Ocular pigmentation in humans, great apes, and gibbons is not suggestive of communicative functions

Abstract

Pigmentation patterns of the visible part of the eyeball, encompassing the iris and portions of the sclera, have been discussed to be linked to social cognition in primates. The cooperative eye hypothesis suggests the white sclera of humans to be a derived adaptive trait that enhances eye-mediated communication. Here, we provide a comparative analysis of ocular pigmentation patterns in 15 species of hominoids (humans, great apes & gibbons) that show marked differences in social cognition and quantify scleral exposure at the genus level. Our data reveals a continuum of eye pigmentation traits in hominoids which does not align with the complexity of gaze-mediated communication in the studied taxa. Gibbons display darker eyes than great apes and expose less sclera. Iridoscleral contrasts in orangutans and gorillas approach the human condition but differ between congeneric species. Contrary to recent discussions, we found chimpanzee eyes to exhibit a cryptic coloration scheme that resembles gibbons more than other apes. We reevaluate the evidence for links between social cognition and eye pigmentation in primates, concluding that the cooperative eye hypothesis cannot explain the patterns observed. Differences in scleral pigmentation between great apes and humans are gradual and might have arisen via genetic drift and sexual selection.

Experimental evidence that uniformly white sclera enhances the visibility of eye-gaze direction in humans and chimpanzees

“…H2 posits the perceptual advantage of the iris-sclera color difference. As the iris-sclera color difference (note the difference between the contrast and difference measures employed by previous studies; Perea-García et al, 2019 ; Caspar et al, 2021 ; Mearing and Koops, 2021 ; Kano et al, 2021 ) was similar between chimpanzees and humans in general ( Kano et al, 2021 ) and did not differ between our chimpanzee and human stimuli with both positive and negative eyes (see Appendix 3—figure 2 for the quantitative evaluation of our stimuli), we predicted no performance difference between the stimulus types in participants of both species. H3 posits the perceptual advantage of the horizontally elongated shape.…”

“…However, further tests are necessary to confirm this prediction. Finally, it remains unanswered whether our results are generalizable to other stimuli with some variations in sclera color, specifically given that some chimpanzee individuals have partly unpigmented (white) sclera ( Perea-García et al, 2019 ; Caspar et al, 2021 ; Mearing and Koops, 2021 ; Kano et al, 2021 ). However, such sclera is typically characterized as more graded or patchy compared to humans’ uniformly white sclera.…”

“…H3 posits the perceptual advantage of the horizontally elongated shape. As human eyes were horizontally longer than chimpanzee eyes in general ( Mayhew and Gómez, 2015 ; Caspar et al, 2021 ; Kano et al, 2021 ) and also in our stimulus set ( Appendix 3—figure 2 ), we predicted increased performance for the human stimuli (with both positive and negative eyes) in participants of both species. H4 posits the participants’ perceptual expertise in the contrast polarity of own-species eyes ( Ricciardelli et al, 2000 ) and thus predicted increased performance for the positive eyes of both species in human participants and the negative eyes of both species in chimpanzee participants.…”

“…Despite the widespread popularity of the gaze-signaling and related cooperative-eye hypotheses in the literature, these hypotheses have been severely challenged by recent quantitative morphological studies showing that certain eye features of humans are not necessarily unique among great ape species ( Mayhew and Gómez, 2015 ; Perea-García et al, 2019 ; Caspar et al, 2021 ; Mearing and Koops, 2021 ; Kano et al, 2021 ). Accordingly, there is currently a heated debate over whether the external eye morphology of humans has any communicative function.…”

“…Accordingly, there is currently a heated debate over whether the external eye morphology of humans has any communicative function. Specifically, those studies have shown that (1) the sclera of humans is not necessarily more exposed than that of other great ape species ( Mayhew and Gómez, 2015 ; Caspar et al, 2021 ; Kano et al, 2021 ), that (2) the color contrast/difference between the iris and the sclera is similar between humans and other great apes ( Perea-García et al, 2019 ; Caspar et al, 2021 ; Mearing and Koops, 2021 ; Kano et al, 2021 ), and that (3) there is substantial individual variation in the extent to which sclera is unpigmented among some nonhuman ape species ( Mayhew and Gómez, 2015 ; Caspar et al, 2021 ; Mearing and Koops, 2021 ; Kano et al, 2021 ; Perea García, 2016 ). Given these new findings, one recent study suggested that one (and possibly only) eye feature that both distinguishes humans from other great apes and contributes to the visibility of eye-gaze direction is uniform whiteness in humans’ exposed sclera; i.e., depigmentation all the way from the iris edge to the eye corners ( Kano et al, 2021 ).…”