How and why patterns of sexual dimorphism in human faces vary across the world
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33727579
PubMed Central
PMC7966798
DOI
10.1038/s41598-021-85402-3
PII: 10.1038/s41598-021-85402-3
Knihovny.cz E-zdroje
- MeSH
- algoritmy MeSH
- antropometrie MeSH
- biologická evoluce MeSH
- biologická variabilita populace MeSH
- fenotyp * MeSH
- krása MeSH
- lidé MeSH
- obličej anatomie a histologie MeSH
- pohlavní dimorfismus * MeSH
- tělesná výška MeSH
- teoretické modely MeSH
- Check Tag
- lidé MeSH
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Sexual selection, including mate choice and intrasexual competition, is responsible for the evolution of some of the most elaborated and sexually dimorphic traits in animals. Although there is sexual dimorphism in the shape of human faces, it is not clear whether this is similarly due to mate choice, or whether mate choice affects only part of the facial shape difference between men and women. Here we explore these questions by investigating patterns of both facial shape and facial preference across a diverse set of human populations. We find evidence that human populations vary substantially and unexpectedly in both the magnitude and direction of facial sexually dimorphic traits. In particular, European and South American populations display larger levels of facial sexual dimorphism than African populations. Neither cross-cultural differences in facial shape variation, sex differences in body height, nor differing preferences for facial femininity and masculinity across countries, explain the observed patterns of facial dimorphism. Altogether, the association between sexual shape dimorphism and attractiveness is moderate for women and weak (or absent) for men. Analysis that distinguishes between allometric and non-allometric components reveals that non-allometric facial dimorphism is preferred in women's faces but not in faces of men. This might be due to different regimes of ongoing sexual selection acting on men, such as stronger intersexual selection for body height and more intense intrasexual physical competition, compared with women.
Center for Theoretical Study Charles University and Czech Academy of Sciences Prague Czech Republic
Department of Anatomy Animal Physiology and Biophysics University of Bucharest Bucharest Romania
Department of Psychology Kadir Has University Istanbul Turkey
Department of Zoology Faculty of Science Charles University Prague Czech Republic
Division of Psychology University of Stirling Stirling FK9 4LA UK
Human Behaviour Lab Faculty of Psychology Universidad El Bosque Bogotá Colombia
Zobrazit více v PubMed
Marcinkowska UM, et al. Women’s preferences for men’s facial masculinity are strongest under favorable ecological conditions. Sci. Rep. 2019;9:1–10. doi: 10.1038/s41598-019-39350-8. PubMed DOI PMC
Klein SL. Sex influences immune responses to viruses, and efficacy of prophylaxis and treatments for viral diseases. BioEssays. 2012;34:1050–1059. doi: 10.1002/bies.201200099. PubMed DOI PMC
Moore FR, Law Smith MJ, Taylor V, Perrett DI. Sexual dimorphism in the female face is a cue to health and social status but not age. Pers. Individ. Differ. 2011;50:1068–1073. doi: 10.1016/j.paid.2011.01.026. DOI
Little AC, Jones BC, DeBruine LM. Facial attractiveness: evolutionary based research. Philos. Trans. R. Soc. B Biol. Sci. 2011;366:1638–1659. doi: 10.1098/rstb.2010.0404. PubMed DOI PMC
Hardy B. Steroid hormones in social science research. Biophys. Meas. Exp. Soc. Sci. Res. 2019 doi: 10.1016/b978-0-12-813092-6.00008-3. DOI
Boothroyd LG, et al. Facial masculinity is related to perceived age but not perceived health. Evol. Hum. Behav. 2005;26:417–431. doi: 10.1016/j.evolhumbehav.2005.01.001. DOI
Whitehouse AJO, et al. Prenatal testosterone exposure is related to sexually dimorphic facial morphology in adulthood. Proc. R. Soc. Lond. B Biol. Sci. 2015;282:20151351. PubMed PMC
Enlow DH, Hans MG, McGrew L. Essentials of facial growth. Philadelphia: Saunders; 1996.
Tanner JM. Fetus into Man: Physical Growth from Conception to Maturity. Berlin: Castlemead Publications; 1989.
