Immunoactivation Affects Perceived Body Odor and Facial but Not Vocal Attractiveness
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články
PubMed
38087426
PubMed Central
PMC10722934
DOI
10.1177/14747049231218010
Knihovny.cz E-zdroje
- Klíčová slova
- face, health status, olfaction, perception, voice,
- MeSH
- hlas * fyziologie MeSH
- krása MeSH
- lidé MeSH
- obličej MeSH
- podněty MeSH
- tělesný pach * MeSH
- Check Tag
- lidé MeSH
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
Several previous studies have shown that in mammals, the health status of conspecifics can be assessed based on perceptual cues. Olfactory, visual, or acoustic cues may lead to avoidant behavior, thus reducing the risk of contagion by close contact with infected individuals. We tested whether immune system activation after immunization leads to perceptible changes in body odor and facial and vocal attractiveness in humans. We have experimentally activated the immune system of male participants using vaccination against hepatitis A/B and meningococcus. Their body odor, facial photographs, and vocal recordings were collected before and 14 days after vaccination. Subsequently, the body odor samples, facial photographs, and vocal recordings were assessed by female raters for their attractiveness and healthiness. We have also measured skin coloration (from facial photographs and in vivo using a spectrophotometer), vocal parameters, and C-reactive protein (CRP) levels as a marker of inflammation. We found an increase in perceived body odor attractiveness, a decrease in facial attractiveness and healthiness, and no change in vocal attractiveness 14 days after vaccination compared to the prevaccination condition. Moreover, there was no change in facial coloration or vocal parameters between the prevaccination and postvaccination conditions. Prevaccination CRP levels were negatively associated with body odor and facial attractiveness and positively associated with body odor intensity. Overall, our results suggest that perceived body odor as well as facial but not vocal attractiveness may provide cues to activation of the immune response and that each modality may carry specific information about the individual's condition.
Department of Zoology Faculty of Science Charles University Prague Czech Republic
Faculty of Physical Education and Sport Charles University Prague Czech Republic
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Albert G., Arnocky S., Puts D. A., Hodges-Simeon C. R. (2021). Can listeners assess men's self-reported health from their voice? Evolution and Human Behavior, 42(2), 91–103. 10.1016/j.evolhumbehav.2020.08.001 DOI
Altizer S., Nunn C. L., Thrall P. H., Gittleman J. L., Antonovics J., Cunningham A. A., Dobson A. P., Ezenwa V., Jones K. E., Pedersen A. B., Poss M., Pulliam J. R. C. (2003). Social organization and parasite risk in mammals: Integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics, 34(1), 517–547. 10.1146/annurev.ecolsys.34.030102.151725 DOI
Arakawa H., Arakawa K., Deak T. (2009). Acute illness induces the release of aversive odor cues from adult, but not prepubertal, male rats and suppresses social investigation by conspecifics. Behavioral Neuroscience, 123(5), 964–978. 10.1037/a0017114 PubMed DOI
Arakawa H., Arakawa K., Deak T. (2010). Sickness-related odor communication signals as determinants of social behavior in rat: A role for inflammatory processes. Hormones and Behavior, 57(3), 330–341. 10.1016/j.yhbeh.2010.01.002 PubMed DOI
Arnocky S., Hodges-Simeon C. R., Ouellette D., Albert G. (2018). Do men with more masculine voices have better immunocompetence? Evolution and Human Behavior, 39(6), 602–610. 10.1016/j.evolhumbehav.2018.06.003 DOI
Arshamian A., Sundelin T., Wnuk E., O'Meara C., Burenhult N., Rodriguez G. G., Lekander M., Olsson M. J., Lasselin J., Axelsson J., Majid A. (2021). Human sickness detection is not dependent on cultural experience. Proceedings of the Royal Society B: Biological Sciences, 288(1954), 20210922. 10.1098/rspb.2021.0922 PubMed DOI PMC
Axelsson J., Sundelin T., Olsson M. J., Sorjonen K., Axelsson C., Lasselin J., Lekander M. (2018). Identification of acutely sick people and facial cues of sickness. Proceedings of the Royal Society B: Biological Sciences, 285(1870), 20172430. 10.1098/rspb.2017.2430 PubMed DOI PMC
Balasubramanium R. K., Bhat J. S., Srivastava M., Eldose A. (2012). Cepstral analysis of sexually appealing voice. Journal of Voice, 26(4), 412–415. 10.1016/j.jvoice.2011.03.011 PubMed DOI
Bozzola E., Spina G., Russo R., Bozzola M., Corsello G., Villani A. (2018). Mandatory vaccinations in European countries, undocumented information, false news and the impact on vaccination uptake: The position of the Italian pediatric society. Italian Journal of Pediatrics, 44(1), 67. 10.1186/s13052-018-0504-y PubMed DOI PMC
Brand G., Millot J. L. (2001). Sex differences in human olfaction: Between evidence and enigma. The Quarterly Journal of Experimental Psychology Section B, 54(3b), 259–270. 10.1080/02724990143000045 PubMed DOI
Brown T. A. (2015). Confirmatory factor analysis for applied research. Guilford Publications.
