What is unique about the human eye? Comparative image analysis on the external eye morphology of human and nonhuman great apes

Abstract

The gaze-signaling hypothesis and the related cooperative-eye hypothesis posit that humans have evolved special external eye morphology, including exposed white sclera (the white of the eye), to enhance the visibility of eye-gaze direction and thereby facilitate conspecific communication through joint-attentional interaction and ostensive communication. However, recent quantitative studies questioned these hypotheses based on new findings that humans are not necessarily unique in certain eye features compared to other great ape species. Therefore, there is currently a heated debate on whether external eye features of humans are distinguished from those of other apes and how such distinguished features contribute to the visibility of eye-gaze direction. This study leveraged updated image analysis techniques to test the uniqueness of human eye features in facial images of great apes. Although many eye features were similar between humans and other species, a key difference was that humans have uniformly white sclera which creates clear visibility of both eye outline and iris; the two essential features contributing to the visibility of eye-gaze direction. We then tested the robustness of the visibility of these features against visual noises such as darkening and distancing and found that both eye features remain detectable in the human eye, while eye outline becomes barely detectable in other species under these visually challenging conditions. Overall, we identified that humans have distinguished external eye morphology among other great apes, which ensures robustness of eye-gaze signal against various visual conditions. Our results support and also critically update the central premises of the gaze-signaling hypothesis.

The evolutionary drivers of primate scleral coloration

“…These results are consistent with all three hypotheses of scleral evolution, suggesting that primate scleral morphologies evolve in relation to variation in social environment.The primate order contains a remarkable amount of variation in external ocular morphology (Fig. 1), including differences in scleral volume, width-height ratios and pigment profiles [1][2][3][4][5][6][7][8] . Scleral volumes and width-height ratios have been linked in phylogenetic comparative analyses to social (i.e., group size and neocortex ratio), ecological (i.e., habitat use) and life history (i.e., body mass) drivers 3 .…”

“…Although, for simplicity, we refer to "scleral" pigmentation throughout, the sclera is covered by a thin conjunctival membrane. Whether it is the sclera, the conjunctiva, or both that may be pigmented is not known for each species of nonhuman primate studied 2,3,5,6,8 .Within the primate order, humans are often considered to uniquely possess depigmented sclerae whereas most non-human primate species, including the closely related chimpanzee, instead synthesise dark scleral pigment 1,2,8,9 . Interestingly, the equally closely-related bonobo possesses sclerae of an intermediate average brightness between humans and chimpanzees 5,6,10 .…”

“…Although, for simplicity, we refer to "scleral" pigmentation throughout, the sclera is covered by a thin conjunctival membrane. Whether it is the sclera, the conjunctiva, or both that may be pigmented is not known for each species of nonhuman primate studied 2,3,5,6,8 .…”

“…Within the primate order, humans are often considered to uniquely possess depigmented sclerae whereas most non-human primate species, including the closely related chimpanzee, instead synthesise dark scleral pigment 1,2,8,9 . Interestingly, the equally closely-related bonobo possesses sclerae of an intermediate average brightness between humans and chimpanzees 5,6,10 .…”

“…Recently, a number of studies have examined primate gaze conspicuousness by measuring the brightness contrast between the sclera and iris. Creating a contrast ratio, Perea-Garcia et al 5 found that humans and Pan possessed comparable levels of gaze conspicuousness, though this method was reported as being statistically biased towards comparable results 6,8 . Instead, measuring the iridoscleral brightness range, Caspar et al 6 do not replicate this result, but find conspicuousness overlap between humans, gorillas (Gorilla gorilla) and Sumatran orang-utans (Pongo abelii).…”