Plain faces are more expressive: comparative study of facial colour, mobility and musculature in primates.

Facial colour patterns and facial expressions are among the most important phenotypic traits that primates use during social interactions. While colour patterns provide information about the sender's identity, expressions can communicate its behavioural intentions. Extrinsic factors, including social group size, have shaped the evolution of facial coloration and mobility, but intrinsic relationships and trade-offs likely operate in their evolution as well. We hypothesize that complex facial colour patterning could reduce how salient facial expressions appear to a receiver, and thus species with highly expressive faces would have evolved uniformly coloured faces. We test this hypothesis through a phylogenetic comparative study, and explore the underlying morphological factors of facial mobility. Supporting our hypothesis, we find that species with highly expressive faces have plain facial colour patterns. The number of facial muscles does not predict facial mobility; instead, species that are larger and have a larger facial nucleus have more expressive faces. This highlights a potential trade-off between facial mobility and colour patterning in primates and reveals complex relationships between facial features during primate evolution.

A volumetric comparison of the insular cortex and its subregions in primates.

The neuronal composition of the insula in primates displays a gradient, transitioning from granular neocortex in the posterior-dorsal insula to agranular neocortex in the anterior-ventral insula with an intermediate zone of dysgranularity. Additionally, apes and humans exhibit a distinctive subdomain in the agranular insula, the frontoinsular cortex (FI), defined by the presence of clusters of von Economo neurons (VENs). Studies in humans indicate that the ventral anterior insula, including agranular insular cortex and FI, is involved in social awareness, and that the posterodorsal insula, including granular and dysgranular cortices, produces an internal representation of the body's homeostatic state.We examined the volumes of these cytoarchitectural areas of insular cortex in 30 primate species, including the volume of FI in apes and humans. Results indicate that the whole insula scales hyperallometrically (exponent=1.13) relative to total brain mass, and the agranular insula (including FI) scales against total brain mass with even greater positive allometry (exponent=1.23), providing a potential neural basis for enhancement of social cognition in association with increased brain size. The relative volumes of the subdivisions of the insular cortex, after controlling for total brain volume, are not correlated with species typical social group size. Although its size is predicted by primate-wide allometric scaling patterns, we found that the absolute volume of the left and right agranular insula and left FI are among the most differentially expanded of the human cerebral cortex compared to our closest living relative, the chimpanzee.

Coevolution of facial expression and social tolerance in macaques.

The purpose of this study is to test the hypothesis that social tolerance drives the evolution of facial expression in macaques. Macaque species exhibit a range of social styles that reflect a continuum of social tolerance. Social interactions in more tolerant taxa tend to be less constrained by rank and kinship than in less-tolerant macaques. I predicted that macaques that are more tolerant would exhibit a wider range of facial displays than less-tolerant species because interactions that are open to negotiation are characterized by greater uncertainty than interactions that are constrained by rank or kinship. To test this hypothesis, I conducted a phylogenetically informed regression analysis (N = 11) using previously published data on repertoire size and two quantitative measures of social tolerance (conciliatory tendency and counter-aggression). As predicted, macaques with more tolerant social styles tended to have larger repertoires than less-tolerant species. These results support the hypothesis that increased social tolerance favors the elaboration of communication to mitigate uncertainty.

Correlated evolution of brain regions involved in producing and processing facial expressions in anthropoid primates.

Anthropoid primates are distinguished from other mammals by having relatively large primary visual cortices (V1) and complex facial expressions. We present a comparative test of the hypothesis that facial expression processing coevolved with the expansion of V1 in anthropoids. Previously published data were analysed using phylogenetic comparative methods. The results of our study suggest a pattern of correlated evolution linking social group size, facial motor control and cortical visual processing in catarrhines, but not platyrrhines. Catarrhines that live in relatively large social groups tended to have relatively large facial motor nuclei, and relatively large primary visual cortices. We conclude that catarrhine brains are adapted for producing and processing complex facial displays.

Sexual dimorphism in chin shape: implications for adaptive hypotheses.

The chin, or mentum osseum, is one of the most distinctive anatomical traits of modern humans. A variety of hypotheses for the adaptive value of the chin have been proposed, ranging from mechanical stress resistance to sexual selection via mate choice. While the sexual selection hypothesis predicts dimorphism in chin shape, most biomechanical hypotheses preclude it. Therefore determining the presence or absence of significant sexual dimorphism in chin shape provides a useful method for differentiating between various adaptive hypotheses; however, this has yet to be done due to a lack of quantitative data on chin shape. The goals of this study are therefore: (1) to introduce a new method for quantifying chin shape and (2) to determine the presence or absence of sexual dimorphism in chin shape in a diverse sample of modern humans. Samples were drawn from recent human skeletal collections representing nine geographic regions. Outlines of mentum osseum contours were quantified using elliptical Fourier function analysis (EFFA). Fourier coefficients were analyzed using principal components analysis (PCA). Sexual dimorphism in chin shape was assessed using PC loadings in the pooled geographic sample, and statistically significant differences were found. These findings provide the first quantitative, morphologically based evidence in support of adaptive hypotheses that predict dimorphism in chin shape, including the sexual selection hypothesis.

