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

  1. Fumihiro Kano
  2. Yuri Kawaguchi
  3. Yeow Hanling

  • Curated by eLife

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    Evaluation Summary:

    The study by Kano et al. provides experimental evidence that specific features of the human eye, namely shape and sclera depigmentation, enhance the ability to detect gaze direction of individuals. The study is notable for being the first to adopt a comparative experimental approach, testing both humans and chimpanzees, to demonstrate that white sclera can enhance gaze discrimination in both species, particularly when visibility is poor.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer#2 agreed to share their name with the authors.)

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Abstract

Hallmark social activities of humans, such as cooperation and cultural learning, involve eye-gaze signaling through joint attentional interaction and ostensive communication. The gaze-signaling and related cooperative-eye hypotheses posit that humans evolved unique external eye morphologies, including uniformly white sclera (the whites of the eye), to enhance the visibility of eye-gaze for conspecifics. However, experimental evidence is still lacking. This study tested the ability of human and chimpanzee participants to discriminate the eye-gaze directions of human and chimpanzee images in computerized tasks. We varied the level of brightness and size in the stimulus images to examine the robustness of the eye-gaze directional signal against simulated shading and distancing. We found that both humans and chimpanzees discriminated eye-gaze directions of humans better than those of chimpanzees, particularly in visually challenging conditions. Also, participants of both species discriminated the eye-gaze directions of chimpanzees better when the contrast polarity of the chimpanzee eye was reversed compared to when it was normal; namely, when the chimpanzee eye has human-like white sclera and a darker iris. Uniform whiteness in the sclera thus facilitates the visibility of eye-gaze direction even across species. Our findings thus support but also critically update the central premises of the gaze-signaling hypothesis.

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  1. Version published to 10.7554/elife.74086 on eLife
  2. eLife

    Author Response

    Reviewer #1 (Public Review):

    Kano and authors present a very interesting and unique study investigating whether the white sclera, uniquely characteristic of human eyes, contributes to better gaze detection by individuals, a key prediction of the gaze-signaling and cooperative-eye hypotheses. They test both humans and chimpanzees in a well designed, counter balanced, experiment where they examine both within and cross-species evaluations of gaze from static, controlled images. Overall, they provide compelling evidence that the white sclera not only contribute to better gaze discrimination by both humans and chimpanzees, but that the white sclera also aid gaze discrimination when visibility conditions are poor.

    I found the experiments well designed and carefully thought out. The statistical methods are also appropriately applied in my opinion, although it would be helpful to have the exact R code the authors used as an additional supplement. In general however, the authors should be commended on the transparency with which they describe both the training and testing of individuals for both species.

    One clear weakness of the paper is that the evidence for chimpanzees is limited to only 3 (sometimes 2) individuals, but one can appreciate that this kind of experimental set up and task would have been quite difficult for them. Additionally, although the authors were diligent in selecting a cross-cultural sample of human images, the test subjects were all primarily of one cultural background. Although these weaknesses mean that the generalization of their results need to be taken with caution, I find the methods and results are compelling and provide a significant contribution to the on-going discussion of the importance of external eye morphology in facilitating cooperation and communication.

    Importantly, they show evidence for both white sclera and eye shape/size enhancing gaze discrimination when visibility is compromised, adding empirical evidence for a critical component to the gaze-signaling and cooperative eye hypotheses. I am confident their experimental approach will be useful to other scholars investigating this topic and will provide a comparative framework with which to test other species or test more individuals from different populations of humans and chimpanzees.

    Thank you very much for your positive evaluation. We added our R formula in Table S1. Although the majority of our participants were from similar cultural backgrounds, we believe that the results from the previous two experimental studies on the same topic (Ricciardelli et al. 2000; Yorzinski and Miller, 2020) complement our results because these previous studies tested participants from other cultures. We also added a paragraph explicitly addressing the limitations of our study, including the small number of chimpanzee participants in our test conditions.

