Evolution of color vision to detect social info: Dichromats may be less accurate at detecting others’ emotional states; dichromats may also display weaker approach/avoidance behavior toward healthy/sick individuals

Social Perception of Facial Color Appearance for Human Trichromatic Versus Dichromatic Color Vision. Christopher A. Thorstenson, Adam D. Pazda, Andrew J. Elliot. Personality and Social Psychology Bulletin, April 13, 2019. https://doi.org/10.1177/0146167219841641

Abstract: Typical human color vision is trichromatic, on the basis that we have three distinct classes of photoreceptors. A recent evolutionary account posits that trichromacy facilitates detecting subtle skin color changes to better distinguish important social states related to proceptivity, health, and emotion in others. Across two experiments, we manipulated the facial color appearance of images consistent with a skin blood perfusion response and asked participants to evaluate the perceived attractiveness, health, and anger of the face (trichromatic condition). We additionally simulated what these faces would look like for three dichromatic conditions (protanopia, deuteranopia, tritanopia). The results demonstrated that flushed (relative to baseline) faces were perceived as more attractive, healthy, and angry in the trichromatic and tritanopia conditions, but not in the protanopia and deuteranopia conditions. The results provide empirical support for the social perception account of trichromatic color vision evolution and lead to systematic predictions of social perception based on ecological social perception theory.

Keywords: trichromatic, color vision, social perception, evolution, face color


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The human face is a wellspring of social information; we can make rapid judgments about a wide range of social characteristics (e.g., sex, race, age, attractiveness, health, emotion) based on only a brief exposure to facial stimuli (Weisbuch & Ambady, 2011). Although a majority of traditional social psychological research has focused on assessing how these judgments influence downstream phenomena (e.g., stereotyping and behavior), only recently have researchers focused on elucidating the lower level perceptual mechanisms that produce these judgments in the first place (Freeman & Ambady, 2011; Oosterhof & Todorov, 2008). An emerging line of research has demonstrated that one such perceptual mechanism that can independently influence a range of social judgments is facial color appearance (for reviews, see (Rowland & Burriss, 2017; Stephen & Perrett, 2015; Thorstenson, 2018). This work suggests that human color vision plays a key role in social perception processes. In the current article, we briefly review theoretical accounts of human color vision evolution, including a recent account driven by social evolutionary considerations. We then overview the existing literature on the role of facial color appearance in the expression and perception of social characteristics (i.e., attractiveness, health, and emotion), grounded in an ecological theory of social perception (Zebrowitz-McArthur & Baron, 1983). Finally, we report two experiments that provide an empirical test of the social evolutionary account of human color vision.

Typical human (and most primate species) color vision is considered trichromatic, meaning we possess three distinct classes of wavelength-sensitive photoreceptive cells called cone photorecepters, or cones, that allow us to discriminate chromatic colors across the visible spectrum. These cones are distinguished as short wavelength (S; with peak sensitivity at ~430 nm), medium wavelength (M; with peak sensitivity at ~535 nm), and long wavelength (L; with peak sensitivity at ~562 nm; Jacobs & Deegan, 1999). Whereas most mammalian species possess dichromacy (having one S cone and one M/L cone), trichromacy in humans and most nonhuman primate species evolved when the older M/L cone opsin gene duplicated and diverged into two separate M and L cones (Dulai, von Dornum, Mollon, & Hunt, 1999).

The functional significance of trichromacy evolution is currently under debate. A popular account suggests that trichromacy was selected to aid primates in foraging by facilitating the detection of ripe fruit against green leaves (Allen, 1879; Lucas et al., 2003; Mollon, 1989; Osorio & Vorobyev, 1996; Surridge & Mundy, 2002). While there is support demonstrated for this hypothesis (Bunce, Isbell, Grote, & Jacobs, 2011; Caine & Mundy, 2000; Melin et al., 2009; Osorio, Smith, Vorobyev, & Buchanan-Smith, 2004; Regan et al., 2001; Smith, Buchanan-Smith, Surridge, & Mundy, 2003; Smith, Buchanan-Smith, Surridge, Osorio, & Mundy, 2003; Sumner & Mollon, 2000; Vorobyev, 2004), some ecological studies do not observe a benefit of trichromacy on foraging behavior (Hiramatsu et al., 2008; Vogel, Neitz, & Dominy, 2007). Other theoretical accounts of color vision variation in primates that have received less empirical attention include camouflage detection, predation detection, and nocturnal versus diurnal activity (see Kawamura & Melin, 2017, for a comprehensive review).