Law Smith MJ, et al. Facial appearance is a cue to oestrogen levels in women. Proc. R. Soc. B Biol. Sci. 2006;273:135–140. doi: 10.1098/rspb.2005.3296. PubMed DOI PMC
Penton-Voak IS, Chen JY. High salivary testosterone is linked to masculine male facial appearance in humans. Evol. Hum. Behav. 2004;25:229–241. doi: 10.1016/j.evolhumbehav.2004.04.003. DOI
Rhodes G. The evolutionary psychology of facial beauty. Annu. Rev. Psychol. 2006;57:199–226. doi: 10.1146/annurev.psych.57.102904.190208. PubMed DOI
Verdonck A, Gaethofs M, Carels C, De Zegher F. Effect of low-dose testosterone treatment on craniofacial growth in boys with delayed puberty. Eur. J. Orthod. 1999;21:137–143. doi: 10.1093/ejo/21.2.137. PubMed DOI
Law Smith MJ, et al. Facial appearance is a cue to oestrogen levels in women. Proc. Biol. Sci. 2006;273:135–140. PubMed PMC
Folstad I, Karter AJ. Parasites, Bright Males, and the Immunocompetence Handicap. Am. Nat. 1992;139:603–622. doi: 10.1086/285346. DOI
Zahavi A. Mate selection-a selection for a handicap. J. Theor. Biol. 1975;53:205–214. doi: 10.1016/0022-5193(75)90111-3. PubMed DOI
Rantala MJ, et al. Evidence for the stress-linked immunocompetence handicap hypothesis in humans. Nat. Commun. 2012;3:694. doi: 10.1038/ncomms1696. PubMed DOI PMC
Muehlenbein MP, Bribiescas RG. Testosterone-mediated immune functions and male life histories. Am. J. Hum. Biol. 2005;17:527–558. doi: 10.1002/ajhb.20419. PubMed DOI
Scott IM, et al. Human preferences for sexually dimorphic faces may be evolutionarily novel. Proc. Natl. Acad. Sci. 2014 doi: 10.1073/pnas.1409643111. PubMed DOI PMC
Zaidi AA, et al. Facial masculinity does not appear to be a condition-dependent male ornament and does not reflect MHC heterozygosity in humans. Proc. Natl. Acad. Sci. USA. 2019;116:1633–1638. doi: 10.1073/pnas.1808659116. PubMed DOI PMC
Scott IML, Clark AP, Boothroyd LG, Penton-Voak IS. Do men’s faces really signal heritable immunocompetence? Behav. Ecol. 2013;24:579–589. doi: 10.1093/beheco/ars092. PubMed DOI PMC
Trebický V, Kleisner K, Havlícek J. Evolutionary concepts of human physical attractiveness: the case of male physique. Anthropologie. 2012;50:33.
Arnocky S, Bird BM, Perilloux C. An evolutionary perspective on characteristics of physical attractiveness in humans. In: Rennolds A, editor. Psychology of interpersonal perception and relationships. Hauppauge, NY: NOVA Publishers; 2014. pp. 115–155.
Swaddle JP, Reierson GW. Testosterone increases perceived dominance but not attractiveness in human males. Proc. R. Soc. Lond. B Biol. Sci. 2002;269:2285–2289. doi: 10.1098/rspb.2002.2165. PubMed DOI PMC
Mazur A, Booth A. Testosterone and dominance in men. Behav. Brain Sci. 1998;21:353–397. doi: 10.1017/S0140525X98001228. PubMed DOI
Gangestad SW, Simpson JA. The evolution of human mating: trade-offs and strategic pluralism. Behav. Brain Sci. 2000;23:573–587. doi: 10.1017/S0140525X0000337X. PubMed DOI
DeBruine LM, et al. Correlated preferences for facial masculinity and ideal or actual partner’s masculinity. Proc. R. Soc. B Biol. Sci. 2006;273:1355–1360. doi: 10.1098/rspb.2005.3445. PubMed DOI PMC
Johnston VS, Hagel R, Franklin M, Fink B, Grammer K. Male facial attractiveness: evidence for hormone-mediated adaptive design Victor. Evol. Hum. Behav. 2001;22:251–267. doi: 10.1016/S1090-5138(01)00066-6. DOI
Penton-Voak IS, et al. Symmetry, sexual dimorphism in facial proportions and male facial attractiveness. Proc. R. Soc. B Biol. Sci. 2001;268:1617–1623. doi: 10.1098/rspb.2001.1703. PubMed DOI PMC
Perrett DI, et al. Effects of sexual dimorphism on facial attractiveness. Nature. 1998;394:884–887. doi: 10.1038/29772. PubMed DOI
Rhodes G, Chan J, Zebrowitz LA, Simmons LW. Does sexual dimorphism in human faces signal health? Proc. Biol. Sci. 2003;270(Suppl):S93–S95. PubMed PMC
Todorov A, Christopher S, Verovsky SC. Personality impressions from facial appearance. In: Calder A, Rhodes G, Johnson M, Haxby J, editors. The Oxford Handbook of Face Perception. Oxford: Oxford University Press; 2011. pp. 631–652.