    Reviewer #2 (Public Review):

    The proclaimed goal of Kano et al. is to provide "experimental evidence answering the question of whether the human white sclera serves any communicative function for eye-gaze signaling". This is indeed an important gap in the literature, although it has recently been addressed by e.g., Yorzinski & Miller, J (PLoS ONE 15(2), e0228275 (2020)) in a set-up with human subjects. This study, however, includes the first experimental approach to this issue that is built on an interspecific comparison: The authors tested how well humans and chimpanzees can evaluate eye gaze direction in face pictures deriving from both their own and the other species. Additionally, the human and chimpanzee subjects also had to score manipulated photos, in which irido-scleral colors were inverted.

    The experimental protocol is one of the strengths of the study. The experimental stimuli were thoughtfully crafted to avoid unwanted biases and variable shading and size dimensions of stimulus pictures address relevant perceptual challenges of glance identification in the real world. Minor aspects of stimulus design (e.g. inverting pupil colors) are not justified, though. Research hypotheses are clearly stated and are relevant to the current scientific discourse on the topic. The training procedure for the chimpanzees was made fully transparent, impressively demonstrating the efforts involved in preparing them for the study.

    The results are straight-forward and I have no criticism towards analyses and data presentation in the manuscript, which I believe are all well done. Nevertheless, I want to point out that only two chimpanzee subjects participated in all tests, which limits the conclusiveness of the data. This is particularly true, because several chimpanzees that later dropped out of the training performed better when conspecific rather than human stimuli were presented. This issue should receive more attention in the manuscript.

    In general, I believe that many of the interpretations and a priori assumptions of the authors are problematic, constituting the most important weaknesses of the manuscript. Even key claims of the study are only partially supported by the collected data or by results previously reported in the literature:

    From a methodological perspective, this manuscript simply addresses the question: "Is human eye-gaze more conspicuous than that of chimpanzees?" The authors answer this questions positively, which is an expected result and in line with previous research. Nevertheless, the Introduction and Discussion sections of the manuscript prominently discuss the question "Why is the human eye more conspicuous?". For this, an evolutionary perspective needs to be taken into account (see below) and, if an adaptive conjecture is adopted, potential functions need to be proposed.

    The study endorses social drivers behind the depigmentation of the human sclera. However, social functions of eye gaze were not explored in the experiments, as subjects simply needed to extract basic information on glance direction from pictures. It should be expected that increased contrast, as present in the human eye compared to the chimpanzee eye, facilitates the detection of these patterns. I therefore see no new arguments for the idea that scleral color is importantly involved in social cognition and the link between the results and the authors' interpretations remains speculative. It has been demonstrated that reflexive glance following is found in various catarrhine primates, but only humans appear to use glances as referential cues in social situations. The lack of focus on eye orientation in chimpanzee behavior has been strikingly demonstrated by the training results presented herein and strongly supports this dichotomy. At the same time, extensive scleral depigmentation is not rare among monkeys and apes, so that explanations for this phenomenon should be applicable to species other than humans (Caspar et al. Sci Rep 11, 12994 (2021), Perea-García et al. Symmetry, 13(7), 1270 (2021)).

    Thus, it is unfortunate that the very strong conclusive statement "we found that the key function of white sclera is to enhance the eye-gaze signal", is not balanced out by an exploration of alternative hypotheses or caveats to this conclusion. I would argue that such a claim is difficult to defend when a single species pair with very different expressions of eye pigmentation is studied. The authors do not discuss how their interpretations might or might not fit other primates with strongly depigmented sclerae, like Sumatran orangutans. This is an important shortcoming, because such comparisons could potentially back up or damage the hypotheses drawn from the human-chimpanzee pairing.

    Finally, the authors strongly imply that the human condition of scleral pigmentation alone is the derived one and thus requires a peculiar (functional) explanation. On the contrary, the chimpanzee phenotype is discussed as if it would represent an ancestral condition which is deemed representative for nonhuman primates as a whole. However, recent evidence suggests that both humans and chimpanzees show unusual scleral color patterns, with other great apes displaying variable pigmentation with a strong trend towards (at least localized) depigmentation in orangutans, bonobos, and gorillas (Perea García, J. O. J. Lang. Evol. 1 (2), 151-158 (2016), Caspar et al. Sci Rep 11, 12994 (2021)). This is not mentioned in the manuscript and should be added. The uniformly dark chimpanzee sclera is indeed not representative for great apes or most other groups of nonhuman primates.