Brown W. V., Fujioka K., Wilson P. W., Woodworth K. A. (2009). Obesity: Why be concerned? The American Journal of Medicine, 122(4 Suppl 1), S4–11. PubMed
Cai Z., Hahn A. C., Zhang W., Holzleitner I. J., Lee A. J., DeBruine L. M., Jones B. C. (2019). No evidence that facial attractiveness, femininity, averageness, or coloration are cues to susceptibility to infectious illnesses in a university sample of young adult women. Evolution and Human Behavior, 40(2), 156–159. 10.1016/j.evolhumbehav.2018.10.002 DOI
Coetzee V., Perrett D. I., Stephen I. D. (2009). Facial adiposity: A cue to health? Perception, 38(11), 1700–1711. 10.1068/p6423 PubMed DOI
De Jager S., Coetzee N., Coetzee V. (2018). Facial adiposity, attractiveness, and health: A review. Frontiers in Psychology, 9, 2562. 10.3389/fpsyg.2018.02562 PubMed DOI PMC
De Paula V. S. (2012). Laboratory diagnosis of hepatitis A. Future Virology, 7(5), 461–472. 10.2217/fvl.12.35 DOI
Di Pasquale A., Bonanni P., Garçon N., Stanberry L. R., El-Hodhod M., Da Silva F. T. (2016). Vaccine safety evaluation: Practical aspects in assessing benefits and risks. Vaccine, 34(52), 6672–6680. 10.1016/j.vaccine.2016.10.039 PubMed DOI
Eadie T. L., Baylor C. R. (2006). The effect of perceptual training on inexperienced listeners’ judgments of dysphonic voice. Journal of Voice, 20(4), 527–544. 10.1016/j.jvoice.2005.08.007 PubMed DOI
Feinberg D. (2022). VoiceLab: Automated reproducible acoustical analysis (1.2.0) [Windows]. https://github.com/Voice-Lab/VoiceLab
Feinberg D. R., Cook O. (2020). VoiceLab: Automated reproducible acoustic analysis. PsyArXiv. 10.31234/osf.io/v5uxf DOI
Ferdenzi C., Delplanque S., Atanassova R., Sander D. (2016). Androstadienone’s influence on the perception of facial and vocal attractiveness is not sex specific. Psychoneuroendocrinology, 66, 166–175. 10.1016/j.psyneuen.2016.01.016 PubMed DOI
Fink B., Grammer K., Matts P. J. (2006). Visible skin color distribution plays a role in the perception of age, attractiveness, and health in female faces. Evolution and Human Behavior, 27(6), 433–442. 10.1016/j.evolhumbehav.2006.08.007 DOI
Galson J. D., Trück J., Fowler A., Clutterbuck E. A., Münz M., Cerundolo V., Reinhard C., van der Most R., Pollard A. J., Lunter G., Kelly D. F. (2015). Analysis of B cell repertoire dynamics following hepatitis B vaccination in humans, and enrichment of vaccine-specific antibody sequences. EBioMedicine, 2(12), 2070–2079. 10.1016/j.ebiom.2015.11.034 PubMed DOI PMC
Goodall J. (1986). Social rejection, exclusion, and shunning among the Gombe chimpanzees. Ethology and Sociobiology, 7(3-4), 227–236. 10.1016/0162-3095(86)90050-6 DOI
Groyecka A., Pisanski K., Sorokowska A., Havlíček J., Karwowski M., Puts D., Roberts S. C., Sorokowski P. (2017). Attractiveness is multimodal: Beauty is also in the nose and ear of the beholder. Frontiers in Psychology, 8, 778. 10.3389/fpsyg.2017.00778 PubMed DOI PMC
Hamilton W. D., Zuk M. (1982). Heritable true fitness and bright birds: A role for parasites? Science, 218(4570), 384–387. 10.1126/science.7123238 PubMed DOI
Havlíček J., Lenochová P., Oberzaucher E., Grammer K., Roberts S. C. (2011). Does length of sampling affect quality of body odor samples? Chemosensory Perception, 4(4), 186–194. 10.1007/s12078-011-9104-6 DOI
Havlicek J., Lenochova P. (2006). The effect of meat consumption on body odor attractiveness. Chemical Senses, 31(8), 747–752. 10.1093/chemse/bjl017 PubMed DOI
Havlicek J., Saxton T. K., Roberts S. C., Jozifkova E., Lhota S., Valentova J., Flegr J. (2008). He sees, she smells? Male and female reports of sensory reliance in mate choice and non-mate choice contexts. Personality and Individual Differences, 45(6), 565–570. 10.1016/j.paid.2008.06.019 DOI
Hehman E., Leitner J. B., Gaertner S. L. (2013). Enhancing static facial features increases intimidation. Journal of Experimental Social Psychology, 49(4), 747–754. 10.1016/j.jesp.2013.02.015 DOI