Little AC, Jones BC, Penton-Voak IS, Burt DM, Perrett DI. Partnership status and the temporal context of relationships influence human female preferences for sexual dimorphism in male face shape. Proc. R. Soc. B Biol. Sci. 2002;269:1095–1100. doi: 10.1098/rspb.2002.1984. PubMed DOI PMC
Stower RE, et al. Mating strategies and the masculinity paradox: how relationship context, relationship status, and sociosexuality shape women’s preferences for facial masculinity and beardedness. Arch. Sex. Behav. 2019;49:809–820. doi: 10.1007/s10508-019-1437-2. PubMed DOI
Holzleitner IJ, Perrett DI. Women’s preferences for men’s facial masculinity: trade-off accounts revisited. Adapt. Hum. Behav. Physiol. 2017;3:304–320. doi: 10.1007/s40750-017-0070-3. DOI
Zietsch BP, Lee AJ, Sherlock JM, Jern P. Variation in women’s preferences regarding male facial masculinity is better explained by genetic differences than by previously identified context-dependent effects. Psychol. Sci. 2015;26:1440–1448. doi: 10.1177/0956797615591770. PubMed DOI
Marcinkowska UM, et al. Cross-cultural variation in men’s preference for sexual dimorphism in women’s faces. Biol. Lett. 2014;10:4–7. doi: 10.1098/rsbl.2013.0850. PubMed DOI PMC
Jones D, Hill K. Criteria of facial attractiveness in five populations. Hum. Nat. 1993;4:271–296. doi: 10.1007/BF02692202. PubMed DOI
Scott I, Swami V, Josephson SC, Penton-Voak IS. Context-dependent preferences for facial dimorphism in a rural Malaysian population. Evol. Hum. Behav. 2008;29:289–296. doi: 10.1016/j.evolhumbehav.2008.02.004. DOI
Law Smith MJ, et al. Maternal tendencies in women are associated with estrogen levels and facial femininity. Horm. Behav. 2012;61:12–16. doi: 10.1016/j.yhbeh.2011.09.005. PubMed DOI
Penton-Voak IS, Jacobson A, Trivers R. Populational differences in attractiveness judgements of male and female faces: comparing British and Jamaican samples. Evol. Hum. Behav. 2004;25:355–370. doi: 10.1016/j.evolhumbehav.2004.06.002. DOI
Apicella CL, Tobolsky VA, Marlowe FW, Miller KW. Hadza hunter-gatherer men do not have more masculine digit ratios (2D: 4D) Am. J. Phys. Anthropol. 2016;159:223–232. doi: 10.1002/ajpa.22864. PubMed DOI
Sorokowski P, Sorokowska A, Fink B, Mberira M. Variable preferences for sexual dimorphism in stature (SDS) might not be universal: data from a semi-nomad population (Himba) in Namibia. J. Cross. Cult. Psychol. 2012;43:32–37. doi: 10.1177/0022022110395140. DOI
Sorokowski P, Sorokowska A, Danel D, Mberira ML, Pokrywka L. The second to fourth digit ratio and age at first marriage in semi-nomadic people from Namibia. Arch. Sex. Behav. 2012;41:703–710. doi: 10.1007/s10508-011-9866-6. PubMed DOI PMC
Coetzee V, Perrett DI, Stephen ID. Facial adiposity: a cue to health? Perception. 2009;38:1700–1711. doi: 10.1068/p6423. PubMed DOI
Coetzee V, Perrett DI. African and Caucasian body ideals in South Africa and the United States. Eat. Behav. 2011;12:72–74. doi: 10.1016/j.eatbeh.2010.09.006. PubMed DOI
Schneider TM, Hecht H, Carbon CC. Judging body weight from faces: the height-weight illusion. Perception. 2012;41:121–124. doi: 10.1068/p7140. PubMed DOI
Schneider TM, Hecht H, Stevanov J, Carbon CC. Cross-ethnic assessment of body weight and height on the basis of faces. Pers. Individ. Differ. 2013;55:356–360. doi: 10.1016/j.paid.2013.03.022. DOI
Holzleitner IJ, et al. Men’s facial masculinity: when (body) size matters. Perception. 2014;43:1191–1202. doi: 10.1068/p7673. PubMed DOI
Krams IA, et al. Body height affects the strength of immune response in young men, but not young women. Sci. Rep. 2014;4:6223. doi: 10.1038/srep06223. PubMed DOI PMC
Lee RB. The! Kung San: Men, Women, and Work in a Foraging Society. Cambridge: Cambridge University Press; 1979.