    All in all, this paper represents a valuable experimental contribution to the debate on the evolution of eye pigmentation in apes. In particular, it demonstrates that eye gaze (and therefore coloration) is negligible for chimpanzee communication. However, a more inclusive and nuanced interpretation of results and a better portrayal of their relevance to hypotheses explored in the literature is required. This includes an improved discussion of the limitations of the study's approach when it comes to deducing evolutionary and socio-cognitive patterns.

    Thank you very much for your helpful comments and expertise in this topic.

    Regarding the previous experimental study on this topic, Yorzinski and Miller (2020) is indeed our predecessor, and we detailed this study in our introduction section. Moreover, we want to point out that Ricciardelli et al. 2000 is our predecessor as well, and in fact, we designed our stimulus manipulation based on this previous study. Ricciardelli et al. 2000 tested human participants in a gaze-discrimination task and found that reversing the contrast polarity of the eye regions in the human faces deteriorates the judgment of the gaze directions in participants (thus we should have said this stimulus manipulation as “the reversal of eye contrast polarity”, rather than “the inversion of eye colors”; we apologize for our error in word choice). One advantage of Ricciardelli’s et al. method is that we could change only the contrast polarity but not any color differences within each eye image, namely the color differences between the iris and sclera and also between the pupil and iris (thus this manipulation does not change the conspicuousness of iris or pupil per se). We added Figure S4 to better explain how we made our stimuli. Please also note that the visibility of eye-gaze directions depends on the visibility of both iris and eye-outline edges, not only that of the iris (or pupil). To clarify this aspect, we added Figure S1.

    Regarding a small number of chimpanzee participants, we addressed this limitation more explicitly in our revision.

    Regarding the individual differences in training performance, although we indeed observed some differences between individuals in their performance for the chimpanzee and human stimuli during the training stage, we did not find any relation between these performances and the participants’ particular backgrounds (Figure S3 and Table S3). Most importantly, please note that the key criterion of passing the training stage was learning to reliably discriminate the eye-gaze directions of both human and chimpanzee stimuli.

    Regarding the interpretations and a priori assumptions, we can clarify them by referring to one most recent morphological study on great ape eye color in this revision (Kano, F., Furuichi, T., Hashimoto, C., Krupenye, C., Leinwand, J. G., Hopper, L. M., . . . Tajima, T. (2021). What is unique about the human eye? Comparative image analysis on the external eye morphology of human and nonhuman great apes. Evolution and Human Behavior, in press, DOI: 10.1016/j.evolhumbehav.2021.12.004). Although the current experimental study was performed independently from this related study, we built our experimental designs partly based on this related study. The results from our experimental study and those from this related study are complementary to one another.

    Regarding the iris-sclera color contrast/difference, Kano et al. (in press) found that the iris-sclera color difference (not the contrast measure of Perea-Garcia et al., 2019 criticized by Caspar et al., 2021) did not differ between the human and chimpanzee eyes. Importantly, we confirmed this same result in our chimpanzee and human stimuli (Figure S2). More importantly, as mentioned above, we did not just swap the iris and sclera colors in our eye images, but reversed the contrast polarity of eye images, without changing any local color difference within the eye images such as the iris-sclera or the iris-pupil color contrast/differences. Thus, please note that we did not ask "Is human eye-gaze more conspicuous than that of chimpanzees?", but asked, “Does the uniformly white sclera (with a darker iris) facilitate the visibility of eye-gaze directions across species?”. We expanded our introduction section to clarify our general aims and rationales/explanations for our experimental manipulations.