Allometry of facial mobility in anthropoid primates: implications for the evolution of facial expression.

Body size may be an important factor influencing the evolution of facial expression in anthropoid primates due to allometric constraints on the perception of facial movements. Given this hypothesis, I tested the prediction that observed facial mobility is positively correlated with body size in a comparative sample of nonhuman anthropoids. Facial mobility, or the variety of facial movements a species can produce, was estimated using a novel application of the Facial Action Coding System (FACS). I used FACS to estimate facial mobility in 12 nonhuman anthropoid species, based on video recordings of facial activity in zoo animals. Body mass data were taken from the literature. I used phylogenetic generalized least squares (PGLS) to perform a multiple regression analysis with facial mobility as the dependent variable and two independent variables: log body mass and dummy-coded infraorder. Together, body mass and infraorder explain 92% of the variance in facial mobility. However, the partial effect of body mass is much stronger than for infraorder. The results of my study suggest that allometry is an important constraint on the evolution of facial mobility, which may limit the complexity of facial expression in smaller species. More work is needed to clarify the perceptual bases of this allometric pattern.

Socioecological correlates of facial mobility in nonhuman anthropoids.

Facial mobility, or the variety of facial movements a species can produce, is likely influenced by selection for facial expression in diurnal anthropoids. The purpose of this study is to examine socioecological correlates of facial mobility independent of body size, focusing on social group size and arboreality as possible evolutionary agents. Group size was chosen because facial expressions are important for group cohesion, while arboreality may limit the utility of facial expressions. Data for 12 nonhuman anthropoid species were taken from previous studies and analyzed using a phylogenetic generalized least-squares approach. Regression results indicate that group size is a good predictor of facial mobility independent of body size. No statistical support was found for the hypothesis that arboreality constrains the evolution of facial mobility. The correlation between facial mobility and group size may be a consequence of selection for more effective facial expression to help manage conflicts and facilitate bonding in larger groups. These findings support the hypothesis that the ultimate function of facial expression is related to group cohesion.

Geographic variation in chin shape challenges the universal facial attractiveness hypothesis.

The universal facial attractiveness (UFA) hypothesis proposes that some facial features are universally preferred because they are reliable signals of mate quality. The primary evidence for this hypothesis comes from cross-cultural studies of perceived attractiveness. However, these studies do not directly address patterns of morphological variation at the population level. An unanswered question is therefore: Are universally preferred facial phenotypes geographically invariant, as the UFA hypothesis implies? The purpose of our study is to evaluate this often overlooked aspect of the UFA hypothesis by examining patterns of geographic variation in chin shape. We collected symphyseal outlines from 180 recent human mandibles (90 male, 90 female) representing nine geographic regions. Elliptical Fourier functions analysis was used to quantify chin shape, and principle components analysis was used to compute shape descriptors. In contrast to the expectations of the UFA hypothesis, we found significant geographic differences in male and female chin shape. These findings are consistent with region-specific sexual selection and/or random genetic drift, but not universal sexual selection. We recommend that future studies of facial attractiveness take into consideration patterns of morphological variation within and between diverse human populations.

On the evolution of the serotonin transporter linked polymorphic region (5-HTTLPR) in primates.

Some allelic variants of the serotonin transporter linked polymorphic region (5-HTTLPR) result in lower levels of expression of the serotonin transporter gene (SLC6A4). These low-expressing (LE) alleles are associated with mental-health disorders in a minority of humans that carry them. Humans are not the only primates that exhibit this polymorphism; other species, including some monkeys, also have LE and high-expressing (HE) variants of 5-HTTLPR. We propose a behavioral genetic framework to explain the adaptive evolution of this polymorphism in primates, including humans. We hypothesize that both LE and HE alleles are maintained by balancing selection in species characterized by short-term fluctuations in social competition levels. More specifically, we propose that LE carriers benefit from their hypervigilant tendencies during periods of elevated competition, whereas HE homozygotes cope best when competition levels do not deviate from the norm. Thus, both alleles have long-term benefits when competition levels tend to vary substantially over relatively short timescales within a social group. We describe this hypothesis in detail and outline a series of predictions to test it. Some of these predictions are supported by findings in the current literature, while others remain areas of future research.

Mosaic evolution of brainstem motor nuclei in catarrhine primates.