Marlowe FW. Mate preferences among Hadza hunter-gatherers. Hum. Nat. 2004;15:365–376. doi: 10.1007/s12110-004-1014-8. PubMed DOI
Sear R, Marlowe FW. How universal are human mate choices? Size does not matter when Hadza foragers are choosing a mate. Biol. Lett. 2009;5:606–609. doi: 10.1098/rsbl.2009.0342. PubMed DOI PMC
Shepperd JA, Strathman AJ. Attractiveness and height. Personal. Soc. Psychol. Bull. 1989;15:617–627. doi: 10.1177/0146167289154014. DOI
Stulp G, Barrett L. Evolutionary perspectives on human height variation. Biol. Rev. 2016;91:206–234. doi: 10.1111/brv.12165. PubMed DOI
Pierce CA. Body height and romantic attraction: a meta-analytic test of the male-taller norm. Soc. Behav. Pers. 1996;24:143–150. doi: 10.2224/sbp.1996.24.2.143. DOI
Gustafsson A, Lindenfors P. Human size evolution: no evolutionary allometric relationship between male and female stature. J. Hum. Evol. 2004;47:253–266. doi: 10.1016/j.jhevol.2004.07.004. PubMed DOI
Garvin HM, Sholts SB, Mosca LA. Sexual dimorphism in human cranial trait scores: effects of population, age, and body size. Am. J. Phys. Anthropol. 2014;154:259–269. doi: 10.1002/ajpa.22502. PubMed DOI
Bastir M, Godoy P, Rosas A. Common features of sexual dimorphism in the cranial airways of different human populations. Am. J. Phys. Anthropol. 2011;146:414–422. doi: 10.1002/ajpa.21596. PubMed DOI
Rosas A, Bastir M. Thin-plate spline analysis of allometry and sexual dimorphism in the human craniofacial complex. Am. J. Phys. Anthropol. 2002;117:236–245. doi: 10.1002/ajpa.10023. PubMed DOI
Kimmerle EH, Ross A, Slice D. Sexual dimorphism in America: geometric morphometric analysis of the craniofacial region. J. Forensic Sci. 2008;53:54–57. doi: 10.1111/j.1556-4029.2007.00627.x. PubMed DOI
Saribay SA, et al. The Bogazici face database: Standardized photographs of Turkish faces with supporting materials. PLoS ONE. 2018;13:e0192018. doi: 10.1371/journal.pone.0192018. PubMed DOI PMC
Danel DP, et al. A cross-cultural study of sex-typicality and averageness: correlation between frontal and lateral measures of human faces. Am. J. Hum. Biol. 2018;30:e23147. doi: 10.1002/ajhb.23147. PubMed DOI
Kleisner K, Kočnar T, Rubešová A, Flegr J. Eye color predicts but does not directly influence perceived dominance in men. Pers. Individ. Differ. 2010;49:59–64. doi: 10.1016/j.paid.2010.03.011. DOI
Kleisner K, et al. African and European perception of African female attractiveness. Evol. Hum. Behav. 2017;38:744–755. doi: 10.1016/j.evolhumbehav.2017.07.002. DOI
Kleisner K, Pokorný Š, Saribay SA. Toward a new approach to cross-cultural distinctiveness and typicality of human faces: the cross-group typicality/ distinctiveness metric. Front. Psychol. 2019;10:1–13. doi: 10.3389/fpsyg.2019.00124. PubMed DOI PMC
Valentova JV, Varella MAC, Havlíček J, Kleisner K. Positive association between vocal and facial attractiveness in women but not in men: a cross-cultural study. Behav. Process. 2017;135:95–100. doi: 10.1016/j.beproc.2016.12.005. PubMed DOI
Bookstein FL. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med. Image Anal. 1997;1:225–243. doi: 10.1016/S1361-8415(97)85012-8. PubMed DOI
Adams, D. C., Collyer, M. L. & Kaliontzopoulou, A. Geomorph: software for geometric morphometric analyses. R package version 3.1.0 (2019).