Henderson A. J., Holzleitner I. J., Talamas S. N., Perrett D. I. (2016). Perception of health from facial cues. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1693), 20150380. 10.1098/rstb.2015.0380 PubMed DOI PMC
Henderson A. J., Lasselin J., Lekander M., Olsson M. J., Powis S. J., Axelsson J., Perrett D. I. (2017). Skin colour changes during experimentally-induced sickness. Brain, Behavior, and Immunity, 60, 312–318. 10.1016/j.bbi.2016.11.008 PubMed DOI
Huang W. S., Wang Y. W., Hung K. C., Hsieh P. S., Fu K. Y., Dai L. G., Liou N.-H., Ma K.-H., Liu J.-C., Dai N. T. (2018). High correlation between skin color based on CIELAB color space, epidermal melanocyte ratio, and melanocyte melanin content. PeerJ, 6, e4815. 10.7717/peerj.4815 PubMed DOI PMC
Hunter R. S. (1958). Photoelectric color difference meter. Journal of the Optical Society of America, 48(12), 985–995. 10.1364/JOSA.48.000985 DOI
Kohoutová D., Rubešová A., Havlíček J. (2012). Shaving of axillary hair has only a transient effect on perceived body odor pleasantness. Behavioral Ecology and Sociobiology, 66(4), 569–581. 10.1007/s00265-011-1305-0 DOI
Krams I. A., Skrinda I., Kecko S., Moore F. R., Krama T., Kaasik A., Meija L., Lietuvietis V., Rantala M. J. (2014). Body height affects the strength of immune response in young men, but not young women. Scientific Reports, 4(1), 6223. 10.1038/srep06223 PubMed DOI PMC
Lenochova P., Roberts S. C., Havlicek J. (2009). Methods of human body odor sampling: The effect of freezing. Chemical Senses, 34(2), 127–138. 10.1093/chemse/bjn067 PubMed DOI
Lopes P. C., König B. (2016). Choosing a healthy mate: Sexually attractive traits as reliable indicators of current disease status in house mice. Animal Behaviour, 111, 119–126. 10.1016/j.anbehav.2015.10.011 DOI
Martinec Nováková L., Havlíček J., Roberts S. C. (2014). Olfactory processing and odor specificity: A meta-analysis of menstrual cycle variation in olfactory sensitivity. Anthropological Review, 77, 331–345. 10.2478/anre-2014-0024 DOI
Michalak N. M., Sng O., Wang I. M., Ackerman J. (2020). Sounds of sickness: Can people identify infectious disease using sounds of coughs and sneezes? Proceedings of the Royal Society B: Biological Sciences, 287(1928), 20200944. 10.1098/rspb.2020.0944 PubMed DOI PMC
Moller A. P., Pomiankowski A. (1993). Why have birds got multiple sexual ornaments? Behavioral Ecology and Sociobiology, 32(3), 167–176. 10.1007/BF00173774 DOI
Moshkin M., Litvinova N., Litvinova E. A., Bedareva A., Lutsyuk A., Gerlinskaya L. (2012). Scent recognition of infected status in humans. The Journal of Sexual Medicine, 9(12), 3211–3218. 10.1111/j.1743-6109.2011.02562.x PubMed DOI
Olsson M. J., Lundström J. N., Kimball B. A., Gordon A. R., Karshikoff B., Hosseini N., Sorjonen K., Olgart Höglund C., Solares C., Soop A., Axelsson J., Lekander M. (2014). The scent of disease: Human body odor contains an early chemosensory cue of sickness. Psychological Science, 25(3), 817–823. 10.1177/0956797613515681 PubMed DOI
Palm N. W., Medzhitov R. (2007). Not so fast: Adaptive suppression of innate immunity. Nature Medicine, 13(10), 1142–1144. 10.1038/nm1007-1142b PubMed DOI PMC
Pátková Ž, Schwambergová D., Třebická Fialová J., Třebický V., Stella D., Kleisner K., Havlíček J. (2022). Attractive and healthy-looking male faces do not show higher immunoreactivity. Scientific Reports, 12(1), 18432. 10.1038/s41598-022-22866-x PubMed DOI PMC
Pawłowski B., Nowak J., Borkowska B., Augustyniak D., Drulis-Kawa Z. (2017). Body height and immune efficacy: Testing body stature as a signal of biological quality. Proceedings of the Royal Society B: Biological Sciences, 284(1859), 20171372. 10.1098/rspb.2017.1372 PubMed DOI PMC
Peirce J., Gray J., Halchenko Y., Britton D., Rokem A., Strangman G. (2011). PsychoPy—A Psychology Software in Python.
