Look past the cooperative eye hypothesis: reconsidering the evolution of human eye appearance

Abstract

The external appearance of the human eye has been prominently linked to the evolution of complex sociocognitive functions in our species. The cooperative eye hypothesis (CEH) proposes that human eyeballs, with their weakly expressed conjunctival and scleral pigmentation, are uniquely conspicuous and evolved under selective pressures to behave cooperatively, therefore signalling attentiveness to conspecifics. Non-human primates are instead assumed to display less-salient eye morphologies that help mask their gaze to facilitate competitive, rather than cooperative actions. Here, we argue that the CEH, although continuing to be influential, lacks robust empirical support. Over the past two decades, multidisciplinary research has undermined its original rationale and central premises: human eye pigmentation does not uniquely stand out among primates, it is not uniform at species level and the available evidence does not conclusively suggest that it facilitates gaze following to notable extents. Hence, the CEH currently provides a theoretical framework that risks confusing, rather than informing, inferences about the evolution of human external eye appearance and its selective drivers. In a call to move past it, we review alternative hypotheses with the potential to elucidate the emergence of the human ocular phenotype from the considerable spectrum of diversity found within the primate order.

Keywords: communication; conjunctiva; intraspecific variation; photoprotection; pigmentation; primates; sclera.

Fig. 1

Occurrence of the expression “cooperative eye hypothesis” in academic publications published in the respective year according to Google Scholar. Data inspected on April 21st, 2025, results included only up to 2024. Data collected using code made available by Strobel (2018).

Fig. 2

Brightness measurements of peri‐iridal tissues (sclera and overlying conjunctiva) taken from photographs of two non‐human primate species (golden langur Trachypithecus geei; southern pig‐tailed macaque Macaca nemestrina) that notably overlap with humans (Homo sapiens) in this regard [data for T. geei and H. sapiens from Perea‐García et al. (2022); data for M. nemestrina from Perea‐García et al. (2024); only adults were considered]. Photograph credits: H. sapiens: Duke University, used with permission; M. nemestrina: iNaturalist, Bridgette Gower; T. geei: iNaturalist, Ernst Hüttinger. Non‐human primate images are licensed under CC BY‐NC (https://creativecommons.org/licenses/by‐nc/4.0/).

Fig. 3

Reconstruction of ancestral peri‐iridal pigmentation in anthropoid primates based on species‐averaged brightness [hue‐saturation‐brightness (HSB) colour space] value measurements taken from digital photographs (maximum likelihood estimates assuming a Brownian motion model of evolutionary change). Colour is approximated. Note that weak pigmentation in humans was acquired secondarily but that several lineages of non‐human primates evolved similarly depigmented eyes convergently. Human data incorporated in this graphic primarily derive from white Eurasians and must therefore be interpreted with caution. Data from Perea‐García et al. (2022, 2024). Silhouettes derived from Phylopic. Credits: Kai R. Caspar – Hylobates, Leontopithecus, Macaca, Saguinus, Sapajus, Semnopithecus, Theropithecus; remaining silhouettes are in public domain. Figure created using the contMap() function in the R package phytools (Revell, 2012).

Fig. 4

An impression of the diversity of peri‐iridal pigmentation found among modern humans. All photographs by Marios Forsos unless indicated otherwise. Note that the ethnic background of the persons concerned was often not known to us so that we only indicate the state in which the photograph was taken. Left to right, top to bottom ‐ 1. row: Kenya, Myanmar, Bangladesh, Ethiopia, Mali, 2nd row: Mongolia, Tanzania, Mali, Vietnam, India, 3rd row: India (photograph by Surabhi Vijayaraghavan, CC BY‐SA 4.0, https://creativecommons.org/licenses/by‐sa/4.0/deed.de), India, Ecuador, Australia (photograph by Gunther Deichmann, used with permission), Ladakh (India/Pakistan), 4th row: Ivory Coast, Ethiopia, Singapore (Chinese ancestry; photograph by JOPG), India (photograph by Rita Willaert, CC BY‐NC‐SA 4.0, https://creativecommons.org/licenses/by‐sa/4.0/deed.de). [Correction added on 20 May 2025, after first online publication: In the caption of Figure 4, the description of the 4th row has been corrected.]

Fig. 5

Peri‐iridal pigmentation in primates is indicative of photoregulatory needs. (A) Exemplar ocular phenotypes of catarrhine primates across latitudes, the equator is shown as an orange line. From top to bottom: Homo sapiens (Europe; public domain), Trachypithecus geei (by Ernst Hüttinger ‐ CC BY‐NC, https://creativecommons.org/licenses/by‐nc/4.0/), Macaca sylvanus, Theropithecus gelada, Homo sapiens (East Africa; public domain), Pan troglodytes, Papio ursinus (by flowcomm. CC BY 2.0, https://creativecommons.org/licenses/by/2.0/deed.en). Primate images taken from Perea‐García et al. (2022), if not otherwise indicated. Globe model by Pavel Matoušek (CC BY‐NC, https://creativecommons.org/licenses/by/4.0/). (B) Relationship between peri‐iridal pigmentation and latitude (mean of species range) in anthropoid primates. Taken from Perea‐García et al. (2022). (C) Relationship between peri‐iridal pigmentation and skin brightness in individual macaques (genus Macaca). Data from Perea‐García et al. (2024).

Fig. 6

Examples of anthropoid primate species with contrasting facial coloration highlighting the eyes. (A) Ateles marginatus, photograph by John Sullivan (iNaturalist, CC BY‐NC, https://creativecommons.org/licenses/by/4.0/). (B) Cercocebus torquatus, photograph by Rufus46 (Wikimedia Commons, CC BY‐SA 3.0, https://creativecommons.org/licenses/by‐sa/3.0/deed.de). (C) Theropithecus gelada, photograph by Jose Antonio Pascual Trillo (iNaturalist, CC BY‐NC). (D) Pongo abelii by William B. Grice (CC BY‐SA 4.0, https://creativecommons.org/licenses/by‐sa/4.0/deed.de). In this species, as in orangutans in general, light eyelids and patches around the eyes are invariably found in juveniles and are sometimes retained into adulthood, as is the case here.