{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,13]],"date-time":"2026-05-13T04:49:16Z","timestamp":1778647756580,"version":"3.51.4"},"reference-count":50,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2021,7,15]],"date-time":"2021-07-15T00:00:00Z","timestamp":1626307200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001381","name":"National Research Foundation Singapore","doi-asserted-by":"publisher","award":["NRF-CRP 20-2017-0001"],"award-info":[{"award-number":["NRF-CRP 20-2017-0001"]}],"id":[{"id":"10.13039\/501100001381","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Symmetry"],"abstract":"<jats:p>Comparative examinations of external eye morphology in primates initially focused on communicative functions of the eye. Subsequent work has failed to find consistent associations between specific eye morphologies and communicative functions. In this article, we review the field of primate external eye morphology and inspect publicly available and unpublished photographs. We identify and describe five commonly occurring traits that have not received attention so far. We cross-examined the clinical and psychological literature to propose potential adaptive functions. These potential adaptive functions include communicative functions, but also photoregulatory functions and photoprotective functions.<\/jats:p>","DOI":"10.3390\/sym13071270","type":"journal-article","created":{"date-parts":[[2021,7,15]],"date-time":"2021-07-15T09:32:07Z","timestamp":1626341527000},"page":"1270","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Diversity in Primate External Eye Morphology: Previously Undescribed Traits and Their Potential Adaptive Value"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6559-0652","authenticated-orcid":false,"given":"Juan Olvido","family":"Perea-Garc\u00eda","sequence":"first","affiliation":[{"name":"Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6175-3928","authenticated-orcid":false,"given":"Dariusz P.","family":"Danel","sequence":"additional","affiliation":[{"name":"Department of Anthropology, Hirszfeld Institute of Immunology and Experimental Therapy Polish Academy of Sciences, ul. Rudolfa Weigla 12, 53-114 Wroclaw, Poland"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9696-459X","authenticated-orcid":false,"given":"Ant\u00f3nia","family":"Monteiro","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore"},{"name":"Science Division, Yale-NUS College, Singapore 138609, Singapore"}]}],"member":"1968","published-online":{"date-parts":[[2021,7,15]]},"reference":[{"key":"ref_1","first-page":"767","article-title":"Unique morphology of the human eye","volume":"387","author":"Kobayashi","year":"1997","journal-title":"Nat. Cell Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1006\/jhev.2001.0468","article-title":"Unique morphology of the human eye and its adaptive meaning: Comparative studies on external morphology of the primate eye","volume":"40","author":"Kobayashi","year":"2001","journal-title":"J. Hum. Evol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1023\/A:1014913532057","article-title":"Patterns of Gazing in Orangutans (Pongo pygmaeus)","volume":"23","author":"Kaplan","year":"2002","journal-title":"Int. J. Primatol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00265-020-02894-1","article-title":"Sex differences in ocular morphology in Caucasian people: A dubious role of sexual selection in the evolution of sexual dimorphism of the human eye","volume":"74","author":"Danel","year":"2020","journal-title":"Behav. Ecol. Sociobiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"869","DOI":"10.1002\/ajp.22411","article-title":"Gorillas with white sclera: A naturally occurring variation in a morphological trait linked to social cognitive functions","volume":"77","author":"Mayhew","year":"2015","journal-title":"Am. J. Primatol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1093\/jole\/lzw004","article-title":"Quantifying ocular morphologies in extant primates for reliable interspecific comparisons","volume":"1","year":"2016","journal-title":"J. Lang. Evol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"19248","DOI":"10.1073\/pnas.1911410116","article-title":"Scleral pigmentation leads to conspicuous, not cryptic, eye morphology in chimpanzees","volume":"116","author":"Kret","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_8","first-page":"1","article-title":"Not everything is blue or brown: Quantification of ocular coloration in psychological research beyond dichotomous categorizations","volume":"10","author":"Grenzner","year":"2017","journal-title":"Commun. Integr. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-021-92348-z","article-title":"Ocular pigmentation in humans, great apes, and gibbons is not suggestive of communicative functions","volume":"11","author":"Caspar","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"103043","DOI":"10.1016\/j.jhevol.2021.103043","article-title":"Quantifying gaze conspicuousness: Are humans distinct from chimpanzees and bonobos?","volume":"157","author":"Mearing","year":"2021","journal-title":"J. Hum. Evol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"E1069","DOI":"10.1097\/OPX.0b013e3181b4f010","article-title":"Appearance of the human eye: Optical contributions to the \u2018limbal ring\u2019","volume":"86","author":"Shyu","year":"2009","journal-title":"Optom. Vis. