Abstract
For social species such as primates, the recognition of conspecifics is crucial for their survival. As demonstrated by the ‘face inversion effect’, humans are experts in recognizing faces and unlike objects, recognize their identity by processing it configurally. The human face, with its distinct features such as eye-whites, eyebrows, red lips and cheeks signals emotions, intentions, health and sexual attraction and, as we will show here, shares important features with the primate behind. Chimpanzee females show a swelling and reddening of the anogenital region around the time of ovulation. This provides an important socio-sexual signal for group members, who can identify individuals by their behinds. We hypothesized that chimpanzees process behinds configurally in a way humans process faces. In four different delayed matching-to-sample tasks with upright and inverted body parts, we show that humans demonstrate a face, but not a behind inversion effect and that chimpanzees show a behind, but no clear face inversion effect. The findings suggest an evolutionary shift in socio-sexual signalling function from behinds to faces, two hairless, symmetrical and attractive body parts, which might have attuned the human brain to process faces, and the human face to become more behind-like.
Introduction
For group-living animals, primates included, the recognition of conspecifics is crucial for their survival. Humans have specialized brain areas to recognize faces[1] and whole bodies[2–5] and their expertise in face recognition is demonstrated by the ‘inversion effect’, showing that faces and whole bodies, but not objects, are recognized configurally rather than by their parts[6–8]. Importantly, their recognition is disproportionally impaired, relative to objects such as houses or cars, when they are seen inverted rather than upright[6]. Conclusive evidence has shown that this effect is primarily due to a disruption in the processing of configural, rather than featural, information in faces [e.g., [9–13]. The face inversion effect has been observed in chimpanzees too, and although not all chimpanzees show this effect at all times[14, 15], overall there is evidence that configural processing is a critical element of efficient face detection in chimpanzees as well[16, 17]. Thus, effects of inversion have been observed for faces and whole bodies, but are generally not found for individual body parts[18]. Intriguingly, previous studies included almost all body parts, except the most obvious one, which is the behind, as we will outline below.
Previous research has shown that in recognizing each other, chimpanzees do not rely on the face alone[14], but also easily recognize each other by their behinds[19]. Most non-human female primates, chimpanzees included, show a swelling and reddening of the anogenital region around the time of ovulation[20]. At some point during human evolution, these changes in size and color along the menstrual cycle have disappeared, and large quantities of ‘permanent’ adipose tissue on the behind emerged[21, 22]. Possibly, this became more adaptive when our species started to walk upright, or to hide oestrus as to be attractive for males throughout the menstrual cycle and foster pair bond formation and shared caring for offspring. To date, it is not known how behinds as compared to faces are recognized in humans and their closest relatives, but this knowledge can enhance our understanding of the evolution of face processing, as we will argue below.
Face recognition plays an incredibly important role in the survival of animals living in social groups, including humans and chimpanzees. The changeable properties of faces like expression and gaze, display emotions and intentions and are used by observers to predict behavior[23]. The more or less invariant properties of faces are used for identification and display physical characteristics, including sex, age and attractiveness[1].
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Note: Configural recognition means that something is recognized as a whole (as a gestalt), rather than recognizing parts and assembling them into a whole. David Hays and I discuss this in Metaphor, Recognition, and Neural Process (1987). The Wikipedia entry on the Thatcher effect is about configural processing of faces.
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