Are there vocal cues to human developmental stability? Relationships between facial fluctuating asymmetry and voice attractiveness

Abstract

Fluctuating asymmetry (FA), deviation from perfect bilateral symmetry, is thought to reflect an organism's relative inability to maintain stable morphological development in the face of environmental and genetic stressors. Previous research has documented negative relationships between FA and attractiveness judgments in humans, but scant research has explored relationships between the human voice and this putative marker of genetic quality in either sex. Only one study (and in women only) has explored relationships between vocal attractiveness and asymmetry of the face, a feature-rich trait space central in prior work on human genetic quality and mate choice. We therefore examined this relationship in three studies comprising 231 men and 240 women from two Western samples as well as Hadza hunter–gatherers of Tanzania. Voice recordings were collected and rated for attractiveness, and FA was computed from two-dimensional facial images as well as, for a subset of men, three-dimensional facial scans. Through meta-analysis of our results and those of prior studies, we found a negative association between FA and vocal attractiveness that was highly robust and statistically significant whether we included effect sizes from previously published work, or only those from the present research, and regardless of the inclusion of any individual sample or method of assessing FA (e.g., facial or limb FA). Weighted mean correlations between FA and vocal attractiveness across studies were −.23 for men and −.29 for women. This research thus offers strong support for the hypothesis that voices provide cues to genetic quality in humans.

Introduction

Mate choice is predicated, in part, on heritable fitness benefits (Petrie, 1994), and organisms are attentive to biomarkers that putatively indicate whether a potential mate possesses genes that would contribute additively to offspring fitness (Andersson, 1994)—that is, whether a mate is high in genetic quality (Hunt, Bussiere, Jennions, & Brooks, 2004). One such biomarker is fluctuating asymmetry (FA; e.g., Møller, 1992, Swaddle, 1996, Thornhill and Gangestad, 1999a, Van Valen, 1962, Van Valen, 1973). FA is exhibited in bilaterally symmetrical traits if the difference between the left and right sides has a population normal distribution with a mean of zero (Palmer & Strobeck, 1986). Substantial evidence from humans (e.g., Gangestad et al., 1994, Livshits and Kobyliansky, 1991) as well as an array of vertebrates and insects (Parsons, 1990) indicates that the degree to which bilaterally symmetrical traits deviate from perfect symmetry reflects developmental instability resulting from harmful mutations and environmental perturbations. Experimental exposure to common environmental stressors, for example, can increase asymmetry in laboratory rats (e.g., Mooney et al., 1985, Sciulli et al., 1979).

In humans, individuals with known genetic or chromosomal abnormalities have greater dental FA than do controls (e.g., Barden, 1980, Peretz et al., 1988), and FA displays a negative relationship with genetic heterozygosity (Livshits & Kobyliansky, 1991), which can increase fitness by lowering the risk of expressing deleterious recessive alleles and by increasing acquired immunity through the major histocompatibility complex (MHC; reviewed in Kempenaers, 2007). Lower FA in ear height, wrist breadth, and digit length has predicted reduced resting metabolic rate (Manning, Koukourakis & Brodie, 1997) and better mental health (Martin, Manning, & Dowrick, 1999) in men, and lower facial FA shows a similar relationship with perceptions of physical health (Jones et al., 2001). Moreover, FA is positively correlated with female body mass, age, and age at first childbirth, all indications of reduced fecundity (Manning, Scutt, Whitehouse & Leinster, 1997). A recent meta-analysis also found a small negative relationship between FA and general intelligence (Banks, Batchelor, & McDaniel, 2010). Together, these results suggest that bilateral symmetry may reflect the fit between an organism's genotype and environment during development.

As a putative indicator of a genotype's resilience to environmental insults, FA is related to mate choice across a variety of nonhuman species. For example, among field crickets (Gryllus campestris), males successful in obtaining mates display lower FA than do less successful males (Simmons, 1995). Likewise, female zebra finches (Taeniopygia guttata) prefer to be near males wearing symmetrically colored experimental leg bands (Swaddle, 1996).

In humans, several studies have reported significant correlations between FA and perceptions of facial attractiveness (e.g., Abend et al., 2015, Grammer and Thornhill, 1994, Komori et al., 2009, Perrett et al., 1999, Rhodes et al., 2001). In addition, women who view themselves as attractive show a greater preference for symmetry in male faces (Little, Burt, Penton-Voak, & Perrett, 2001), suggesting that symmetrical mates are valued and are more attainable by women of higher mate value. Some studies (e.g., Little and Jones, 2012, Little et al., 2007b), but not others (e.g., Peters, Simmons, & Rhodes, 2009), have found that women in the fertile phase of the ovulatory cycle exhibit a greater preference for symmetrical faces and bodies, again suggesting an association between symmetry and genetic quality, since genetic benefits can be obtained only when conception is possible. There is also evidence that humans mate assortatively for facial symmetry, indicating that symmetry or correlated traits may influence mate choice (Burriss, Roberts, Welling, Puts, & Little, 2011).