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1136\/bjophthalmol-2011-300550","article-title":"In vivo confocal microscopic features of normal limbus","volume":"96","author":"Miri","year":"2012","journal-title":"Br. J. Ophthalmol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1101\/gad.314351.118","article-title":"The impact of mitotic errors on cell proliferation and tumorigenesis","volume":"32","author":"Levine","year":"2018","journal-title":"Genes Dev."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1097\/ICL.0b013e318223394e","article-title":"Ultraviolet Radiation and the Anterior Eye","volume":"37","author":"Coroneo","year":"2011","journal-title":"Eye Contact Lens Sci. Clin. Pract"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1139\/bcb-2012-0082","article-title":"Phenotypic alteration of limbal niche\u2013associated limbal epithelial stem cell deficiency by ultraviolet-B exposure\u2013induced phototoxicity in mice","volume":"91","author":"Das","year":"2013","journal-title":"Biochem. Cell Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1177\/147470491100900201","article-title":"Preliminary Evidence that the Limbal Ring Influences Facial Attractiveness","volume":"9","author":"Peshek","year":"2011","journal-title":"Evol. Psychol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1016\/j.ijresmar.2016.02.001","article-title":"White eyes are the window to the pure soul: Metaphorical association and overgeneralization effects for spokespeople with limbal rings","volume":"33","author":"Ilicic","year":"2016","journal-title":"Int. J. Res. Mark."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1177\/0146167217733072","article-title":"Put a (Limbal) Ring on It: Women Perceive Men\u2019s Limbal Rings as a Health Cue in Short-Term Mating Domains","volume":"44","author":"Brown","year":"2017","journal-title":"Pers. Soc. Psychol. Bull."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1037\/ebs0000135","article-title":"Women\u2019s short-term mating goals elicit avoidance of faces whose eyes lack limbal rings","volume":"13","author":"Brown","year":"2019","journal-title":"Evol. Behav. Sci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1007\/s40806-019-00205-0","article-title":"Perfectionism and Relationship Status Influence Health Evaluations of Faces with Limbal Rings","volume":"5","author":"Sacco","year":"2019","journal-title":"Evol. Psychol. Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1111\/pere.12308","article-title":"Relational insecurity heightens sensitivity to limbal rings in partnered women","volume":"27","author":"Brown","year":"2020","journal-title":"Pers. Relatsh."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Oie, Y., and Nishida, K. (2013). Regenerative Medicine for the Cornea. BioMed Res. Int., 2013.","DOI":"10.1155\/2013\/428247"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Christoffersen, M., Frikke-Schmidt, R., Schnohr, P., Jensen, G.B., Nordestgaard, B.G., and Tybj\u00e6rg-Hansen, A. (2011). Xanthelasmata, arcus corneae, and ischaemic vascular disease and death in general population: Prospective cohort study. BMJ, 343.","DOI":"10.1136\/bmj.d5497"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.amjmed.2012.10.001","article-title":"White Rings: Arcus Lipoides","volume":"126","author":"Brenes","year":"2013","journal-title":"Am. J. Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1037\/1528-3542.7.4.724","article-title":"Processing of observed pupil size modulates perception of sadness and predicts empathy","volume":"7","author":"Harrison","year":"2007","journal-title":"Emotion"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1080\/02699931.2017.1370417","article-title":"The role of pupil size in communication. Is there room for learning?","volume":"32","author":"Kret","year":"2017","journal-title":"Cogn. Emot."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Behrens, F., Moulder, R.G., Boker, S.M., and Kret, M. (2020). Quantifying physiological synchrony through windowed cross-correlation analysis: Statistical and theoretical considerations. BioRxiv.","DOI":"10.1101\/2020.08.27.269746"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"20162554","DOI":"10.1098\/rspb.2016.2554","article-title":"Pupil-mimicry conditions trust in partners: Moderation by oxytocin and group membership","volume":"284","author":"Kret","year":"2017","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"9601","DOI":"10.1038\/s41598-017-08223-3","article-title":"Human eyes with dilated pupils induce pupillary contagion in infants","volume":"7","author":"Fawcett","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Kret, M.E., Tomonaga, M., and Matsuzawa, T. (2014). Chimpanzees and humans mimic pupil-size of conspecifics. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0104886"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1097\/OPX.0b013e3182059ef3","article-title":"Perceived Direction of Gaze from Eyes with Dark vs. Light Irises","volume":"88","author":"West","year":"2011","journal-title":"Optom. Vis. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"676","DOI":"10.3389\/fpsyg.2021.632616","article-title":"Sclera and Iris Color Interact to Influence Gaze Perception","volume":"12","author":"Yorzinski","year":"2021","journal-title":"Front. Psychol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1002\/ajpa.22280","article-title":"The convergent evolution of blue iris pigmentation in primates took distinct molecular paths","volume":"151","author":"Meyer","year":"2013","journal-title":"Am. J. Phys. Anthr."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.biopsycho.2007.01.007","article-title":"Associations between iris characteristics and personality in adulthood","volume":"75","author":"Larsson","year":"2007","journal-title":"Biol. Psychol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1007\/s10329-006-0021-2","article-title":"Preliminary study on eye colour in Japanese macaques (Macaca fuscata) in their natural habitat","volume":"48","author":"Zhang","year":"2006","journal-title":"Primates"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.evolhumbehav.2005.07.002","article-title":"European hair and eye color: A case of frequency-dependent sexual selection?","volume":"27","author":"Frost","year":"2006","journal-title":"Evol. Hum. Behav."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1002\/ajpa.21010","article-title":"Brief communication: Blue eyes in lemurs and humans: Same phenotype, different genetic mechanism","volume":"139","author":"Bradley","year":"2009","journal-title":"Am. J. Phys. Anthr."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1002\/da.1083","article-title":"Depressive symptomatology differentiates subgroups of patients with seasonal affective disorder","volume":"15","author":"Goel","year":"2002","journal-title":"Depress. Anxiety"},{"key":"ref_39","first-page":"180002","article-title":"Blue Eyes Keep away the Winter Blues: Is Blue Eye Pigmentation an Evolved Feature to Provide Resilience to Seasonal Affective Disorder","volume":"1","author":"Workman","year":"2018","journal-title":"OA J. Behav. Sci. Psychol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1159\/000477093","article-title":"Blue-Enriched Morning Light as a Countermeasure to Light at the Wrong Time: Effects on Cognition, Sleepiness, Sleep, and Circadian Phase","volume":"74","author":"Nowozin","year":"2016","journal-title":"Neuropsychobiology"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e201900102","DOI":"10.1002\/jbio.201900102","article-title":"The inner clock\u2014Blue light sets the human rhythm","volume":"12","author":"Wahl","year":"2019","journal-title":"J. Biophotonics"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/0038-092X(77)90083-4","article-title":"Variations in the spectral distribution of daylight at various geographical locations on the earth\u2019s surface","volume":"19","author":"Goldberg","year":"1977","journal-title":"Sol. Energy"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2018\/8620172","article-title":"The Role of Limbal Epithelial Stem Cells in Regulating Corneal (Lymph)angiogenic Privilege and the Micromilieu of the Limbal Niche following UV Exposure","volume":"2018","author":"Notara","year":"2018","journal-title":"Stem Cells Int."},{"key":"ref_44","first-page":"705","article-title":"Peripheral light focusing by the anterior eye and the ophthalmohelioses","volume":"22","author":"Coroneo","year":"1991","journal-title":"Ophthalmic Surg."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.exer.2015.08.003","article-title":"Three-dimensional structure of the mammalian limbal stem cell niche","volume":"140","author":"Grieve","year":"2015","journal-title":"Exp. Eye Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"206","DOI":"10.12816\/0004449","article-title":"Conjunctival Melanosis: Review of the Literature","volume":"35","author":"Alqahtani","year":"2013","journal-title":"Bahrain Med Bull."},{"key":"ref_47","first-page":"61","article-title":"Primary acquired melanosis of the conjunctiva: Experience with 311 eyes","volume":"105","author":"Shields","year":"2007","journal-title":"Trans. Am. Ophthalmol. Soc."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1250","DOI":"10.1364\/BOE.10.001250","article-title":"Jaundice Eye Color Index (JECI): Quantifying the yellowness of the sclera in jaundiced neonates with digital photography","volume":"10","author":"Leung","year":"2019","journal-title":"Biomed. Opt. Express"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1111\/eth.12144","article-title":"The emotional eye: Red sclera as a uniquely human cue of emotion","volume":"119","author":"Provine","year":"2013","journal-title":"Ethology"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1007\/s12110-013-9168-x","article-title":"Red, Yellow, and Super-White Sclera","volume":"24","author":"Provine","year":"2013","journal-title":"Hum. Nat."}],"container-title":["Symmetry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-8994\/13\/7\/1270\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:31:05Z","timestamp":1760164265000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-8994\/13\/7\/1270"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7,15]]},"references-count":50,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2021,7]]}},"alternative-id":["sym13071270"],"URL":"https:\/\/doi.org\/10.3390\/sym13071270","relation":{},"ISSN":["2073-8994"],"issn-type":[{"value":"2073-8994","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,15]]}}}