Hiromi Kobayashi & Unique morphology of the human eye and Shiro Kohshima its adaptive meaning: comparative studies Biological Laboratory, Faculty on external morphology of the primate eye of Bioscience and Biotechnology, Tokyo Institute In order to clarify the morphological uniqueness of the human eye of Technology (c/o Faculty of and to obtain cues to understanding its adaptive significance, we Science), 12-1, O-okayama compared the external morphology of the primate eye by measuring 2-chome, Meguro-ku, Tokyo nearly half of all extant primate species. The results clearly showed 152-8551, Japan. E-mail: exceptional features of the human eye: (1) the exposed white sclera is [email protected] void of any pigmentation, (2) humans possess the largest ratio of exposed sclera in the eye outline, and (3) the eye outline is extraor- Received 30 October 1998 dinarily elongated in the horizontal direction. The close correlation of Revision received the parameters reflecting (2) and (3) with habitat type or body size of 29 January 2001 the species examined suggested that these two features are adapta- and accepted 5 February tions for extending the visual field by eyeball movement, especially in 2001 the horizontal direction. Comparison of eye coloration and facial Keywords: primates, eye coloration around the eye suggested that the dark coloration of morphology, sclera colour, exposed sclera of nonhuman primates is an adaptation to camouflage communication, adaptation, the gaze direction against other individuals and/or predators, and that human evolution, theory of the white sclera of the human eye is an adaptation to enhance the gaze mind. signal. The uniqueness of human eye morphology among primates illustrates the remarkable difference between human and other primates in the ability to communicate using gaze signals. 2001 Academic Press Journal of Human Evolution (2001) 40, 419–435 doi:10.1006/jhev.2001.0468 Available online at http://www.idealibrary.com on Introduction the human eye. For example, in humans, the widely exposed white sclera (the white of the Recognizing others’ gaze direction is one of eye) surrounding the darker coloured iris the important cognitive bases for communi- makes it easy for others to discern the gaze cation in humans (Gibson & Pick, 1963; direction and has been said to be a charac- Kendon, 1967). To clarify the biological teristic of humans not found in other pri- basis of this ability, especially in relation to mate species (Morris, 1985). However, this the evolution of social intelligence, has not been examined in detail, partly researchers have experimentally examined because of the difficulty in measuring the the cognitive ability to detect gaze direction soft parts of living animals. of others in nonhuman primates (Gomez, In this study, we measured the external 1991; Itakura & Anderson, 1996; Tomasello eye morphologies of nearly half of all extant et al., 1998). However, little attention has primate species with video camera and been given to external morphology of the computer-aided image analysing techniques eye, although this ability of humans might to clarify the morphological uniqueness of be supported by a unique morphology of the human eye and to understand adaptive Address correspondence to: Hiromi Kobayashi, meanings of external eye morphology in Ph.D., 6–8, Nakanoshima-cho, Fukakusa, Fushimi-ku, Kyoto-city, Kyoto, 612-0049, Japan. Tel.: +81 75 644 primates. The results clearly showed excep- 1402; Fax: +81 75 644 1402. tional features of the human eye in both 0047–2484/01/050419+17$35.00/0 2001 Academic Press 420 . . shape and coloration. In our preceding coidea; 43, Hominoidea; 9) were studied paper (Kobayashi & Kohshima, 1997), we (Table 1). Facial images of 80 species were briefly reported the morphological unique- recorded by video camera at the Japan ness of the human eye and discussed its Monkey Centre. Facial images of eight adaptive meanings. In the present paper we species (Microcebus (1), Loris tardigradus (2), fully analysed the results and examined the Perodicticus potto (1), Tarsius (1), Saguinus following hypotheses on adaptive meanings imperator (1), Pithecia monachus (1), Cacajao of primate eye morphology. rubicundus (1), Cercopithecus hamlyni (1)) We measured width/height ratio of the eye were collected from books (Itani & Uehara, outline (WHR) and an index of exposed 1986; Yoshino, 1994). For humans, facial sclera size in the eye outline (SSI) to analyse images of 244 Japanese, 347 Caucasian and eye shape. These eye-shape parameters 68 Afro-Caribbean adults were studied. 