From an early age, we are able to detect the direction others are looking in (known as eye-gaze) and make eye contact with each other to communicate. The front of the human eye has a large white area known as the sclera that surrounds the darker colored iris and pupil in the center.

Compared to us, chimpanzees and other nonhuman great apes have sclerae that are much darker in color or at least not as uniformly white as human eyes. Some researchers believe that the white sclera of the human eye may have evolved to make it easier for other individuals to detect the direction of our gaze. However, there is a lack of experimental evidence as to whether white sclerae actually helps humans to distinguish the direction of eye-gaze.

Here, Kano, Kawaguchi and Yeow presented human and chimpanzee participants with images of other humans and chimpanzees on a computer screen and asked them to indicate the direction of eye-gaze in each image. The experiments found that both humans and chimpanzees were better able to discriminate the directions of eye-gaze from the images of humans than those of chimpanzees, particularly when the images were smaller or more shaded. Moreover, artificially altering the eyes in the chimpanzee images so that they were more human-like – that is, had a light-colored sclera and a darker iris – enabled both humans and chimpanzees to better discriminate the eye-gaze directions of the chimpanzees.

Kano, Kawaguchi and Yeow’s findings indicate that white sclerae do indeed help both humans and chimpanzees to discriminate the direction of eye-gaze, even though only humans have white sclerae. This is likely because humans use eye-gaze in key social activities (including learning languages, coordinating to complete complex tasks and transmitting cultural information), indicating that white sclerae may have evolved to enhance human-specific communication. To learn more about this type of communication, future research could focus on finding out when white sclerae first evolved.

In humans, eye-gaze is employed in critical ways for conspecific communication during social activities such as cooperation, teaching, and language learning (Csibra and Gergely, 2009; Tomasello et al., 2005). Humans excel at detecting another’s direct gaze and following another’s gaze directions from early infancy (Farroni et al., 2002; Farroni et al., 2004). Moreover, during social interactions, humans exchange communicative intentions with one another via eye contact (Senju and Johnson, 2009; Kleinke, 1986), and an experience of being watched by another affects one’s reputational concerns (Bateson et al., 2006; Engelmann et al., 2012). Comparative studies have found that closely related species such as nonhuman great apes also excel at detecting another’s direct gaze (Myowa-Yamakoshi et al., 2003) and following another’s gaze directions (Bräuer et al., 2005; Okamoto et al., 2002), and adjust their gaze-following behaviors flexibly and cognitively (Kano and Call, 2014; Okamoto-Barth et al., 2007; Povinelli and Eddy, 1996; Tomasello et al., 1999). Moreover, they make eye contact with other individuals at critical moments of social interactions, such as when requesting food from an experimenter (Gomez, 1996) and initiating affiliative social interactions with conspecifics (Heesen et al., 2021; Yamagiwa, 1992). However, several potential differences might exist between humans and nonhuman apes in their use and interpretation of gaze behaviors. For example, in the gaze-following/cueing experiments, while humans primarily relied on another’s eye-directional cues, nonhuman apes relied on head-directional rather than eye-directional cues (Tomasello et al., 2007; Tomonaga, 2007, but see Povinelli and Eddy, 1996; Deaner and Platt, 2003). In general, reliance on eye-directional rather than head-directional cues indicates one’s inclination/ability to identify a specific spot that another’s foveae are directing at, rather than a large area that another’s field of view covers. Thus, the former strategy leads to efficient identification of the interaction partners’ focused objects during joint attentional interaction and ostensive communication. Relatedly, a previous study observed that, while both human infants and nonhuman apes alternately looked at both the interaction partner’s face and the focused object during joint-attentional interactions, nonhuman apes made only brief looks to the interaction partner’s face while human infants made more long-lasting looks (Carpenter and Tomasello, 1995). Furthermore, in a communicative gaze-following task, while human infants responded to an agent’s eye contact as if they interpreted it as an ostensive signal preceding referential information (Senju and Csibra, 2008; Okumura et al., 2020; but see Gredebäck et al., 2018), great apes did not show any evidence supporting this understanding (Kano et al., 2018). These potential differences between human and nonhuman apes might be partly related to differences in their sociocognitive skills but also humans’ specialization to eye-gaze signals in conspecific communication.

Relatedly, one influential hypothesis, the gaze-signaling hypothesis (Kobayashi and Kohshima, 2001; Kobayashi and Kohshima, 1997), proposes that humans have evolved special morphological features in the eye, including uniform whiteness in the exposed sclera, to enhance the visibility of eye-gaze directions and thereby help conspecifics communicate via eye-gaze without much attentional effort. This hypothesis is based on comparative analyses showing that (1) uniformly white sclera is a unique feature of the human eye among primates and that (2) the human eye is horizontally more elongated, and the human sclera is horizontally more exposed compared to other primates’ eyes (Kobayashi and Kohshima, 2001; Kobayashi and Kohshima, 1997). The cooperative-eye hypothesis (Tomasello et al., 2007) extended this gaze-signaling hypothesis based on the results from their gaze-following study, proposing that humans evolved these morphological features as well as a special sensitivity to these features to facilitate joint-attentional and communicative interactions in a cooperative context. Others discussed that humans’ white sclera not only signals gaze direction but also emotional cues in combination with fine musculatures around the eyes (Whalen et al., 2004; Baron-Cohen et al., 2001; Jessen and Grossmann, 2014), and also emotional and health-status cues by its color variations (Provine et al., 2013a; Provine et al., 2013b). Moreover, typically developing human adults and children show basic preferences for an animal agent having white sclera (Segal et al., 2016).