Facial motor nucleus volume coevolves with both social group size and primary visual cortex volume in catarrhine primates as part of a specialized neuroethological system for communication using facial expressions. Here, we examine whether facial nucleus volume also coevolves with functionally unrelated brainstem motor nuclei (trigeminal motor and hypoglossal) due to developmental constraints. Using phylogenetically informed multiple regression analyses of previously published brain component data, we demonstrate that facial nucleus volume is not correlated with the volume of other motor nuclei after controlling for medulla volume. Our results show that brainstem motor nuclei can evolve independently of other developmentally linked structures in association with specific behavioral ecological conditions. This finding provides additional support for the mosaic view of brain evolution.

The degree and pattern of phylogenetic signal in primate long-bone structure.

Interspecific scaling is a fundamental tool for comparative studies of primate long-bone structure and adaptation. However, scaling analyses based on conventional statistical methods can lead to false positives regarding adaptive relationships when traits exhibit strong phylogenetic signal. This problem can be addressed through the use of phylogenetic comparative methods (PCMs). To date, PCMs have not been incorporated into comparative studies of primate long-bone structure because it has been assumed that long-bone structure is free of phylogenetic signal once appropriately scaled. To test this assumption, we evaluated the degree of phylogenetic signal in three types of long-bone structural traits (bone length, articular surface areas, and cross-sectional geometric properties) from 17 quadrupedal primate species. We compared the pattern of phylogenetic signal in raw trait values and residual trait values after regression against body mass, bone length, and the product of body mass x bone length. Our results show that significant phylogenetic signal is present in all traits before scaling, due in part to their strong covariance with body mass. After scaling, bone length still exhibits strong phylogenetic signal, but articular surface areas do not, and cross-sectional properties exhibit different levels of signal depending on the variable used to scale the data. These results suggest that PCMs should be incorporated into interspecific studies of bone length and perhaps cross-sectional geometric properties. Our results also demonstrate that tests for phylogenetic signal prior to implementing a PCM should focus on residual variance, not individual traits.

Are the differences between Stw 431 (Australopithecus africanus) and A.L. 288-1 (A. afarensis) significant?

Recent studies of early hominin body proportions paint a complex evolutionary picture, with multiple instances of reversal in body shape. These interpretations rest heavily upon the inferred limb joint proportions of Australopithecus africanus. For example, the partial skeleton Stw 431 has been suggested to show ape-like joint proportions compared to the A. afarensis specimen A.L. 288-1. This suggests an evolutionary reversal in the more recent A. africanus. However, no study has examined the probability of sampling the differences between Stw 431 and A.L. 288-1 from a single extant hominoid species. The present study compares elbow/hip and elbow/lumbosacral joint size ratios between Stw 431 and A.L. 288-1 using exact randomization, based on chimpanzee and human models of variation. Results indicate that differences in elbow/hip proportions between Stw 431 and A.L. 288-1 can be sampled from a single species. In contrast, differences in elbow/lumbosacral proportions between Stw 431 and A.L. 288-1 show a significantly low probability of being sampled from a single species. Thus, Stw 431 and A.L. 288-1 are not significantly different from each with regard to limb joint proportions, but Stw 431 has a significantly smaller lumbosacral joint. This pattern does not conform to previous interpretations of limb proportions in A. africanus. Low statistical power in the present study may account for the discrepancy. Further research is needed to illuminate the functional implications of variation in relative lumbosacral joint size in early hominins.

Cross-sectional geometry and morphology of the mandibular symphysis in Middle and Late Pleistocene Homo.

Studies of the evolutionary emergence of the human "chin" have been investigated from a phylogenetic perspective during the later Pleistocene or from a biomechanical perspective across extant primates. Since it was during the Middle and Late Pleistocene that the distinctive human mentum osseum emerged, the relationship between mentum osseum form and resistance to mechanical stress at the mandibular symphysis was examined for forty-two Middle and Late Pleistocene human mandibles. Mentum osseum variation was scored on a five-point ordinal scale (mentum osseum rank). Resistance to bending was represented by second moments of area calculated from symphyseal cross-sections. Relative strength in bending was represented by second moments of area divided by estimated moment arm or beam length. Vertical bending resistance in the coronal plane was maintained across the range of mentum osseum variation within and between later Pleistocene human groups. In contrast, resistance to lateral transverse bending (wishboning) was significantly negatively correlated with the emergence of a protruding mentum osseum. However, Neandertals and early modern humans were equivalent in their abilities to resist this bending regime, while both groups were less resistant in wishboning than earlier archaic humans. In addition, symphyseal inclination, which decreased throughout the later Pleistocene, was highly correlated with mentum osseum rank. Although the overall pattern of differential stasis and change in vertical bending and wishboning resistance at the symphysis is consistent with aspects of the current biomechanical model of the "chin," the decoupling of bending resistance and mentum osseum form in the Late Pleistocene suggests that the evolutionary emergence of the modern human "chin" was at least partly independent of the biomechanical demands placed on the symphysis.