Human eyes have a widely exposed white sclera surrounding the darker coloured iris, making it easy to discern the direction in which they are looking1. We compared the external morphology of primate eyes in nearly half of all primate species, and show that this feature is uniquely human. Humans have the largest ratio of exposed sclera in the eye outline, which itself is elongated horizontally. We suggest that these are adaptations to extend the visual field by allowing greater eye movement, especially in the horizontal direction, and to enhance the ease of detecting the gaze direction of another individual.
We measured three parameters in 88 primate species: an index of exposed sclera size (SSI) in the eye outline, the width-height ratio (WHR) of the eye outline and the sclera coloration. Human eyes have the largest SSI and the outline shows extraordinary horizontal elongation. Humans are also the only species with white sclera. We failed to detect any significant sexual or racial differences in these parameters. Although a small number of primates had pale sclera (Macaca sylvanus, M. nemestrina) or brown sclera with small white regions to the side of the iris ( Saguinus midas, S. labiatus, Callithrix argentata, Callimico goeldii), almost all other primates examined have similar coloration to that of the skin around the eyes (Fig. 1).
SSI correlates with weight and crown-rump length2,3 (r=0.59, P r=0.65, P r=0.71, PFig. 2). Larger SSIs allow the iris a wider range of movement and hence a larger visual field. This may be advantageous to larger species where eye movement becomes increasingly more efficient than head or body movement, especially as comparative eyeball size is smaller in larger animals4. In addition, in small species with comparatively large eyeballs in a small skull, muscle space may be seriously limited.
We video-recorded various primates eating (18 species, 29 individuals), and counted eye and head movements. The amount of scanning by eye movement alone was correlated with SSI (r=0.73, P n=5) compared with other primates (4.3-24.4%; mean, 10.6%). The highest rate in non-human primates was observed in the chimpanzee, Pan troglodytes (20-35%, n=3).
WHR is largest in terrestrial species, smallest in arboreal species, with semi-arboreal species lying in-between (Fig. 1). There is a corresponding high ratio of horizontal to vertical scanning in terrestrial species, as might be expected to suit this lifestyle, and a low ratio in arboreal species. The ratio is correlated with WHR (scanning time ratio: r=0.74, P r=0.88, P
Microscopic analysis of Japanese macaque (Macaca fuscata) eyes showed brown pigmentation of the sclera tissue around the cornea, apparently common in primates and other mammals. This pigmentation was thought to reduce glare as it is absent in many nocturnal and crepuscular species5, but nocturnal primates (Gelago senegalensis, Tarsius syrichta, Perodicticus potto, Nycticebus coucang and Aotus trivirgatus) also had coloured sclera and diurnal humans showed no pigmentation.
In many primates, gaze direction is important in communication, and direct eye contact often elicits attacks. Sclera pigmentation to obscure the gaze direction may thus be adaptive6. It may also serve to deceive natural predators, as if the predator believes that the prey animal is aware of its presence, it may be less likely to attack7. In some non-human primates (9 of 10 species examined), sclera coloration of newborns was paler than adults, indicating that infant gaze signals might have special meanings in these species. In all of 14 species examined, including humans, SSI and WHR of newborns were lower than those of adults.
The human sclera is much paler than the facial skin or iris so it is very easy to discern the gaze direction. Predation risk might have decreased with the evolution of enlarged body size and the use of tools and fire. In addition, gaze-signal enhancement might aid the communication required for increased cooperative and mutualistic behaviours to allow group hunting and scavenging. A small change in sclera coloration may have altered ‘gaze-camouflaged’ to ‘gaze-signalling’ eyes. SSI and WHR of human eyes are even larger than those of gorillas, the largest primate, which suggests adaptation for gaze-signal enhancement. The uniqueness of human eye morphology among primates illustrates the difference between humans and other primates in the ability to communicate using gaze signals.
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We thank our colleagues for discussion and for communicating unpublished results; P. Freemont, N. Jones and A. Parker for their suggestions and for critically reading the manuscript; P. Chambon for pBL1, pASV3 and the anti-ER monoclonal antibody; B. Katzenellenbogen for 2EREppS2-CAT; N. Jones for the yeast strain; K. Hobbs for oligonucleotides; N. O'Reilly for peptides; W. Bessant for photography; and G. Clark for automated sequencing. D.M.H. and E.K. were supported by grants from the European Community TMR program and the Netherlands Organisation of Scientific Research (NWO), respectively.
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