songbirds learn songs least degraded by environmental transmission. Biol Let 8(5):736–739. https://doi.org/10.1098/rsbl.2012.0446
Petkov CI, Jarvis ED (2012) Birds, primates, and spoken language origins: Behavioral phenotypes and neurobiological substrates. Front Evol Neurosci. https://doi.org/10.3389/fnevo.2012.00012
Phillips CT, Johnston CE (2008) Geographical divergence of acoustic signals in Cyprinella galactura, the whitetail shiner (Cyprinidae). Anim Behav 75(2):617–626. https://doi.org/10.1016/j.anbehav.2007.06.022
Plavcan JM, van Schaik CP (1997) Intrasexual competition and body weight dimorphism in anthropoid primates. Am J Phys Anthropol 103(1):37–68. https://doi.org/10.1002/(SICI)1096-8644(199705)103:1%3c37::AID-AJPA4%3e3.0.CO;2-A
Poole JH, Tyack PL, Stoeger-Horwath AS, Watwood S (2005) Elephants are capable of vocal learning. Nature 434(7032):455–456. https://doi.org/10.1038/434455a
Pradhan GR, van Schaik CP (2009) Why do females find ornaments attractive? The coercion-avoidance hypothesis. Biol J Lin Soc 96(2):372–382. https://doi.org/10.1111/j.1095-8312.2008.01131.x
Prat Y, Taub M, Yovel Y (2015) Vocal learning in a social mammal: Demonstrated by isolation and playback experiments in bats. Sci Adv 1(2):e1500019. https://doi.org/10.1126/sciadv.1500019
Prum. (2012) Aesthetic evolution by mate choice: Darwin’s really dangerous idea. Philos Trans R Soc B Biol Sci 367(1600):2253–2265. https://doi.org/10.1098/rstb.2011.0285
Prum RO (2010) The lande-kirkpatrick mechanism is the null model of evolution by intersexual selection: Implications for meaning, honesty, and design in intersexual signals. Evolution 64(11):3085–3100. https://doi.org/10.1111/j.1558-5646.2010.01054.x
Prum RO (2013) Coevolutionary aesthetics in human and biotic artworlds. Biol Philos 28(5):811–832. https://doi.org/10.1007/s10539-013-9389-8
Puechmaille SJ, Borissov IM, Zsebok S, Allegrini B, Hizem M, Kuenzel S, Schuchmann M, Teeling EC, Siemers BM (2014) Female mate choice can drive the evolution of high frequency echolocation in bats: a case study with Rhinolophus mehelyi. PLoS ONE 9(7):e103452. https://doi.org/10.1371/journal.pone.0103452
Puts DA (2010) Beauty and the beast: Mechanisms of sexual selection in humans. Evol Human Behav 31:157–175. https://doi.org/10.1016/j.evolhumbehav.2010.02.005
Ravignani A (2018) Darwin, sexual selection, and the origins of music. Trends Ecol Evol 33(10):716–719. https://doi.org/10.1016/J.TREE.2018.07.006
Reichmuth C, Casey C (2014) Vocal learning in seals, sea lions, and walruses. Curr Opin Neurobiol 28:66–71. https://doi.org/10.1016/j.conb.2014.06.011
Richman B (1978) The synchronization of voices by gelada monkeys. Primates 19(3):569–581. https://doi.org/10.1007/BF02373317
Richman B (1987) Rhythm and melody in gelada vocal exchanges. Primates 28(2):199–223. https://doi.org/10.1007/BF02382570
Rico-Guevara A, Hurme KJ (2019) Intrasexually selected weapons. Biol Rev 94(1):60–101. https://doi.org/10.1111/brv.12436
Ridgway S, Carder D, Jeffries M, Todd M (2012) Spontaneous human speech mimicry by a cetacean. Curr Biol 22(20):R860–R861. https://doi.org/10.1016/j.cub.2012.08.044
Riebel K, Odom KJ, Langmore NE, Hall ML (2019) New insights from female bird song: towards an integrated approach to studying male and female communication roles. Biol Lett 15(4):20190059. https://doi.org/10.1098/rsbl.2019.0059