Alternatively, a more recent functional account posits that trichromacy may have been selected by social evolutionary pressures (Changizi, 2010; Changizi & Shimojo, 2011; Changizi, Zhang, & Shimojo, 2006). Specifically, this account suggests that the divergence of M and L cones allows for the optimal detection of socially relevant skin color appearance fluctuations in others. Changizi and colleagues (2006) note that changes in dermal hemoglobin oxygenation and concentration lead to predictable changes in the spectral reflectance (and consequently visible color) of skin. Increases in hemoglobin oxygenation heighten relative L-cone to M-cone activation, resulting in redder skin appearance (while decreases in hemoglobin oxygenation produce the opposite, resulting in greener skin appearance). Increases in hemoglobin concentration tend to increase M- and L-cone activation relative to the S cone, resulting in blue skin appearance, whereas decreases in hemoglobin concentration produce the opposite, resulting in yellow skin appearance (see also Thorstenson, 2018 for a review). Importantly, Changizi and colleagues (2006) demonstrated that M- and L-cone sensitivities in trichromats are situated in the visible spectrum such that they are able to optimally detect these skin color appearance fluctuations. This corre-spondence, between the spectral sensitivity of trichromatic photoreceptors and spectral fluctuations of skin enduring transient hemoglobin changes, presumably enables particu-lar sensitivity to discriminate socially relevant physiologi-cal conditions (e.g., emotional states, sexual signals, and threat displays). It has also been noted that trichromatic primates tend to be bare-faced, allowing rapid access to visual skin color appearance modulations. See Figure 1 for an illustration of the spectral characteristics of human skin and trichromatic photoreceptors. While there is some recent work supporting this hypothesis for viewing nonhuman pri-mate targets (Hiramatsu, Melin, Allen, Dubuc, & Higham, 2017) research in this area is still sparse and has yet to be conducted using human targets.

An ecological theory of social perception holds that social perception processes serve an adaptive function (Zebrowitz, Bronstad, & Montepare, 2011; Zebrowitz-McArthur & Baron, 1983). Perception facilitates goal attainment and species propagation by informing behavior (Gibson, 1979). This ecological approach to social perception assumes that (a) the external environment provides information to guide biologically and socially functional behaviors, and (b) the success-ful transfer of this information relies on a compatibility between a signal (stimulus information) and the perceiver (perceptual system). In the current investigation, we focus on the stimulus information (facial color expression) and the perceptual system (facial color perception) involved in social processes related to evaluation of attractiveness, health, and emotion. We chose to focus on these evaluations because they represent interpersonally important perceptions that shape social interaction and decision making. For instance, perceptions of attractiveness and health guide mating deci-sions because they provide an indicator of overall mate quality and reproductive potential (Etcoff, 1999; Perrett, 2010; Rhodes et al., 2007; Weeden & Sabini, 2005). Similarly, perceptions of emotion (e.g., anger) inform situational context (e.g., dominance, hostility) and guide behavior (e.g., avoidance; Marsh, Adams, & Kleck, 2005).

Indeed there is evidence that skin color appearance subtly undergoes change as an inevitable consequence of socially relevant states. In nonhuman primates, female skin color appearance becomes redder throughout the ovulatory ycle, when sexual cues afford the most significant reproductive consequences (Bielert, Girolami, & Jowell, 1989; Deschner, Heistermann, Hodges, & Boesch, 2004; Dixson, 1983; Gerald, 2003; Setchell & Wickings, 2004; Setchell, Wickings, & Knapp, 2006; Waitt, Gerald, Little, & Kraiselburd, 2006). Skin color appearance in male nonhu-man primates also influences female preferences by signal-ing elevated testosterone (Rhodes et al., 1997; Waitt et al., 2003). In addition, there is evidence that the same skin color appearance modulations occur in human females (Burriss et al., 2015; Edwards & Duntley, 1949; B. C. Jones et al., 2015; McGuiness, 1961; Oberzaucher et al., 2012; Snell & Turner, 1966; van den Berghe & Frost, 1986) and possibly males (due to elevated testosterone; Miller & Maner, 2010). Furthermore, skin color appearance undergoes change as a consequence of physiological states related to health, includ-ing skin vascularization (Changizi & Shimojo, 2011; Charkoudian, 2003; Henderson et al., 2017; Panza, Quyyumi, Brush, & Epstein, 1990; Ponsonby, Dwyer, & Couper, 1997; Sibenge & Gawkrodger, 1992; Wilkin, 1994), bilirubin (Knudsen & Brodersen, 1989), melanin (Stamatas, Zmudzka, Kollias, & Beer, 2004; Zonios, Bykowski, & Kollias, 2001) and carotenoids (Alaluf, Heinrich, Stahl, Tronnier, & Wiseman, 2002; Coetzee & Perrett, 2014; Tan, Graf, Mitra, & Stephen, 2015, 2017; Whitehead, Re, Xiao, Ozakinci, & Perrett, 2012). Finally, there is a sizable litera-ture examining the physiological correlates of experiencing various emotion states, which can then be used to predict how skin color appearance likely changes with respect to these emotions (see Thorstenson, 2018; Thorstenson, Elliot, Pazda, Perrett, & Xiao, 2018, for reviews).



Discussion: [...] Although the prevalence of dichromatic indi-viduals in the general population is quite low (between 2% and 8% of males and approximately 0.4% of females have a red-green color deficiency, and approximately 0.002% of both males and females have a blue-yellow color defi-ciency; Birch, 2012; Simunovic, 2010), these findings raise the possibility that certain color deficiencies exhibit less informed decision making in the social domain as a consequence of systematic misperception. For example, dichromats may be less accurate at detecting others’ emo-tional states, especially when facial expressions can be controlled (e.g., an angry person can maintain a neutral expression, but will still experience facial flushing). This may have problematic behavioral implications, such as failing to avoid someone with a flaring temper and a straight face. Dichromats may also display weaker approach/avoidance behavior toward healthy/sick individuals, and in the medical domain, it has been noted that dichromatic clinicians have significant difficulty in assess-ing clinically relevant skin color modulations (Changizi & Rio, 2010). Although empirical investigations into these possibilities would be difficult due to the relatively low prevalence of dichromats, they would be extremely informative nonetheless. [...]