244 closely correlated with habitat type or body Japanese, 280 Caucasian and 2 Afro- size of the species examined. To explain the Caribbean images were recorded by video correlation, we postulated a hypothesis that camera, and 67 Caucasian and 66 Afro- these two features are adaptations for Caribbean images were collected from extending the visual field by eyeball move- books (Ohara, 1970; Gomi, 1994). ment, especially in the horizontal direction. Two parameters were measured for each This hypothesis was examined and sup- species: the width/height ratio of the eye ported by analysing the eye movement of outline (WHR) and an index of exposed video-recorded primates and comparing the sclera size in the eye outline (SSI). Frontal way that gaze direction changes among full-face images without obvious facial species with various body sizes and habitat expression of subjects were recorded by types. video camera. These images were processed To explain the unique coloration of the and analysed on a Macintosh Quadra human eye with its exposed white sclera void 840AV computer using the public domain of any pigmentation, we postulated a NIH Image program. For each image, (A) hypothesis that only coloration of the human the distance between the corners of the eye, eye is adapted to enhance the gaze signal (B) the longest perpendicular line between while eye coloration of other primates is the upper and lower eyelid, (C) width of the adapted to camouflage the gaze direction exposed eyeball, and (D) diameter of the iris against other individuals and/or predators. were measured (Figure 1). WHR means This hypothesis was examined and sup- (A)/(B) and SSI means (C)/(D). Data of ported by analysing relationships among iris weight, crown–rump length and habitat type coloration, sclera coloration and facial col- of primates were collected from books (Itani oration around the eye. Our results sug- & Uehara, 1986; Napier & Napier, 1985) gested that unique features of the human eye since we could not get permission for started to evolve as adaptations to large body physical contact with primates. Walking- size and terrestrial life and were completed height and sitting-height of primates were as a device for communication using gaze measured in the Japan Monkey Centre using signal. marks on the wall of the cages. Eye-coloration measurements Method Coloration of the exposed sclera (including Eye shape measurements the conjunctiva to be precise), iris and face A total of 874 adult animals (88 species: around the eye was recorded for each of 91 Prosimii; 10, Ceboidea; 26, Cercopithe- species by direct observation of living 421 animals (82 species) and of eyeball speci- To calculate the ratio of scanning per- mens (55 species, 124 animals) kept in the formed only by eyeball movement, move- Japan Monkey Centre (Table 1). The sclera ments of the eyeball and the head scanning colour included in the term ‘‘Pale brown’’ were counted (total observation time: was a paler one than yellow ochre: 10YR 10,037 sec) for 29 individuals of 18 species 6/7·5 of Munsell Colour System (see (Table 1). Figure 9). To calculate the ratio of horizontal scan- Eye coloration of 82 primate species were ning to vertical scanning frequency and classified into 4 types (see Type 1–4, Figure time duration of horizontal and vertical 11) by the differences of colour or contrast scanning were measured (total observation between sclera and iris/face. This classifica- time=12,579 sec) for 40 individuals of 26 tion was carried out by one person observing species (Table 1): arboreal species: Lemur living animals. To check reliability of this catta, Cebus apella, C. albifrons*, Pithecia classification, another person independently pithecia*, Ateles belzebuth*, A. geoffroyi, A. classified the face pictures of 76 primate paniscus, Cercocebus galeritus, Cercopithecus species (see Figure 11). The results agreed cephus*, Colobus angolensis, Presbytis cristata, in 70 species (92%). Disagreement was only P. vetulus, P. francoisi*, Nasalis larvatus, observed between Type 1 and Type 2 in 6 Hylobates lar and H. pileatus; semi-arboreal species (8%). species: Macaca fuscata*, Cercocebus torqua- Eyeball specimens of the Japanese tus, Mandrillus sphinx*, M. leucophaeus*, macaque (1 subject) and crab-eating Cercopithecus ascanius, Presbytis entellus and macaque (2 subjects) were supplied from a Pan troglodytes; terrestrial species: Papio co-operative program of the Primate hamadryas, Erythrocebus patas and Homo Research Institute, Kyoto University, sapiens (*: duration time only) (Table 1). Inuyama, Aichi, Japan. Eyeballs were fixed All these videotape analyses were carried with 4% paraformaldehyde in 0·1 M phos- out by one person. To check reliability of the phate buffer (pH 7·2) at 4"C overnight. The analyses, a second person scored every tissue including the conjunctiva and cornea 0·5 sec randomly sampled 20% of the video- separated from eyeballs was washed several tapes independently. Agreement between times in cold phosphate-buffered saline the persons was 82% on average. The (PBS), dehydrated in an ethanolic series Cohen’s kappa (Bakeman & Gobbman, finishing xylene and embedded in paraffin. 1997) was 0·63 on average. Serial sections with a 4 !m thickness were cut with disposable blades, floated on water Results and discussion and placed on slides. These sections were deparaffinized in xylene, washed in ethanol Unique shape of the human eye and PBS and studied by light microscopy Figure 2(a) shows that human eyes have the (see Figure 10).