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. 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). This previous study used image analysis and computer vision techniques and identified that uniformly white sclera characterizes clear visibilities of both iris and eye-outline edges – the two essential features that contribute to the visibility of eye-gaze directions (see Appendix 3—figure 1 for the illustration of this aspect). More specifically, while the iris is highly visible in all great ape species, the visibility of eye-outline edges is limited in nonhuman apes because most nonhuman ape individuals have darker or more graded/patchy sclera colors compared to humans’ sclera colors, which more easily blend into the adjacent skin/hair colors. On the other hand, nearly all human individuals have uniformly white sclera, which is clearly distinguished from the adjacent skin/hair colors around the eyes (irrespective of the skin color variations) even when the eyes are viewed in visually challenging conditions (e.g., shading, distancing). However, experimental evidence is lacking to support these findings.

Previously, several experimental studies demonstrated that humans’ white sclera facilitates gaze perception at least in human participants. Ricciardelli et al., 2000 tested human participants in a gaze-discrimination task and found that reversing the contrast polarity of human eye images makes the judgment of gaze direction less accurate. Specifically, the gaze directions were more accurately judged in eyes having a positive (normal) contrast polarity (white sclera with a darker iris) than those having a negative (reversed) contrast polarity (black sclera with a bright iris), even though these two eye images were composed of the same colors. Ricciardelli et al. thus suggested that humans have perceptual expertise in positive contrast polarity of eyes (see Itier et al., 2006; Yoshizaki and Kato, 2011 for related results). Also, Yorzinski and Miller, 2020 tested human participants in a gaze-discrimination task in which the sclera colors of human faces were manipulated to be either conspicuous (white or lighter than the iris color) or inconspicuous (similar or darker than the iris color); human participants detected the faces with conspicuous sclera colors faster and more accurately. Yorzinski and Miller thus suggested that humans’ white sclera facilitates their gaze perception. Importantly, although these two studies found similar results, it remains unclear whether humans’ white sclera facilitates their gaze perception by its perceptual properties per se or by human participants’ perceptual expertise in the positive contrast polarity of human eyes. To answer this question, a comparative approach is helpful.

Tomonaga and Imura, 2010 tested whether a chimpanzee could be trained to discriminate eye-gaze directions of human facial images, and in one of their experimental conditions, they replicated the results from Ricciardelli et al., 2000. Specifically, they showed that the chimpanzee’s task performance dropped when the contrast polarity of the eyes was reversed in the stimulus human faces. Unfortunately, however, the conclusion from this result is severely limited because the chimpanzee was trained to discriminate the gaze directions of the human positive eyes (positive contrast polarity) before being tested in the trials presenting the human negative eyes (reversed contrast polarity). Therefore, it remains unclear whether the chimpanzee’s performance was affected by the change in the eye contrast polarity or merely the change in the trained color pattern. Critically, no previous study adopted a fully crossed design for species comparison to examine the effect of sclera colors on primate gaze perception; namely, a study design that presents the stimuli of both species to the participants of both species. Chimpanzees are a suitable species for this design because their eyes have relatively uniformly dark sclera and a bright iris, namely, having a negative contrast polarity opposite to the positive contrast polarity that human eyes have. Therefore, in a fully crossed design with chimpanzees and humans, one can test whether the uniformly white sclera of human positive (normal) eyes and chimpanzee positive (reversed) eyes facilitates the gaze-discrimination performances of both chimpanzee and human participants. Such a question would clarify whether the uniformly white sclera has a perceptual advantage independently from perceptual advantages of other eye features or the participants’ perceptual expertise in a certain eye contrast polarity (as we will detail below).

Consequently, this study tested both humans and chimpanzees on their ability to discriminate the gaze direction of both chimpanzee and human faces with the eyes manipulated to have both normal and reversed contrast polarities. The contrast polarity of both species’ eyes (only the eyeball regions) was reversed by inverting the lightness (or grayscale) values of the eyeball images in the faces (Figure 1A and Appendix 3—figure 3). This manipulation created artificial white sclera in chimpanzee eyes and artificial dark sclera in human eyes, while not affecting the iris-sclera (or pupil-iris) color differences in each species’ eyes. The task for human and chimpanzee participants was to discriminate the gaze direction of human and chimpanzee eye images on a computer monitor (either in a keypress or visual search task; Figure 1B). Our experimental procedures followed a previous study adopting training procedures (Tomonaga and Imura, 2010) instead of spontaneous gaze-following/cueing procedures for chimpanzees (Tomasello et al., 2007; Tomonaga, 2007) because, while the former study successfully trained a chimpanzee to discriminate eye-gaze directions of a stimulus (human) face, the latter studies reported that chimpanzees predominantly rely on head-directional cues but not eye-gaze directional cues in the spontaneous tasks. Also, as the strength of the visual signal generally depends on its degradation caused by natural noises (Endler, 1990), we tested the robustness of eye-gaze signals against shading and distancing (Figure 1A), namely the simulated visual conditions where stimulus eyes were presented darker (in shadows) and smaller (in the distance), following a previous study on great ape eye color (Kano et al., 2021).