Penn D., Potts W. K. (1998). Chemical signals and parasite-mediated sexual selection. Trends in Ecology & Evolution, 13(10), 391–396. 10.1016/S0169-5347(98)01473-6 PubMed DOI
Phalane K. G., Tribe C., Steel H. C., Cholo M. C., Coetzee V. (2017). Facial appearance reveals immunity in African men. Scientific reports, 7(1), 7443. 10.1038/s41598-017-08015-9 PubMed DOI PMC
Pisanski K., Mishra S., Rendall D. (2012). The evolved psychology of voice: Evaluating interrelationships in listeners’ assessments of the size, masculinity, and attractiveness of unseen speakers. Evolution and Human Behavior, 33(5), 509–519. 10.1016/j.evolhumbehav.2012.01.004 DOI
Rantala M. J., Coetzee V., Moore F. R., Skrinda I., Kecko S., Krama T., Kivleniece I., Krams I. (2013). Facial attractiveness is related to women's cortisol and body fat, but not with immune responsiveness. Biology Letters, 9(4), 20130255. 10.1098/rsbl.2013.0255 PubMed DOI PMC
Regenbogen C., Axelsson J., Lasselin J., Porada D. K., Sundelin T., Peter M. G., Lekander M., Lundström J. N., Olsson M. J. (2017). Behavioral and neural correlates to multisensory detection of sick humans. Proceedings of the National Academy of Sciences of the USA, 114(24), 6400–6405. 10.1073/pnas.1617357114 PubMed DOI PMC
Reinberg A., Lagoguey M., Cesselin F., Touitou Y., Legrand J. C., Delassalle A., Antreassian J., Lagoguey A. (1978). Circadian and circannual rhythms in plasma hormones and other variables of five healthy young human males. European Journal of Endocrinology, 88(3), 417–427. 10.1530/acta.0.0880417 PubMed DOI
Sarabian C., Ngoubangoye B., MacIntosh A. J. (2017). Avoidance of biological contaminants through sight, smell and touch in chimpanzees. Royal Society Open Science, 4(11), 170968. 10.1098/rsos.170968 PubMed DOI PMC
Sarolidou G., Tognetti A., Lasselin J., Regenbogen C., Lundström J. N., Kimball B. A., Garke M., Lekander M., Axelsson J., Olsson M. J. (2020). Olfactory communication of sickness cues in respiratory infection. Frontiers in Psychology, 11, 1004. 10.3389/fpsyg.2020.01004 PubMed DOI PMC
Schaller M., Park J. H. (2011). The behavioral immune system (and why it matters). Current Directions in Psychological Science, 20(2), 99–103. 10.1177/0963721411402596 DOI
Schwambergová D., Sorokowska A., Slámová Ž, Fialová J. T., Sabiniewicz A., Nowak-Kornicka J., Borkowska B., Pawłowski B., Havlíček J. (2021). No evidence for association between human body odor quality and immune system functioning. Psychoneuroendocrinology, 132, 105363. 10.1016/j.psyneuen.2021.105363 PubMed DOI
Schwambergová D., Třebická Fialová J., Havlíček J. (2023). Olfactory mediated pathogen avoidance in mammals. In Schaal B., Keller M., Rekow D. (Eds.), Chemical signals in vertebrates XV (pp. 207–232). Springer Nature.