    Regarding the social drivers, one sentence in the conclusion paragraph (that you pointed out) was indeed misleading and thus rephrased it as “one function of the uniformly white sclera is to equip eye-gaze signal with robustness against its degradation caused by natural noises (e.g., shading, distancing)”. Indeed, our aim was to test the perceptual advantage of the uniformly white sclera, one key premise of the gaze-signaling hypothesis, but not to test the social drivers of eye-gaze signals.

    Regarding the sclera colors of other great ape species, we also recognized in Kano et al. (in press) that some nonhuman ape individuals have partly unpigmented sclera. However, this related study found that such partly unpigmented sclera is characterized as more graded or patchy color patterns compared to humans’ uniformly unpigmented sclera and that these color patterns more easily blend into adjacent skin/hair colors around the eyes, particularly in visually challenging conditions (e.g., shading, distancing). We thus predict that the same pattern of results would be obtained even when we use partly unpigmented sclera as our stimulus. However, further experimental studies are necessary to confirm this prediction. We clarified these points in both our introduction and discussion sections.

    Thank you once again for your critical but constructive comments.

  3. eLife

    Evaluation Summary:

    The study by Kano et al. provides experimental evidence that specific features of the human eye, namely shape and sclera depigmentation, enhance the ability to detect gaze direction of individuals. The study is notable for being the first to adopt a comparative experimental approach, testing both humans and chimpanzees, to demonstrate that white sclera can enhance gaze discrimination in both species, particularly when visibility is poor.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer#2 agreed to share their name with the authors.)

  4. eLife

    Reviewer #1 (Public Review):

    Kano and authors present a very interesting and unique study investigating whether the white sclera, uniquely characteristic of human eyes, contributes to better gaze detection by individuals, a key prediction of the gaze-signaling and cooperative-eye hypotheses. They test both humans and chimpanzees in a well designed, counter balanced, experiment where they examine both within and cross-species evaluations of gaze from static, controlled images. Overall, they provide compelling evidence that the white sclera not only contribute to better gaze discrimination by both humans and chimpanzees, but that the white sclera also aid gaze discrimination when visibility conditions are poor.

    I found the experiments well designed and carefully thought out. The statistical methods are also appropriately applied in my opinion, although it would be helpful to have the exact R code the authors used as an additional supplement. In general however, the authors should be commended on the transparency with which they describe both the training and testing of individuals for both species.

    One clear weakness of the paper is that the evidence for chimpanzees is limited to only 3 (sometimes 2) individuals, but one can appreciate that this kind of experimental set up and task would have been quite difficult for them. Additionally, although the authors were diligent in selecting a cross-cultural sample of human images, the test subjects were all primarily of one cultural background. Although these weaknesses mean that the generalization of their results need to be taken with caution, I find the methods and results are compelling and provide a significant contribution to the on-going discussion of the importance of external eye morphology in facilitating cooperation and communication.

    Importantly, they show evidence for both white sclera and eye shape/size enhancing gaze discrimination when visibility is compromised, adding empirical evidence for a critical component to the gaze-signaling and cooperative eye hypotheses. I am confident their experimental approach will be useful to other scholars investigating this topic and will provide a comparative framework with which to test other species or test more individuals from different populations of humans and chimpanzees.

  5. eLife

    Reviewer #2 (Public Review):

    The proclaimed goal of Kano et al. is to provide "experimental evidence answering the question of whether the human white sclera serves any communicative function for eye-gaze signaling". This is indeed an important gap in the literature, although it has recently been addressed by e.g., Yorzinski & Miller, J (PLoS ONE 15(2), e0228275 (2020)) in a set-up with human subjects. This study, however, includes the first experimental approach to this issue that is built on an interspecific comparison: The authors tested how well humans and chimpanzees can evaluate eye gaze direction in face pictures deriving from both their own and the other species. Additionally, the human and chimpanzee subjects also had to score manipulated photos, in which irido-scleral colors were inverted.

    The experimental protocol is one of the strengths of the study. The experimental stimuli were thoughtfully crafted to avoid unwanted biases and variable shading and size dimensions of stimulus pictures address relevant perceptual challenges of glance identification in the real world. Minor aspects of stimulus design (e.g. inverting pupil colors) are not justified, though. Research hypotheses are clearly stated and are relevant to the current scientific discourse on the topic. The training procedure for the chimpanzees was made fully transparent, impressively demonstrating the efforts involved in preparing them for the study.