Figure 1

Download asset Open asset

We developed five sets of hypotheses and predictions (Table 1). H1 is our key hypothesis, which posits the perceptual advantage of uniformly white sclera (Kobayashi and Kohshima, 2001; Kobayashi and Kohshima, 1997; Kano et al., 2021) and thus predicted increased performance for both human and chimpanzee positive eyes in participants of both species. 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. 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. H5 addressed a general possibility arising from our manipulation of both species’ eye colors, namely, that participants of both species perform more poorly in such artificial conditions, and thus predicted increased performance for the human positive eyes and the chimpanzee negative eyes in participants of both species. Related to this last hypothesis, our chimpanzee participants had extensive experiences in interacting with both conspecifics and humans from youth and thus were familiar with both species’ eyes. We also ensured that our human participants had a minimum of a few months (to decades) of experiences in interacting with chimpanzees and thus were familiar with both species’ eyes.

In Study 1, we tested 25 adult human participants (14 females, 11 males) in two experiments. Experiment 1 presented participants with the stimuli of both humans and chimpanzees with normal contrast polarity at four stimulus levels (L1–4) varying in size and brightness. We tested the effect of stimulus level and species on participants’ correct responses (correct, incorrect) in a binomial generalized linear mixed model (GLMM; see Appendix 1—table 1 for the formulas) and found that human participants performed better in trials presenting the human stimuli than those presenting the chimpanzee stimuli (χ² = 37.08, df = 1, p<10^–8). We also found that their performance was worse in trials presenting smaller and more shaded stimuli (χ² = 45.85, df = 3, p<10^–9; see Appendix 1—table 2 for the full GLMM results; Figure 2A). Experiment 2 presented the same participants with the stimuli of both species with both normal and reversed contrast polarities at stimulus levels L3 and L4. We tested the effect of stimulus level, species, and contrast polarity on participants’ correct responses in GLMM and found a significant three-way interaction effect between these factors (Figure 2B; χ² = 17.57, df = 1, p<10^–4; also see Appendix 1—table 2). We then performed simple effects tests to examine the observed interaction effect further (Figure 2B and Appendix 1—table 2). Critically, we found that human participants performed better in trials presenting the positive (reversed) eyes of chimpanzees (i.e., the white sclera and a darker iris) than those presenting the negative (normal) eyes of chimpanzees (i.e., the dark sclera and a bright iris), while they performed worse in trials presenting the negative (reversed) eyes of humans than those presenting the positive (normal) eyes of humans.

Figure 2

Download asset Open asset

In Study 2, we began with training 10 chimpanzees. Only three (Natsuki, Hatsuka, Pendesa) passed all the required training and subsequently participated in test phases (see Appendix 2—table 1 for details about participants; also see Appendix 4—table 1 and Figure 1 for the number and performance of training sessions for each chimpanzee). Study 2 involved two experiments. Experiment 1 tested those three chimpanzees and presented them with the human and chimpanzee eye images with normal contrast polarity. To test chimpanzees at stimulus levels higher than L1 (i.e., smaller and more shaded), we gradually incremented the stimulus level (by 0.5) across sessions when individuals showed high performance in target trials presenting a given stimulus level (above 85% in two successive sessions). The test phase was defined as the sessions presenting stimulus level higher than (or equal to) L2.5, given that we observed clear performance differences between stimulus species at stimulus levels higher than L2 in Study 1 (see Appendix 4—table 3 for the number of sessions in the pre-test and test phases). We tested chimpanzees’ correct responses during the test phase across repeated sessions at the individual level (with the α level corrected for the number of individuals in the Bonferroni correction, α = 0.05/3). Each chimpanzee completed a minimum of 20 test sessions. To avoid the ceiling effect, we incremented the stimulus level also during the test phase when chimpanzees showed high performance in target trials based on the same criteria. We tested the effect of stimulus species in binomial GLMM on each chimpanzee’s correct responses (correct, incorrect) during the test phase and found that all three chimpanzees performed significantly better for the human stimuli than the chimpanzee stimuli (Natsuki: χ² = 8.28, df = 1, p=0.004; Hatsuka: χ² = 9.50, df = 1, p=0.002; Pendesa: χ² = 21.94, df = 1, p<10^–5; also see Appendix 1—table 2).

Experiment 2 tested two (Natsuki and Hatsuka) out of the three chimpanzees. Pendesa was dropped from this experiment because she took about twice as many training sessions as the other two chimpanzees (Appendix 4—table 2 and Figure 1). Experiment 2 presented them with eye stimuli having reversed contrast polarity in the first test phase (Test B) and then eye stimuli having normal contrast polarity in the next test phase (Test A2); thus, together with the results from Experiment 1 (also called Test A1 phase), we tested chimpanzees in the ABA design. The Test A2 phase started from stimulus level L3, which these two chimpanzees reached during the Test A1 phase. The other procedures were identical with Experiment 1 (with α = 0.05/2). We compared each chimpanzee’s correct responses in target trials across Test A1 and Test B in GLMM and found a significant interaction effect between stimulus species and phase in both chimpanzees (Natsuki: χ² = 34.61, df = 1, p<10^–8; Hatsuka; χ² = 8.39, df = 1, p=0.004; also see Appendix 1—table 2). We then compared each chimpanzee’s performance across Test B and Test A2 and found a significant interaction effect between the two factors in both chimpanzees (Natsuki: χ² = 37.04, df = 1, p<10^–8; Hatsuka; χ² = 33.75, df = 1, p<10^–8). To examine these observed interaction effects further, we performed simple effects tests (Figure 3 and Appendix 1—table 2). Critically, we found that both chimpanzees’ performance significantly increased from Test A1 (normal contrast polarity) to Test B (reversed contrast polarity) and then their performance decreased from Test B to Test A2 (normal contrast polarity) in trials presenting the chimpanzee stimuli. Natsuki’s performance significantly decreased from Test A1 to Test B and then increased from Test B to Test A2 in trials presenting the human stimuli. Hatsuka’s performance did not significantly decrease from Test A1 to Test B but significantly increased from Test B to Test A2 in those trials.

