The erotic appeal of the human-typical face-to-face posture during sex may related to the fact that human faces have evolved to become more behind-like

From 2016... Kret ME, Tomonaga M (2016) Getting to the Bottom of Face Processing. Species-Specific Inversion Effects for Faces and Behinds in Humans and Chimpanzees (Pan Troglodytes). PLoS ONE 11(11): e0165357. https://doi.org/10.1371/journal.pone.0165357

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.

Discussion

The current study shows chimpanzee’s expertise in recognizing behinds and suggests they process the bright pink sex swellings of female chimpanzees configurally and in a similar way as humans process faces. The female chimpanzee’s behind has a very high socio-sexual signaling function and the changes in size and color over the menstrual cycle reflect fertility. For that reason, it is important for conspecifics to be able to quickly detect this signal in the environment, but at the same time, it is vital to know who the behind belongs to[19]. For male chimpanzees this is relevant to prevent inbreeding. In turn, for female chimpanzees it is relevant to be aware of competing females to protect their own mating success.

The current study replicates previous research on the face inversion effect in humans, demonstrating that they process faces configurally[2]. In line with our hypothesis, the face inversion effect was dampened when faces were turned into greyscale, but still strongly significant, which is in line with previous research in humans showing that orientation is more important than color when it comes to processing human faces[31]. Also without color, the human face contains many high contrasting features such as eye whites, a prominent nose and lips and eyebrows. Although facial color can provide important social information, such as about emotions and health, there are also minor alterations over the menstrual cycle [40]. However, these small changes are beyond any comparison with the rich coloration of the chimpanzee behind where the alterations are much more obvious. In chimpanzees, the relevance of color for processing behinds is reflected in the absence of the behind inversion effect when pictures of behinds were presented in greyscale. In real life, the size and color of the swelling change in synchrony over the menstrual cycle. Thus, a full swelling around estrus is always redder than the female behind half a cycle later. It is therefore possible that due to the un-naturalistic mismatch between color (grey) and size (full swelling), these behinds were processed as objects, i.e., identified by the parts rather than as a whole.

Like humans, great apes are optimally equipped to process color and the spectral sensitivity of the cones in their retinas is ideal for discriminating both density of hemoglobin and oxygen saturation of the blood[30]. Also, the brain areas specialized in processing faces and bodies possess unique neural wiring to effectively process color[32, 33]. Once developed over the course of evolution, color vision (and especially trichromatic color perception) proceeded to impose a selective pressure on certain external traits such as the pink female sexual swelling in chimpanzees and the red lips and cheeks in humans.

A limitation of this study is the low number of individuals in the chimpanzee sample. Although this is common in most primate research and is largely compensated for by the large number of trials per individual, it is possible that effects would have been stronger had we been able to test a larger sample. Moreover, the chimpanzees in our sample were adolescents and adults and we can therefore only speculate about whether this specialization in processing behinds is inborn or related to expertise and emerged sometime during the developmental trajectory. In humans, the specialization for faces occurs already in the first couple of months of life[41]. In fact, already from birth, infants are interested in other people’s faces and eyes and make eye-contact[42]. The making of eye-contact is also facilitated in our species as walking upright freed the hands of parents, allowing them to carry their babies in their arms more often[43]. In contrast, chimpanzees are knuckle-walkers and carry their infants on their belly or back. For them, the swellings become particularly relevant only around puberty. The swellings also appear around that time, i.e., around the age of 10, and at that age, the color of the face changes from pink to a permanent black tint, reducing the contrast with the rest of the body[20]. The swellings stand out enormously in terms of color, size, smoothness and shininess and have a much stronger socio-sexual signaling function in the chimpanzee than the face. Future experiments with larger sample sizes are needed to test for sex differences and could also benefit from including male behinds as a control condition. In addition, it might be valuable to repeat this experiment in the bonobo (Pan Paniscus), as this species is as closely related to us as the chimpanzee but uses sex as a way to prevent and solve conflicts, has an alpha female rather than an alpha male[44] and is known to be highly attentive towards pictures showing genitals and even pay more attention to this category than to images showing threat displays[45].

In sum, applying well-established psychological paradigms to our closest relatives represents a promising approach to providing insight into the evolution of behavior. For primates, being able to recognize each other is necessary for detecting mates. Yin’s(1969) landmark article about the ‘face inversion effect’ turned the face-literature upside-down and hundreds of articles since describe that humans process faces unlike objects. But how faces compare to another body part similar in shape, size, color and attractiveness was thus far unknown. The present study demonstrates that chimpanzees, unlike humans, show a ‘behind inversion effect’ and suggests that identity recognition ‘moved up’ from the bottom to the face in our uprightly walking species. The findings of our study suggest that over human evolution the face took over important properties shared with the primate behind and largely replaced its socio-sexual signaling function, making our species attuned to faces.