    The results are straight-forward and I have no criticism towards analyses and data presentation in the manuscript, which I believe are all well done. Nevertheless, I want to point out that only two chimpanzee subjects participated in all tests, which limits the conclusiveness of the data. This is particularly true, because several chimpanzees that later dropped out of the training performed better when conspecific rather than human stimuli were presented. This issue should receive more attention in the manuscript.

    In general, I believe that many of the interpretations and a priori assumptions of the authors are problematic, constituting the most important weaknesses of the manuscript. Even key claims of the study are only partially supported by the collected data or by results previously reported in the literature:
    From a methodological perspective, this manuscript simply addresses the question: "Is human eye-gaze more conspicuous than that of chimpanzees?" The authors answer this questions positively, which is an expected result and in line with previous research. Nevertheless, the Introduction and Discussion sections of the manuscript prominently discuss the question "Why is the human eye more conspicuous?". For this, an evolutionary perspective needs to be taken into account (see below) and, if an adaptive conjecture is adopted, potential functions need to be proposed.
    The study endorses social drivers behind the depigmentation of the human sclera. However, social functions of eye gaze were not explored in the experiments, as subjects simply needed to extract basic information on glance direction from pictures. It should be expected that increased contrast, as present in the human eye compared to the chimpanzee eye, facilitates the detection of these patterns. I therefore see no new arguments for the idea that scleral color is importantly involved in social cognition and the link between the results and the authors' interpretations remains speculative. It has been demonstrated that reflexive glance following is found in various catarrhine primates, but only humans appear to use glances as referential cues in social situations. The lack of focus on eye orientation in chimpanzee behavior has been strikingly demonstrated by the training results presented herein and strongly supports this dichotomy. At the same time, extensive scleral depigmentation is not rare among monkeys and apes, so that explanations for this phenomenon should be applicable to species other than humans (Caspar et al. Sci Rep 11, 12994 (2021), Perea-García et al. Symmetry, 13(7), 1270 (2021)).

    Thus, it is unfortunate that the very strong conclusive statement "we found that the key function of white sclera is to enhance the eye-gaze signal", is not balanced out by an exploration of alternative hypotheses or caveats to this conclusion. I would argue that such a claim is difficult to defend when a single species pair with very different expressions of eye pigmentation is studied. The authors do not discuss how their interpretations might or might not fit other primates with strongly depigmented sclerae, like Sumatran orangutans. This is an important shortcoming, because such comparisons could potentially back up or damage the hypotheses drawn from the human-chimpanzee pairing.

    Finally, the authors strongly imply that the human condition of scleral pigmentation alone is the derived one and thus requires a peculiar (functional) explanation. On the contrary, the chimpanzee phenotype is discussed as if it would represent an ancestral condition which is deemed representative for nonhuman primates as a whole. However, recent evidence suggests that both humans and chimpanzees show unusual scleral color patterns, with other great apes displaying variable pigmentation with a strong trend towards (at least localized) depigmentation in orangutans, bonobos, and gorillas (Perea García, J. O. J. Lang. Evol. 1 (2), 151-158 (2016), Caspar et al. Sci Rep 11, 12994 (2021)). This is not mentioned in the manuscript and should be added. The uniformly dark chimpanzee sclera is indeed not representative for great apes or most other groups of nonhuman primates.

    All in all, this paper represents a valuable experimental contribution to the debate on the evolution of eye pigmentation in apes. In particular, it demonstrates that eye gaze (and therefore coloration) is negligible for chimpanzee communication. However, a more inclusive and nuanced interpretation of results and a better portrayal of their relevance to hypotheses explored in the literature is required. This includes an improved discussion of the limitations of the study's approach when it comes to deducing evolutionary and socio-cognitive patterns.

  6. Version published to 10.1101/2021.09.21.461201v1 on bioRxiv