Figure 3

Download asset Open asset

Overall, these results revealed a striking advantage of eyes having positive contrast polarity, namely, the eyes of both species with the uniformly white sclera and a darker iris, in the gaze-discrimination performance of both human and chimpanzee participants. Our results thus supported H1 (perceptual advantage of uniformly white sclera). We also found that, although both human and chimpanzee eye-gaze directions are reliably discernible when those eyes were presented sufficiently large and bright (i.e., L1–2 stimuli), the human eye-gaze directions were more discernible than the chimpanzee eye-gaze particularly when those eyes were presented smaller and more shaded (i.e., L3–4 stimuli).

Our alternative hypotheses (H2–5) cannot explain the overall patterns of our results. H2 (perceptual advantage of the iris-sclera color difference) cannot explain our results likely because it supposes clear visibility of only iris but not that of eye-outline edges, another critical feature that contributes to the visibility of eye-gaze (Kobayashi and Kohshima, 2001; Kano et al., 2021) (also see Appendix 3—figure 1). H3 (perceptual advantage of the horizontally elongated eye shape) also cannot explain our results likely because small variations in the horizontal eye length do not critically affect the visibility of eye-gaze. However, it should be noted that humans can take more extreme sideway eye positions than chimpanzees due to their horizontally elongated eye shape (Kobayashi and Kohshima, 2001), and such mechanistic difference may be one advantage of the human eye in eye-gaze signaling. Yet, this fact might be of limited relevance to real-life social interaction because previous eye-tracking studies measuring eye movements of chimpanzees and humans in naturalistic conditions indicated that the majority of eye positions fall within 20°, the eye position adopted in our stimuli, in both species (Kano and Tomonaga, 2013; Kothari et al., 2020). H4 and H5 (perceptual expertise in own-species and normal eye contrast polarity) also cannot largely explain our results. Finally, one pattern of our results could not be explained by H1 alone, specifically that the negative human eyes and positive chimpanzee eyes affected participants’ task performance similarly in some conditions. More specifically, human participants (collectively) performed similarly in trials presenting the human and chimpanzee stimuli in the L4-reversed condition (i.e., the negative human eye and positive chimpanzee eye in the darkest and smallest images). Also, chimpanzee Hatsuka performed similarly in trials presenting the human and chimpanzee stimuli during the Test B (reversed contrast polarity) phase (unlike Natsuki). These partial results are explained by either H2 or the combination of H1 and H3. Overall, however, our results indicate that the presence of the uniformly white sclera (and a darker iris) in our stimuli is the primary factor affecting the similarity of our results between the participants of both species in our study design.

Our results thus suggest that the visibility of human eye-gaze is primarily supported by basic color properties of the eyes, and thus by a basic perceptual mechanism shared among human and chimpanzee participants. Relatedly, there are a number of previous studies documenting the similarities in visual perception, including spectrum sensitivity, visual acuity, and contrast sensitivity, between humans and nonhuman apes (Deeb et al., 1994; Dulai et al., 1994; Jacobs et al., 1996; Matsuno et al., 2004; Matsuno and Tomonaga, 2006; Matsuzawa, 1990; Bard et al., 1995; Adams et al., 2017) though small differences might exist (Jacobs et al., 1996; Adams et al., 2017). One notable aspect of our results is that chimpanzees required extensive training to distinguish between different gaze directions of human and chimpanzee eyes, and many of our chimpanzees were unable to pass all the required training phases. Given that many of our chimpanzees were already trained for simple color and form perception tasks (e.g., Matsuno et al., 2004; Matsuzawa, 1990), this difficulty might suggest that chimpanzees may generally find it more difficult attending to detailed perceptual features of the eyes compared to humans, consistent with the previous training (Tomonaga and Imura, 2010) and gaze-following/cueing studies (Tomasello et al., 2007; Tomonaga, 2007; but see Povinelli and Eddy, 1996). In this sense, consistent with the previous experimental studies in humans (Tomasello et al., 2007; Whalen et al., 2004; Provine et al., 2013b; Ricciardelli et al., 2000), our results also suggest that gaze perception in humans is supported by both the uniformly white sclera of eyes and their perceptual expertise in such detailed eye features.

One clear limitation of this study is that only a small number of chimpanzees could participate in our test conditions, which hampers the generalization of our results. Nonetheless, if the performance of the current task is supported by simple color properties of eyes and basic visual perception of great apes as argued above, our results should be replicated in other (trained) individuals and likely also in other great ape species. 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. Moreover, as noted earlier, the previous simulation study demonstrated that the visibility of eye-gaze (especially that of eye-outline edges) is limited with the eyes of all nonhuman ape species without the human-like uniformly white sclera, particularly in visually challenging conditions (Kano et al., 2021). We thus expect a similar pattern of results even when using eyes with partly unpigmented sclera in our experiments. Again, however, further experimental studies are necessary to confirm this prediction.