Collyer, M. L. & Adams, D. C. {RRPP}: linear model evaluation with randomized residuals in a permutation procedure. R package version 0.4.0 (2019).
Schlager, S. Morpho: calculations and visualisations related to geometric morphometrics. R package version 2.3.1.1 (2016).
Bookstein FL. Principal warps: thin-plate splines and the decomposition of deformations. IEEE Trans. Pattern Anal. Mach. Intell. 1989;11:567–585. doi: 10.1109/34.24792. DOI
James Rohlf F, Marcus LF. A revolution morphometrics. Trends Ecol. Evol. 1993;8:129–132. doi: 10.1016/0169-5347(93)90024-J. PubMed DOI
Komori M, Kawamura S, Ishihara S. Multiple mechanisms in the perception of face gender: effect of sex-irrelevant features. J. Exp. Psychol. Hum. Percept. Perform. 2011;37:626–633. doi: 10.1037/a0020369. PubMed DOI
Valenzano DR, Mennucci A, Tartarelli G, Cellerino A. Shape analysis of female facial attractiveness. Vision Res. 2006;46:1282–1291. doi: 10.1016/j.visres.2005.10.024. PubMed DOI
Mitteroecker P, Windhager S, Müller GB, Schaefer K. The morphometrics of" masculinity" in human faces. PLoS ONE. 2015;10:e0118374. doi: 10.1371/journal.pone.0118374. PubMed DOI PMC
Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 2017 doi: 10.18637/jss.v082.i13. DOI
McElreath, R. rethinking: statistical rethinking book package version 1.59 from GitHub. (2020).
Van den Berghe PL, Frost P. Skin color preference, sexual dimorphism and sexual selection: a case of gene culture co-evolution?*. Ethn. Racial Stud. 1986;9:87–113. doi: 10.1080/01419870.1986.9993516. DOI
Coetzee V, Greeff JM, Stephen ID, Perrett DI. Cross-cultural agreement in facial attractiveness preferences: the role of ethnicity and gender. PLoS ONE. 2014;9:e99629. doi: 10.1371/journal.pone.0099629. PubMed DOI PMC
Han C, et al. Cultural differences in preferences for facial coloration. Evol. Hum. Behav. 2018;39:154–159. doi: 10.1016/j.evolhumbehav.2017.11.005. DOI
Tan KW, Tiddeman B, Stephen ID. Skin texture and colour predict perceived health in Asian faces. Evol. Hum. Behav. 2018;39:320–335. doi: 10.1016/j.evolhumbehav.2018.02.003. DOI
Ardener EW. 101. Some Ibo attitudes to skin pigmentation. Man. 1954;54:71–73. doi: 10.2307/2793760. DOI
Wagatsuma H. The social perception of skin color in Japan. Daedalus. 1967;96:407–443.