Ríos-Chelén AA, Salaberria C, Barbosa I, Macías Garcia C, Gil D (2012) The learning advantage: Bird species that learn their song show a tighter adjustment of song to noisy environments than those that do not learn. J Evol Biol 25(11):2171–2180. https://doi.org/10.1111/j.1420-9101.2012.02597.x
Roberts G (2010) An experimental study of social selection and frequency of interaction in linguistic diversity. Interact Stud 11(1):138–159. https://doi.org/10.1075/is.11.1.06rob
Ruff CB, Burgess ML, Ketcham RA, Kappelman J (2016) Limb Bone Structural Proportions and Locomotor Behavior in A.L. 288-1 (“Lucy”). PLoS ONE 11(11):e0166095. https://doi.org/10.1371/journal.pone.0166095
Ryan MJ (1998) Sexual selection, receiver biases, and the evolution of sex differences. Science 281(5385):1999–2003. https://doi.org/10.1126/science.281.5385.1999
Ryan MJ (2018) A taste for the beautiful: The evolution of attraction. Princeton University Press, Princeton
Ryan MJ, Rand AS (1990) The sensory basis of sexual selection for complex calls in the tungara frog, Physalaemus pustulosus (sexual selection for sensory exploitation). Evolution 44(2):305–314. https://doi.org/10.1111/j.1558-5646.1990.tb05200.x
Savage PE, Loui P, Tarr B, Schachner A, Glowacki L, Mithen S, Fitch WT (2020) Music as a coevolved system for social bonding. Behav Brain Sci. https://doi.org/10.1017/S0140525X20000333
Saxton TK, Mackey LL, McCarty K, Neave N (2016) A lover or a fighter? Opposing sexual selection pressures on men’s vocal pitch and facial hair. Behav Ecol 27(2):512–519. https://doi.org/10.1093/beheco/arv178
Sayigh LS, Fellner W, Janik VM, King SL, Wells RS (2013) Vocal copying of individually distinctive signature whistles in bottlenose dolphins. Proc R Soc B Biol Sci 280(1757):20130053–20130053. https://doi.org/10.1098/rspb.2013.0053
Scarl JC, Bradbury JW (2009) Rapid vocal convergence in an Australian cockatoo, the galah Eolophus roseicapillus. Anim Behav 77(5):1019–1026. https://doi.org/10.1016/j.anbehav.2008.11.024
Scharff C, Petri J (2011) Evo-devo, deep homology and Fox P2: Implications for the evolution of speech and language. Philos Trans R Soc B Biol Sci 366(1574):2124–2140. https://doi.org/10.1098/rstb.2011.0001
Schmidt KL, Moore SD, MacDougall-Shackleton EA, MacDougall-Shackleton SA (2013) Early-life stress affects song complexity, song learning and volume of the brain nucleus RA in adult male song sparrows. Anim Behav 86(1):25–35. https://doi.org/10.1016/j.anbehav.2013.03.036
Schusterman RJ (2008) Vocal Learning in Mammals with Special Emphasis on Pinnipeds. In: Oller DK, Griebel U (eds) Evolution of Communicative Flexibility. MIT Press, Cambridge, pp 41–70. https://doi.org/10.7551/mitpress/9780262151214.003.0003
Searcy WA (2019) Animal communication, cognition, and the evolution of language. Anim Behav 151:203–205. https://doi.org/10.1016/j.anbehav.2019.03.001
Searcy WA, Nowicki S (2019) Birdsong learning, avian cognition and the evolution of language. Anim Behav 151:217–227
Searcy WA, Nowicki S (2019) Birdsong learning, avian cognition and the evolution of language. Anim Behav 151:217–227. https://doi.org/10.1016/j.anbehav.2019.01.015
Sewall KB (2015) Social complexity as a driver of communication and cognition. Integr Comp Biol 55(3):384–395. https://doi.org/10.1093/icb/icv064
Sewall KB, Young AM, Wright TF (2016) Social calls provide novel insights into the evolution of vocal learning. Anim Behav 120:163–172. https://doi.org/10.1016/j.anbehav.2016.07.031