In conclusion, we demonstrated that uniform whiteness in the exposed sclera enhances eye-gaze signaling. We thus provided experimental support for the gaze-signaling hypothesis despite recent criticisms on this hypothesis (Perea-García et al., 2019; Caspar et al., 2021; Mearing and Koops, 2021). However, we also propose several significant updates on this hypothesis. Specifically, we found that it is the uniformly white sclera but not necessarily other distinguishing features, such as iris-sclera color difference and some variation in horizontal eye elongation, that critically distinguishes the human eye from the chimpanzee eye in terms of the visibility of eye-gaze direction. Moreover, we found that one function of the uniformly white sclera is to equip the eye-gaze signal with robustness against degradation caused by natural noises (e.g., shading, distancing). These new findings, when combined with the original and related hypotheses, suggest that humans have evolved special external eye morphology for conspecific communication and that it is a vital part of communication for humans to read conspecific eye-gaze cues during their everyday cooperative and cultural activities.

All data are available in our online repository (https://osf.io/2xny3/).

1. 1. Kano F

   (2021) Open Science Framework

   ID 2xny3. Experimental evidence for the gaze signaling hypothesis.

   https://osf.io/2xny3/

1. 1. Adams L
   2. Wilkinson F
   3. MacDonald S

   (2017) Limits of Spatial Vision in Sumatran Orangutans (Pongo abelii)

   Animal Behavior and Cognition 4:204–222.

   https://doi.org/10.26451/abc.04.03.02.2017

   • Google Scholar
2. 1. Bard KA
   2. Street EA
   3. McCrary C
   4. Boothe RG

   (1995) Development of visual acuity in infant chimpanzees

   Infant Behavior and Development 18:225–232.

   https://doi.org/10.1016/0163-6383(95)90051-9

   • Google Scholar
3. 1. Baron-Cohen S
   2. Wheelwright S
   3. Hill J
   4. Raste Y
   5. Plumb I

   (2001)

   The “Reading the Mind in the Eyes” Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism

   Journal of Child Psychology and Psychiatry, and Allied Disciplines 42:241–251.

   • PubMed
   • Google Scholar
4. 1. Barr DJ
   2. Levy R
   3. Scheepers C
   4. Tily HJ

   (2013) Random effects structure for confirmatory hypothesis testing: Keep it maximal

   Journal of Memory and Language 68:255–278.

   https://doi.org/10.1016/j.jml.2012.11.001

   • Google Scholar
5. 1. Bateson M
   2. Nettle D
   3. Roberts G

   (2006) Cues of being watched enhance cooperation in a real-world setting

   Biology Letters 2:412–414.

   https://doi.org/10.1098/rsbl.2006.0509

   • PubMed
   • Google Scholar
6. 1. Bekerman I
   2. Gottlieb P
   3. Vaiman M

   (2014) Variations in eyeball diameters of the healthy adults

   Journal of Ophthalmology 2014:503645.

   https://doi.org/10.1155/2014/503645

   • PubMed
   • Google Scholar
7. 1. Bräuer J
   2. Call J
   3. Tomasello M

   (2005) All great ape species follow gaze to distant locations and around barriers

   Journal of Comparative Psychology 119:145–154.

   https://doi.org/10.1037/0735-7036.119.2.145

   • PubMed
   • Google Scholar
8. 1. Carpenter M
   2. Tomasello M

   (1995) Joint Attention and Imitative Learning in Children, Chimpanzees, and Enculturated Chimpanzees*

   Social Development 4:217–237.

   https://doi.org/10.1111/j.1467-9507.1995.tb00063.x

   • Google Scholar
9. 1. Caspar KR
   2. Biggemann M
   3. Geissmann T
   4. Begall S

   (2021) Ocular pigmentation in humans, great apes, and gibbons is not suggestive of communicative functions

   Scientific Reports 11:12994.

   https://doi.org/10.1038/s41598-021-92348-z

   • PubMed
   • Google Scholar
10. 1. Csibra G
    2. Gergely G

    (2009) Natural pedagogy

    Trends in Cognitive Sciences 13:148–153.

    https://doi.org/10.1016/j.tics.2009.01.005

    • PubMed
    • Google Scholar
11. 1. Deaner RO
    2. Platt ML

    (2003) Reflexive social attention in monkeys and humans

    Current Biology 13:1609–1613.

    https://doi.org/10.1016/j.cub.2003.08.025

    • PubMed
    • Google Scholar
12. 1. Deeb SS
    2. Jorgensen AL
    3. Battisti L
    4. Iwasaki L
    5. Motulsky AG

    (1994) Sequence divergence of the red and green visual pigments in great apes and humans

    PNAS 91:7262–7266.

    https://doi.org/10.1073/pnas.91.15.7262

    • PubMed
    • Google Scholar
13. 1. Dulai KS
    2. Bowmaker JK
    3. Mollon JD
    4. Hunt DM

    (1994) Sequence divergence, polymorphism and evolution of the middle-wave and long-wave visual pigment genes of great apes and Old World monkeys

    Vision Research 34:2483–2491.

    https://doi.org/10.1016/0042-6989(94)90233-x

    • PubMed
    • Google Scholar
14. 1. Egger HL
    2. Pine DS
    3. Nelson E
    4. Leibenluft E
    5. Ernst M
    6. Towbin KE
    7. Angold A

