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

External eye appearance across primate species is diverse in shape and colouration, yet we still lack an explanation for the drivers of such diversity. Here we quantify substantial interspecific variation in eye shape and colouration across 77 primate species representing all extant genera of anthropoid primates. We reassess a series of hypotheses aiming to explain ocular variation in horizontal elongation and in colouration across species. Heavier body weight and terrestrial locomotion are associated with elongated eye outlines. Species living closer to the equator present more pigmented conjunctivae, suggesting photoprotective functions. Irises become bluer in species living further away from the equator, adding to existing literature supporting a circadian clock function for bluer irises. These results shift the current focus from communicative, to ecological factors in driving variation in external eye appearance in anthropoid primates. They also highlight the possibility that similar ecological factors contributed to selection for blue eyes in ancestral human populations living in northern latitudes.

Section: Discussionmentioning

confidence: 70%

Ecological factors are likely drivers of eye shape and colour pattern variations across anthropoid primates

García

Ramarajan

Kret

et al. 2022

“…Recently, an investigation using iridoscleral ratios found humans, bonobos and chimpanzees to have comparable, not distinct, gaze conspicuousness www.nature.com/scientificreports/ despite large differences in scleral pigmentation 5 . This methodology, however, does not account for physical properties of visible light that may bias the naturalistic perception of shade 6,7,10 , a phenomenon that has recently been shown to influence the successful recognition of an averted gaze, even between primate species 7 . Furthermore, another recent study suggested that variation in primate external eye morphology may be due to genetic drift 6 .…”

Section: Discussionmentioning

confidence: 99%

“…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 .…”

mentioning

confidence: 99%

“…The cooperative eye hypothesis 9 suggests that, in human evolution, the human depigmented sclera has functioned to facilitate hyper-cooperative behaviours observed 9,17 through, for example, the establishment of joint attentional states. A white background may signal iridal direction more conspicuously and in a manner that is more difficult to conceal than would a dark background 7,10,18 . Contrastingly, the 'gaze camouflage hypothesis'…”

mentioning

confidence: 99%

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The evolutionary drivers of primate scleral coloration

Mearing

Burkart

Dunn

et al. 2022

The drivers of divergent scleral morphologies in primates are currently unclear, though white sclerae are often assumed to underlie human hyper-cooperative behaviours. Humans are unusual in possessing depigmented sclerae whereas many other extant primates, including the closely-related chimpanzee, possess dark scleral pigment. Here, we use phylogenetic generalized least squares (PGLS) analyses with previously generated species-level scores of proactive prosociality, social tolerance (both n = 15 primate species), and conspecific lethal aggression (n = 108 primate species) to provide the first quantitative, comparative test of three existing hypotheses. The ‘self-domestication’ and ‘cooperative eye’ explanations predict white sclerae to be associated with cooperative, rather than competitive, environments. The ‘gaze camouflage’ hypothesis predicts that dark scleral pigment functions as gaze direction camouflage in competitive social environments. Notably, the experimental evidence that non-human primates draw social information from conspecific eye movements is unclear, with the latter two hypotheses having recently been challenged. Here, we show that white sclerae in primates are associated with increased cooperative behaviours whereas dark sclerae are associated with reduced cooperative behaviours and increased conspecific lethal violence. These results are consistent with all three hypotheses of scleral evolution, suggesting that primate scleral morphologies evolve in relation to variation in social environment.

“…Likewise, the involvement of irido-scleral contrast in triadic communication 4 may not have been the most basal driver of selection for scleral depigmentation as proposed by Tomasello et al 3 , but the result of co-option. As we have no way of reaching into the past to interview our extinct ancestors, answers to such questions can only be approximated through comparative research with other animals, in particular other primates 11,14,43,47,[69][70][71] . The recent spike in such studies highlights the importance of comparative research in assessing the adaptive significance of human ocular morphology.…”

Section: Discussionmentioning

confidence: 99%

The adaptive significance of human scleral brightness: an experimental study

Wacewicz

García

Lewandowski

et al. 2022

Homogeneously depigmented sclerae have long been proposed to be uniquely human—an adaptation to enable cooperative behaviour by facilitating interpersonal coordination through gaze following. However, recent evidence has shown that deeply pigmented sclerae also afford gaze following if surrounding a bright iris. Furthermore, while current scleral depigmentation is clearly adaptive in modern humans, it is less clear how the evolutionarily intermediate stages of scleral pigmentation may have been adaptive. In sum, it is unclear why scleral depigmentation became the norm in humans, while not so in sister species like chimpanzees, or why some extant species display intermediate degrees of pigmentation (as our ancestors presumably did at some point). We created realistic facial images of 20 individually distinct hominins with diverse facial morphologies, each face in the (i) humanlike bright sclera and (ii) generalised apelike dark sclera version. Participants in two online studies rated the bright-sclera hominins as younger, healthier, more attractive and trustworthy, but less aggressive than the dark-sclera hominins. Our results support the idea that the appearance of more depigmented sclerae promoted perceived traits that fostered trust, increasing fitness for those individuals and resulting in depigmentation as a fixed trait in extant humans.