De Barra M, DeBruine LM, Jones BC, Mahmud ZH, Curtis VA. Illness in childhood predicts face preferences in adulthood. Evol. Hum. Behav. 2013;34:384–389. doi: 10.1016/j.evolhumbehav.2013.07.001. DOI
Adhikari K, et al. A genome-wide association scan in admixed Latin Americans identifies loci influencing facial and scalp hair features. Nat. Commun. 2016;7:1–12. PubMed PMC
Carvalho-Silva DR, Santos FR, Rocha J, Pena SDJ. The phylogeography of Brazilian Y-chromosome lineages. Am. J. Hum. Genet. 2001;68:281–286. doi: 10.1086/316931. PubMed DOI PMC
Ackermann RR, Cheverud JM. Detecting genetic drift versus selection in human evolution. Proc. Natl. Acad. Sci. USA. 2004;101:17946–17951. doi: 10.1073/pnas.0405919102. PubMed DOI PMC
Weaver TD, Roseman CC, Stringer CB. Were neandertal and modern human cranial differences produced by natural selection or genetic drift? J. Hum. Evol. 2007;53:135–145. doi: 10.1016/j.jhevol.2007.03.001. PubMed DOI
Roseman CC. Random genetic drift, natural selection, and noise in human cranial evolution. Am. J. Phys. Anthropol. 2016;160:582–592. doi: 10.1002/ajpa.22918. PubMed DOI
Harvati K, Weaver TD. Human cranial anatomy and the differential preservation of population history and climate signatures. Anat. Rec. Part A Discov Mol. Cell. Evol. Biol. 2006;288:1225–1233. doi: 10.1002/ar.a.20395. PubMed DOI
Hubbe M, Hanihara T, Harvati K. Climate signatures in the morphological differentiation of worldwide modern human populations. Anat. Rec. 2009;292:1720–1733. doi: 10.1002/ar.20976. PubMed DOI
Froment A, Hiernaux J. Climate-associated anthropometric variation between populations of the Niger bend. Ann. Hum. Biol. 1984;11:189–200. doi: 10.1080/03014468400007061. PubMed DOI
Mariak Z, White MD, Lewko J, Lyson T, Piekarski P. Direct cooling of the human brain by heat loss from the upper respiratory tract. J. Appl. Physiol. 1999;87:1609–1613. doi: 10.1152/jappl.1999.87.5.1609. PubMed DOI
Maddux SD, Yokley TR, Svoma BM, Franciscus RG. Absolute humidity and the human nose: a reanalysis of climate zones and their influence on nasal form and function. Am. J. Phys. Anthropol. 2016;161:309–320. doi: 10.1002/ajpa.23032. PubMed DOI
Strom MA, Zebrowitz LA, Zhang S, Bronstad PM, Lee HK. Skin and bones: The contribution of skin tone and facial structure to racial prototypicality ratings. PLoS ONE. 2012;7:e41193. doi: 10.1371/journal.pone.0041193. PubMed DOI PMC
White MD, Greiner JG, McDonald PLL. Point: humans do demonstrate selective brain cooling during hyperthermia. J. Appl. Physiol. 2011;110:569–571. doi: 10.1152/japplphysiol.00992.2010. PubMed DOI
Marzoli D, Havlíček J, Roberts SC. Human mating strategies: from past causes to present consequences. Wiley Interdiscip. Rev. Cogn. Sci. 2018;9:e1456. doi: 10.1002/wcs.1456. PubMed DOI
Scelza BA, Prall SP. Partner preferences in the context of concurrency: what Himba want in formal and informal partners. Evol. Hum. Behav. 2018;39:212–219. doi: 10.1016/j.evolhumbehav.2017.12.005. DOI
Hill AK, et al. Quantifying the strength and form of sexual selection on men’s traits. Evol. Hum. Behav. 2013;34:334–341. doi: 10.1016/j.evolhumbehav.2013.05.004. DOI
Larson JR, et al. Body size and allometric variation in facial shape in children. Am. J. Phys. Anthropol. 2018;165:327–342. doi: 10.1002/ajpa.23356. PubMed DOI PMC
Boothroyd LG, et al. Male facial appearance and offspring mortality in two traditional societies. PLoS ONE. 2017;12:e0169181. doi: 10.1371/journal.pone.0169181. PubMed DOI PMC
Van Dongen S. Fluctuating asymmetry and masculinity/femininity in humans: a meta-analysis. Arch. Sex. Behav. 2012;41:1453–1460. doi: 10.1007/s10508-012-9917-7. PubMed DOI
Sexual Dimorphism: The Interrelation of Shape and Color