    (2011) The NIMH Child Emotional Faces Picture Set (NIMH-ChEFS): a new set of children’s facial emotion stimuli

    International Journal of Methods in Psychiatric Research 20:145–156.

    https://doi.org/10.1002/mpr.343

    • PubMed
    • Google Scholar
15. 1. Endler JA

    (1990) On the measurement and classification of colour in studies of animal colour patterns

    Biological Journal of the Linnean Society 41:315–352.

    https://doi.org/10.1111/j.1095-8312.1990.tb00839.x

    • Google Scholar
16. 1. Engelmann JM
    2. Herrmann E
    3. Tomasello M

    (2012) Five-year olds, but not chimpanzees, attempt to manage their reputations

    PLOS ONE 7:e48433.

    https://doi.org/10.1371/journal.pone.0048433

    • PubMed
    • Google Scholar
17. 1. Farroni T
    2. Csibra G
    3. Simion F
    4. Johnson MH

    (2002) Eye contact detection in humans from birth

    PNAS 99:9602–9605.

    https://doi.org/10.1073/pnas.152159999

    • PubMed
    • Google Scholar
18. 1. Farroni T
    2. Massaccesi S
    3. Pividori D
    4. Johnson MH

    (2004) Gaze Following in Newborns

    Infancy 5:39–60.

    https://doi.org/10.1207/s15327078in0501_2

    • Google Scholar
19. Book

    1. Gomez JC

    (1996)

    Ostensive Behavior in Great Apes: The Role of Eye Contact. In Reaching into Thought: The Minds of the Great Apes

    New York: Cambridge University Press).

    • Google Scholar
20. 1. Gredebäck G
    2. Astor K
    3. Fawcett C

    (2018) Gaze Following Is Not Dependent on Ostensive Cues: A Critical Test of Natural Pedagogy

    Child Development 89:2091–2098.

    https://doi.org/10.1111/cdev.13026

    • PubMed
    • Google Scholar
21. 1. Heesen R
    2. Bangerter A
    3. Zuberbühler K
    4. Iglesias K
    5. Neumann C
    6. Pajot A
    7. Perrenoud L
    8. Guéry JP
    9. Rossano F
    10. Genty E

    (2021) Assessing joint commitment as a process in great apes

    IScience 24:102872.

    https://doi.org/10.1016/j.isci.2021.102872

    • PubMed
    • Google Scholar
22. 1. Itier RJ
    2. Latinus M
    3. Taylor MJ

    (2006) Face, eye and object early processing: what is the face specificity?

    NeuroImage 29:667–676.

    https://doi.org/10.1016/j.neuroimage.2005.07.041

    • PubMed
    • Google Scholar
23. 1. Jacobs GH
    2. Deegan JF
    3. Moran JL

    (1996) ERG measurements of the spectral sensitivity of common chimpanzee (Pan troglodytes)

    Vision Research 36:2587–2594.

    https://doi.org/10.1016/0042-6989(95)00335-5

    • PubMed
    • Google Scholar
24. 1. Jessen S
    2. Grossmann T

    (2014) Unconscious discrimination of social cues from eye whites in infants

    PNAS 111:16208–16213.

    https://doi.org/10.1073/pnas.1411333111

    • PubMed
    • Google Scholar
25. 1. Kaneko T
    2. Sakai T
    3. Miyabe-Nishiwaki T
    4. Tomonaga M

    (2013) A case of naturally occurring visual field loss in a chimpanzee with an arachnoid cyst

    Neuropsychologia 51:2856–2862.

    https://doi.org/10.1016/j.neuropsychologia.2013.09.011

    • PubMed
    • Google Scholar
26. 1. Kano F
    2. Tomonaga M

    (2013) Head-mounted eye tracking of a chimpanzee under naturalistic conditions

    PLOS ONE 8:e59785.

    https://doi.org/10.1371/journal.pone.0059785

    • PubMed
    • Google Scholar
27. 1. Kano F
    2. Call J

    (2014) Cross-species variation in gaze following and conspecific preference among great apes, human infants and adults

    Animal Behaviour 91:137–150.

    https://doi.org/10.1016/j.anbehav.2014.03.011

    • Google Scholar
28. 1. Kano F
    2. Moore R
    3. Krupenye C
    4. Hirata S
    5. Tomonaga M
    6. Call J

    (2018) Human ostensive signals do not enhance gaze following in chimpanzees, but do enhance object-oriented attention

    Animal Cognition 21:715–728.

    https://doi.org/10.1007/s10071-018-1205-z

    • PubMed
    • Google Scholar
29. 1. Kano F
    2. Furuichi T
    3. Hashimoto C
    4. Krupenye C
    5. Leinwand JG
    6. Hopper LM
    7. Martin CF
    8. Otsuka R
    9. 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 1:e4.

    https://doi.org/10.1016/j.evolhumbehav.2021.12.004

    • Google Scholar
30. 1. Kirk EC

    (2004) Comparative morphology of the eye in primates: The Anatomical Record Part A: Discoveries in Molecular

    Cellular, and Evolutionary Biology 281:1095–1103.

    https://doi.org/10.1002/ar.a.20115

    • PubMed
    • Google Scholar
31. 1. Kleinke CL

    (1986) Gaze and eye contact: a research review

    Psychological Bulletin 100:78–100.