While bilateral symmetry appears to be important in predicting mating decisions, preferences for symmetrical mates may not always reflect preferences for symmetry per se. Bilateral symmetry has been found to predict attractiveness even in the absence of visual cues to asymmetry itself, and thus asymmetry must be related to other phenotypic cues. For example, women in the fertile phase of the ovulatory cycle have shown a preference for symmetrical men when exposed exclusively to the men's body odor (Gangestad and Thornhill, 1998, Thornhill and Gangestad, 1999b). Another study found a female preference for low FA in men even when study participants were shown only the left or right half of each male face, preventing them from assessing symmetry directly (Scheib, Gangestad, & Thornhill, 1999).

Developmental stability may also be conveyed vocally. Hughes, Harrison, and Gallup (2002) found both sexes to exhibit a negative relationship between upper limb FA (particularly finger length FA) and attractiveness assessed from vocal stimuli alone. Abend et al. (2015) similarly obtained a negative relationship between women's vocal attractiveness and measures of FA from their upper and lower limbs as well as the head and face. These studies join other research demonstrating the salience of voice as an influence on mate choice in humans (reviewed in Feinberg, 2008, Pisanski and Feinberg, 2013, Puts et al., 2012).

Moreover, vocal and facial attractiveness may covary (e.g., Saxton, Burriss, Murray, Rowland, & Roberts, 2009) in part because both the face and vocal folds are bilaterally symmetrical, and both may therefore reflect deleterious environmental influences during development. For example, asymmetric shape, size, or tension in the vocal folds could result in audible changes in the voice, such as hoarseness (Eysholdt, Rosanowski, & Hoppe, 2003), and indeed, Hughes, Pastizzo, and Gallup (2008) found that limb FA in men predicted a measure of vocal hoarseness. Developmental instability may also affect the size and shape of vocal structures, as well as tension on the vocal folds or the positioning of the larynx in the vocal tract, which would influence vocal pitch and timbre, respectively (for fuller consideration of potential links between FA and vocal attractiveness, please see Discussion).

Some research indicates that women's vocal attractiveness is related to fertility and reproductive potential (Bryant and Haselton, 2009, Pipitone and Gallup, 2008, Pipitone and Gallup, 2011, Puts et al., 2013, Wheatley et al., 2014), though scant research has explored relationships between vocal attractiveness and FA in either sex. To our knowledge, Abend et al. (2015) is the only study conducted to date investigating relationships between vocal attractiveness and facial FA. Furthermore, not all research on FA supports the prediction that individuals will tend to prefer mates lower in FA. For example, some research on humans (e.g., Langlois et al., 1994, Swaddle and Cuthill, 1995), as well as nonhuman species (e.g., Oakes and Barnard, 1994, Tomkins and Simmons, 1998), has failed to show preferences for mates with low FA, while other research has found a statistically significant relationship between FA and attractiveness only in particular situations (Springer et al., 2007).

There are likely several reasons for these discrepancies. First, FA is a weak index of developmental instability, such that associations between FA and measures of mate quality are difficult to detect using modest sample sizes (Van Dongen & Gangestad, 2011). Second, relationships with FA may be complicated by directional asymmetry (DA), which characterizes traits for which the difference between the left and right sides has a population normal distribution with a mean that deviates from zero (Møller, 1994). Directional asymmetry, such as occurs in testes size in many bird species (Møller, 1994) and in the lower limbs of humans (Auerbach & Ruff, 2006), may constitute part of an organism's normal development (Graham et al., 1998, Martin et al., 2008). Since the presence of DA may complicate measures of FA, it is critical to take DA into consideration in research examining FA. While some studies have done so (e.g., Abend et al., 2015, Brown et al., 2008, Manning, 1995), others have not (e.g., Gangestad and Thornhill, 1997, Hughes et al., 2002, Thornhill et al., 1995). Finally, prior research has disproportionately sampled from Western societies, especially individuals of European genetic ancestry. Not only do such individuals differ in facial morphology from those of other populations (Farkas, Katic, & Forrest, 2005), but Westerners may also have greater access to modern medical and cosmetic technologies that can buffer them from environmental stressors, weakening relationships between FA and measures of attractiveness (Apicella, 2011).

In the present paper, we tested whether somatic FA predicts vocal attractiveness by collecting data in three studies that were designed in part to address the limitations of prior research while enabling us to explore the robustness of these relationships across methodologies and populations. We measured FA from the face due to the centrality of facial symmetry in prior work as well as the status of the face as a feature-rich space that is developmentally distinct from the upper limb, measured by Hughes et al. (2002) and the upper and lower limb included in Abend et al. (2015). In Studies 1 and 2, we measured FA from two-dimensional (2D) facial photographs, following most prior studies of facial asymmetry and attractiveness (Jones et al., 2001). Study 1 data were collected from U.S. undergraduate students, whereas Study 2 data were collected from the Hadza, a Tanzanian forager population less protected by modern medicine from environmental insults than are samples drawn from the West. Compared to Western samples, Hadza facial and vocal characteristics should thus more strongly reflect individuals' constitutional resilience to environmental stressors, such as pathogens. Finally, in Study 3, we explored facial FA and vocal attractiveness among U.S. undergraduates using the 2D methods employed in the first two studies as well as three-dimensional (3D) images measured via spatially dense geometric morphometrics, which provides far greater shape information than does 2D imagery (Abend et al., 2015, Brown et al., 2008).