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

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.