    https://doi.org/10.1037/0033-2909.100.1.78

    • PubMed
    • Google Scholar
32. 1. Kobayashi H
    2. Kohshima S

    (1997) Unique morphology of the human eye

    Nature 387:767–768.

    https://doi.org/10.1038/42842

    • PubMed
    • Google Scholar
33. 1. Kobayashi H
    2. Kohshima S

    (2001) Unique morphology of the human eye and its adaptive meaning: comparative studies on external morphology of the primate eye

    Journal of Human Evolution 40:419–435.

    https://doi.org/10.1006/jhev.2001.0468

    • PubMed
    • Google Scholar
34. 1. Kothari R
    2. Yang Z
    3. Kanan C
    4. Bailey R
    5. Pelz JB
    6. Diaz GJ

    (2020) Gaze-in-wild: A dataset for studying eye and head coordination in everyday activities

    Scientific Reports 10:2539.

    https://doi.org/10.1038/s41598-020-59251-5

    • PubMed
    • Google Scholar
35. 1. Matsuno T
    2. Kawai N
    3. Matsuzawa T

    (2004) Color classification by chimpanzees (Pan troglodytes) in a matching-to-sample task

    Behavioural Brain Research 148:157–165.

    https://doi.org/10.1016/s0166-4328(03)00185-2

    • PubMed
    • Google Scholar
36. 1. Matsuno T
    2. Tomonaga M

    (2006) Measurement of contrast thresholds of chimpanzees using a Parameter Estimation by Sequential Testing (PEST) procedure

    The Japanese Journal of Psychonomic Science 25:115–116.

    https://doi.org/10.14947/psychono.KJ00004450516

    • Google Scholar
37. 1. Matsuzawa T

    (1990) Form perception and visual acuity in a chimpanzee

    Folia Primatologica; International Journal of Primatology 55:24–32.

    https://doi.org/10.1159/000156494

    • PubMed
    • Google Scholar
38. 1. Mayhew JA
    2. Gómez JC

    (2015) Gorillas with white sclera: A naturally occurring variation in a morphological trait linked to social cognitive functions

    American Journal of Primatology 77:869–877.

    https://doi.org/10.1002/ajp.22411

    • PubMed
    • Google Scholar
39. 1. Mearing AS
    2. Koops K

    (2021) Quantifying gaze conspicuousness: Are humans distinct from chimpanzees and bonobos?

    Journal of Human Evolution 157:103043.

    https://doi.org/10.1016/j.jhevol.2021.103043

    • PubMed
    • Google Scholar
40. 1. Myowa-Yamakoshi M
    2. Tomonaga M
    3. Tanaka M
    4. Matsuzawa T

    (2003) Preference for human direct gaze in infant chimpanzees (Pan troglodytes)

    Cognition 89:B53–B64.

    https://doi.org/10.1016/s0010-0277(03)00071-4

    • PubMed
    • Google Scholar
41. 1. Okamoto S
    2. Tomonaga M
    3. Ishii K
    4. Kawai N
    5. Tanaka M
    6. Matsuzawa T

    (2002) An infant chimpanzee (Pan troglodytes) follows human gaze

    Animal Cognition 5:107–114.

    https://doi.org/10.1007/s10071-002-0133-z

    • PubMed
    • Google Scholar
42. 1. Okamoto-Barth S
    2. Call J
    3. Tomasello M

    (2007) Great apes’ understanding of other individuals’ line of sight

    Psychological Science 18:462–468.

    https://doi.org/10.1111/j.1467-9280.2007.01922.x

    • PubMed
    • Google Scholar
43. 1. Okumura Y
    2. Kanakogi Y
    3. Kobayashi T
    4. Itakura S

    (2020) Ostension affects infant learning more than attention

    Cognition 195:104082.

    https://doi.org/10.1016/j.cognition.2019.104082

    • PubMed
    • Google Scholar
44. 1. Perea García JO

    (2016) Quantifying ocular morphologies in extant primates for reliable interspecific comparisons

    Journal of Language Evolution 1:151–158.

    https://doi.org/10.1093/jole/lzw004

    • Google Scholar
45. 1. Perea-García JO
    2. Kret ME
    3. Monteiro A
    4. Hobaiter C

    (2019) Scleral pigmentation leads to conspicuous, not cryptic, eye morphology in chimpanzees

    PNAS 116:19248–19250.

    https://doi.org/10.1073/pnas.1911410116

    • PubMed
    • Google Scholar
46. 1. Povinelli DJ
    2. Eddy TJ

    (1996) Joint visual attention

    Psychological Science 7:129–135.

    https://doi.org/10.1111/j.1467-9280.1996.tb00345.x

    • Google Scholar
47. 1. Provine RR
    2. Cabrera MO
    3. Nave-Blodgett J

    (2013a) Red, Yellow, and Super-White Sclera

    Human Nature 24:126–136.

    https://doi.org/10.1007/s12110-013-9168-x

    • PubMed
    • Google Scholar
48. 1. Provine RR
    2. Nave-Blodgett J
    3. Cabrera MO
    4. Zeh D

    (2013b) The Emotional Eye: Red Sclera as a Uniquely Human Cue of Emotion

    Ethology: Formerly Zeitschrift Fur Tierpsychologie 119:12144.