Simmons LW, Peters M, Rhodes G (2011) Low pitched voices are perceived as masculine and attractive but do they predict semen quality in men? PLoS ONE 6(12):29271
Simmons LW, Peters M, Rhodes G (2011) Low Pitched Voices Are Perceived as Masculine and Attractive but Do They Predict Semen Quality in Men? PLoS ONE 6(12):29271. https://doi.org/10.1371/journal.pone.0029271
Sjare B, Stirling I (1996) The breeding-behavior of atlantic walruses, Odobenus rosmarus rosmarus, in the Canadian high arctic. Can J Zool 74:897–911
Sjare B, Stirling I, Spencer C (2003) Structural variation in the songs of Atlantic walruses breeding in the Canadian High Arctic. Aquat Mamm 29:297–318
Slabbekoorn H, den Boer-Visser A (2006) Cities change the songs of birds. Curr Biol 16(23):2326–2331. https://doi.org/10.1016/j.cub.2006.10.008
Soma M, Garamszegi LZ (2011) Rethinking birdsong evolution: Meta-analysis of the relationship between song complexity and reproductive success. Behav Ecol 22(2):363–371. https://doi.org/10.1093/beheco/arq219
Sousa-Lima RS, Paglia AP, da Fonseca GAB (2008) Gender, age, and identity in the isolation calls of Antillean manatees (Trichechus manatus manatus). Aquat Mamm 34(1):109–122. https://doi.org/10.1578/AM.34.1.2008.109
Sousa-Lima RS, Paglia AP, Da Fonseca GAB (2002) Signature information and individual recognition in the isolation calls of Amazonian manatees, Trichechus inunguis (Mammalia: Sirenia). Anim Behav 63(2):301–310. https://doi.org/10.1006/ANBE.2001.1873
Stafford KM, Lydersen C, Wiig Ø, Kovacs KM (2018) Extreme diversity in the songs of Spitsbergen’s bowhead whales. Biol Let 14:20180056. https://doi.org/10.1098/RSBL.2018.0056
Stansbury AL, Janik VM (2019) Formant modification through vocal production learning in gray seals. Curr Biol 29(13):2244-2249.e4. https://doi.org/10.1016/j.cub.2019.05.071
Stewart-Williams S, Thomas AG (2013) The ape that thought it was a peacock: does evolutionary psychology exaggerate human sex differences? Psychol Inq 24:137–168. https://doi.org/10.1080/1047840X.2013.804899
Stirling I, Thomas JA (2003) Relationships between underwater vocalizations and mating systems in phocid seals. Aquat Mamm 29(2):227–246. https://doi.org/10.1578/016754203101024176
Stoeger AS, Manger P (2014) Vocal learning in elephants: Neural bases and adaptive context. Curr Opin Neurobiol 28:101–107. https://doi.org/10.1016/j.conb.2014.07.001
Stoeger AS, Mietchen D, Oh S, De Silva S, Herbst CT, Kwon S, Fitch WT (2012) An Asian elephant imitates human speech. Curr Biol 22(22):2144–2148. https://doi.org/10.1016/j.cub.2012.09.022
Sukumar R (2003) The living elephants: evolutionary ecology, behaviour, and conservation. Oxford University Press, Oxford
Suwa G, Kono RT, Simpson SW, Asfaw B, Owen Lovejoy C, White TD (2009) Paleobiological implications of the ardipithecus ramidus dentition. Science 326(5949):94–99. https://doi.org/10.1126/science.1175824
Symington MMF (1990) Fission-fusion social organization in Ateles and Pan. Int J Primatol 11(1):47–61. https://doi.org/10.1007/BF02193695
Takahashi DY, Fenley AR, Teramoto Y, Narayanan DZ, Borjon JI, Holmes P, Ghazanfar AA (2015) The developmental dynamics of marmoset monkey vocal production. Science 349(6249):734–738. https://doi.org/10.1126/science.aab1058
Takahashi DY, Liao DA, Ghazanfar AA (2017) vocal learning via social reinforcement by infant marmoset monkeys. Curr Biol 27(12):1844-1852.e6. https://doi.org/10.1016/j.cub.2017.05.004