Šebesta P., Kleisner K., Tureček P., Kočnar T., Akoko R. M., Třebický V., Havlíček J. (2017). Voices of Africa: Acoustic predictors of human male vocal attractiveness. Animal Behaviour, 127, 205–211. 10.1016/j.anbehav.2017.03.014 DOI
Shattuck E. C., Muehlenbein M. P. (2015). Human sickness behavior: Ultimate and proximate explanations. American Journal of Physical Anthropology, 157(1), 1–18. 10.1002/ajpa.22698 PubMed DOI
Shepard C. W., Simard E. P., Finelli L., Fiore A. E., Bell B. P. (2006). Hepatitis B virus infection: Epidemiology and vaccination. Epidemiologic Reviews, 28(1), 112–125. 10.1093/epirev/mxj009 PubMed DOI
Skrinda I., Krama T., Kecko S., Moore F. R., Kaasik A., Meija L., Lietuvietis V., Rantala M. J., Krams I. (2014). Body height, immunity, facial and vocal attractiveness in young men. Naturwissenschaften, 101(12), 1017–1025. 10.1007/s00114-014-1241-8 PubMed DOI
Sorokowska A., Sorokowski P., Hilpert P., Cantarero K., Frackowiak T., Ahmadi K., Alghraibeh A. M., Aryeetey R., Bertoni A., Bettache K., Blumen S., Błażejewska M., Bortolini T., Butovskaya M., Castro F. N., Cetinkaya H., Cunha D., David D., David O. A., Dileym F. A., …, Pierce J. D. (2017). Preferred interpersonal distances: A global comparison. Journal of Cross-Cultural Psychology, 48(4), 577–592. 10.1177/0022022117698039 DOI
Sproston N. R., Ashworth J. J. (2018). Role of C-reactive protein at sites of inflammation and infection. Frontiers in Immunology, 9, 754. 10.3389/fimmu.2018.00754 PubMed DOI PMC
Stephen I. D., Luoto S. (2023). Physical cues of partner quality. In Mogilski J. K., Shackelford T. K. (Eds.), The Oxford handbook of evolutionary psychology and romantic relationships (pp. 42–73). Oxford University Press.
Třebický V., Delplanque S., Ferdenzi C., Fink B., Jelínková L., Pátková Ž, Craig Roberts S., Röder S., Saxton T. K., Schwambergová D., Štěrbová Z., Fialová J. T., Havlíček J. (2022). Cross-modal associations of human body odour attractiveness with facial and vocal attractiveness provide little support for the backup signals hypothesis: A systematic review and meta-analysis. Evolution and Human Behavior, 44(1), 19–29. 10.1016/j.evolhumbehav.2022.11.001 DOI
Třebický V., Fialová J., Kleisner K., Havlíček J. (2016). Focal length affects depicted shape and perception of facial images. PLoS One, 11(2), e0149313. 10.1371/journal.pone.0149313 PubMed DOI PMC
Třebický V., Fialová J., Stella D., Coufalová K., Pavelka R., Kleisner K., Kuba R., Štěrbová Z., Havlíček J. (2019). Predictors of fighting ability inferences based on faces. Frontiers in Psychology, 9, 2740. 10.3389/fpsyg.2018.02740 PubMed DOI PMC
Třebický V., Fialová J., Stella D., Štěrbová Z., Kleisner K., Havlíček J. (2018). 360 Degrees of facial perception: Congruence in perception of frontal portrait, profile, and rotation photographs. Frontiers in Psychology, 9, 2405. 10.3389/fpsyg.2018.02405 PubMed DOI PMC
Xu M., Homae F., Hashimoto R. I., Hagiwara H. (2013). Acoustic cues for the recognition of self-voice and other-voice. Frontiers in Psychology, 4, 735. 10.3389/fpsyg.2013.00735 PubMed DOI PMC
Żelaźniewicz A., Nowak J., Łącka P., Pawłowski B. (2020). Facial appearance and metabolic health biomarkers in women. Scientific Reports, 10(1), 13067. 10.1038/s41598-020-70119-6 PubMed DOI PMC
Zuk M., Thornhill R., Ligon J. D., Johnson K. (1990). Parasites and mate choice in red jungle fowl. American Zoologist, 30(2), 235–244. 10.1093/icb/30.2.235 DOI