    https://doi.org/10.1111/eth.12144

    • Google Scholar
49. 1. Ricciardelli P
    2. Baylis G
    3. Driver J

    (2000) The positive and negative of human expertise in gaze perception

    Cognition 77:B1–B14.

    https://doi.org/10.1016/s0010-0277(00)00092-5

    • PubMed
    • Google Scholar
50. 1. Ross CF
    2. Kirk EC

    (2007) Evolution of eye size and shape in primates

    Journal of Human Evolution 52:294–313.

    https://doi.org/10.1016/j.jhevol.2006.09.006

    • PubMed
    • Google Scholar
51. 1. Segal NL
    2. Goetz AT
    3. Maldonado AC

    (2016) Preferences for visible white sclera in adults, children and autism spectrum disorder children: implications of the cooperative eye hypothesis

    Evolution and Human Behavior 37:35–39.

    https://doi.org/10.1016/j.evolhumbehav.2015.06.006

    • Google Scholar
52. 1. Senju A
    2. Csibra G

    (2008) Gaze following in human infants depends on communicative signals

    Current Biology 18:668–671.

    https://doi.org/10.1016/j.cub.2008.03.059

    • PubMed
    • Google Scholar
53. 1. Senju A
    2. Johnson MH

    (2009) The eye contact effect: mechanisms and development

    Trends in Cognitive Sciences 13:127–134.

    https://doi.org/10.1016/j.tics.2008.11.009

    • PubMed
    • Google Scholar
54. 1. Stevens M
    2. Stoddard MC
    3. Higham JP

    (2009) Studying Primate Color: Towards Visual System-dependent Methods

    International Journal of Primatology 30:893–917.

    https://doi.org/10.1007/s10764-009-9356-z

    • Google Scholar
55. 1. Tomasello M
    2. Hare B
    3. Agnetta B

    (1999) Chimpanzees, Pan troglodytes, follow gaze direction geometrically

    Animal Behaviour 58:769–777.

    https://doi.org/10.1006/anbe.1999.1192

    • PubMed
    • Google Scholar
56. 1. Tomasello M
    2. Carpenter M
    3. Call J
    4. Behne T
    5. Moll H

    (2005) Understanding and sharing intentions: The origins of cultural cognition

    Behavioral and Brain Sciences 28:675–691.

    https://doi.org/10.1017/S0140525X05000129

    • PubMed
    • Google Scholar
57. 1. Tomasello M
    2. Hare B
    3. Lehmann H
    4. Call J

    (2007) Reliance on head versus eyes in the gaze following of great apes and human infants: the cooperative eye hypothesis

    Journal of Human Evolution 52:314–320.

    https://doi.org/10.1016/j.jhevol.2006.10.001

    • PubMed
    • Google Scholar
58. 1. Tomonaga M

    (2007) Is chimpanzee (Pan troglodytes) spatial attention reflexively triggered by gaze cue?

    Journal of Comparative Psychology 121:156–170.

    https://doi.org/10.1037/0735-7036.121.2.156

    • PubMed
    • Google Scholar
59. 1. Tomonaga M
    2. Imura T

    (2010) Visual search for human gaze direction by a Chimpanzee (Pan troglodytes)

    PLOS ONE 5:e9131.

    https://doi.org/10.1371/journal.pone.0009131

    • PubMed
    • Google Scholar
60. 1. Whalen PJ
    2. Kagan J
    3. Cook RG
    4. Davis FC
    5. Kim H
    6. Polis S
    7. McLaren DG
    8. Somerville LH
    9. McLean AA
    10. Maxwell JS
    11. Johnstone T

    (2004) Human amygdala responsivity to masked fearful eye whites

    Science 306:2061.

    https://doi.org/10.1126/science.1103617

    • PubMed
    • Google Scholar
61. 1. Yamagiwa J

    (1992) Functional analysis of social staring behavior in an all-male group of mountain gorillas

    Primates 33:523–544.

    https://doi.org/10.1007/BF02381153

    • Google Scholar
62. 1. Yorzinski JL
    2. Miller J

    (2020) Sclera color enhances gaze perception in humans

    PLOS ONE 15:e0228275.

    https://doi.org/10.1371/journal.pone.0228275

    • PubMed
    • Google Scholar
63. 1. Yoshizaki K
    2. Kato K

    (2011) Contrast polarity of eyes modulates gaze-cueing effect1

    Japanese Psychological Research 53:333–340.

    https://doi.org/10.1111/j.1468-5884.2011.00474.x

    • Google Scholar

Author details

1. Fumihiro Kano

   1. Centre for the Advanced Study of Collective Behaviour, University of Konstanz, Konstanz, Germany
   2. Kumamoto Sanctuary, Kyoto University, Kumamoto, Japan
   3. Max Planck Institute of Animal Behavior, Radolfzell, Germany

   Contribution

   Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   fkano@ab.mpg.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4534-6630

2. Yuri Kawaguchi

   1. Messerli Research Institute, University of Veterinary Medicine Vienna, Vienna, Austria
   2. Japan Society for the Promotion of Science (JSPS), Tokyo, Japan
   3. Primate Research Institute, Kyoto University, Inuyama, Japan

   Contribution

   Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

3. Yeow Hanling

   Kumamoto Sanctuary, Kyoto University, Kumamoto, Japan

   Contribution

   Investigation, Writing – review and editing

   Competing interests

   No competing interests declared

• 6,515

  views

• 179

  downloads

• 11

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.