Tchernichovski O, Schwabl H, Nottebohm F (1998) Context determines the sex appeal of male zebra finch song. Anim Behav 55(4):1003–1010. https://doi.org/10.1006/anbe.1997.0673
Tellechea JS, Norbis W, Olsson D, Fine ML (2011) Calls of the black drum (Pogonias cromis: Sciaenidae): geographical differences in sound production between northern and southern hemisphere populations. J Exp Zool Part A Ecol Genet Physio 315A(1):48–55. https://doi.org/10.1002/jez.651
Toth CA, Parsons S (2018) The high-output singing displays of a lekking bat encode information on body size and individual identity. Behav Ecol Sociobiol 72(7):1–14. https://doi.org/10.1007/s00265-018-2496-4
Tyack PL (2020) A taxonomy for vocal learning. Philos Trans R Soc B Biol Sci 375(1789):20180406. https://doi.org/10.1098/rstb.2018.0406
Uhen MD (2007) Evolution of marine mammals: Back to the sea after 300 million years. Anatom Record 290(6):514–522. https://doi.org/10.1002/ar.20545
Verhaegen M (2013) The aquatic ape evolves: common misconceptions and unproven assumptions about the so-called aquatic ape hypothesis. Hum Evol 28(3–4):237–266
Vernes SC (2017) What bats have to say about speech and language. Psychon Bull Rev 24(1):111–117. https://doi.org/10.3758/s13423-016-1060-3
Verpooten J, Eens M (in press) Singing is not associated with social complexity across species. Behav Brain Sci.
Voeten DFAE, Cubo J, de Margerie E, Röper M, Beyrand V, Bureš S, Tafforeau P, Sanchez S (2018) Wing bone geometry reveals active flight in Archaeopteryx. Nat Commun 9(1):923. https://doi.org/10.1038/s41467-018-03296-8
Weinstein D, Launay J, Pearce E, Dunbar RIM, Stewart L (2016) Singing and social bonding: changes in connectivity and pain threshold as a function of group size. Evol Hum Behav 37:152–158. https://doi.org/10.1016/j.evolhumbehav.2015.10.002
White TD, Lovejoy CO, Asfaw B, Carlson JP, Suwa G (2015) Neither chimpanzee nor human, Ardipithecus reveals the surprising ancestry of both. Proc Natl Acad Sci 112(16):4877–4884. https://doi.org/10.1073/pnas.1403659111
Whitehead H, Rendell L (2012) The cultural lives of whales and dolphins. University of Chicago Press, Chicago
Wilkinson GS (2003) Social and vocal complexity in bats. In: de Waal F, Tyack PL (eds) Animal social complexity: intelligence, culture and individualized societies. Harvard University Press, Harvard, p 86
Winter P, Handley P, Ploog D, Schott D (1973) Ontogeny of squirrel monkey calls under normal conditions and under acoustic isolation. Behaviour 47(3–4):230–239. https://doi.org/10.1163/156853973X00085
Zann R, Dunstan E (2008) Mimetic song in superb lyrebirds: Species mimicked and mimetic accuracy in different populations and age classes. Anim Behav 76(3):1043–1054. https://doi.org/10.1016/j.anbehav.2008.05.021
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I thank Sally Street, Krist Vaesen, Marcel Eens, and Gert Verpooten for discussion and comments on an initial version of the manuscript. I especially thank the associate editor and two anonymous reviewers for their in-depth comments on previous versions of the manuscript.
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Verpooten, J. Complex vocal learning and three-dimensional mating environments. Biol Philos 36, 12 (2021). https://doi.org/10.1007/s10539-021-09786-2
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DOI: https://doi.org/10.1007/s10539-021-09786-2