Human Faces Are Slower than Chimpanzee Faces

Background

While humans (like other primates) communicate with facial expressions, the evolution of speech added a new function to the facial muscles (facial expression muscles). The evolution of speech required the development of a coordinated action between visual (movement of the lips) and auditory signals in a rhythmic fashion to produce “visemes” (visual movements of the lips that correspond to specific sounds). Visemes depend upon facial muscles to regulate shape of the lips, which themselves act as speech articulators. This movement necessitates a more controlled, sustained muscle contraction than that produced during spontaneous facial expressions which occur rapidly and last only a short period of time. Recently, it was found that human tongue musculature contains a higher proportion of slow-twitch myosin fibers than in rhesus macaques, which is related to the slower, more controlled movements of the human tongue in the production of speech. Are there similar unique, evolutionary physiologic biases found in human facial musculature related to the evolution of speech?

Methodology/Prinicipal Findings

Using myosin immunohistochemistry, we tested the hypothesis that human facial musculature has a higher percentage of slow-twitch myosin fibers relative to chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). We sampled the orbicularis oris and zygomaticus major muscles from three cadavers of each species and compared proportions of fiber-types. Results confirmed our hypothesis: humans had the highest proportion of slow-twitch myosin fibers while chimpanzees had the highest proportion of fast-twitch fibers.

Conclusions/significance

These findings demonstrate that the human face is slower than that of rhesus macaques and our closest living relative, the chimpanzee. They also support the assertion that human facial musculature and speech co-evolved. Further, these results suggest a unique set of evolutionary selective pressures on human facial musculature to slow down while the function of this muscle group diverged from that of other primates.     

Asian horses deepen the MSY phylogeny

Humans have shaped the population history of the horse ever since domestication about 5500 years ago. Comparative analyses of the Y chromosome can illuminate the paternal origin of modern horse breeds. This may also reveal different breeding strategies that led to the formation of extant breeds. Recently, a horse Y‐chromosomal phylogeny of modern horses based on 1.46 Mb of the male‐specific Y (MSY) was generated. We extended this dataset with 52 samples from five European, two American and seven Asian breeds. As in the previous study, almost all modern European horses fall into a crown group, connected via a few autochthonous Northern European lineages to the outgroup, the Przewalski's Horse. In total, we now distinguish 42 MSY haplotypes determined by 158 variants within domestic horses. Asian horses show much higher diversity than previously found in European breeds. The Asian breeds also introduce a deep split to the phylogeny, preliminarily dated to 5527 ± 872 years. We conclude that the deep splitting Asian Y haplotypes are remnants of a far more diverse ancient horse population, whose haplotypes were lost in other lineages.     

Decision-Making in Przewalski Horses (Equus ferus przewalskii) is Driven by the Ecological Contexts of Collective Movements

We addressed decision-making processes in the collective movements of two groups of Przewalski horses ( Equus ferus przewalskii ) living in a semi free-ranging population. We investigated whether different patterns of group movement are related to certain ecological contexts (habitat use and group activity) and analysed the possible decision-making processes involved. We found two distinct patterns; 'single-bout' and 'multiple-bout' movements occurred in both study groups. The movements were defined by the occurrence of collective stops between bouts and differed by their duration, distance covered and ecological context. For both movements, we found that a preliminary period involving several horses occurred before departure. In single-bout movements, all group members rapidly joined the first moving horse, independently of the preliminary period. In multiple-bout movements, however, the joining process was longer; in particular when the number of decision-makers and their pre-departure behaviour before departure increased. Multiple-bout movements were more often used by horses to switch habitats and activities. This observation demonstrates that the horses need more time to resolve motivational conflicts before these departures. We conclude that decision-making in Przewalski horses is based on a shared consensus process driven by ecological determinants.     

Genetic variation in Przewalski's horses, with special focus on the last wild caught mare, 231 Orlitza III

In our continuing efforts to document genetic diversity in Przewalski's horses and relatedness with domestic horses, we report genetic variation at 22 loci of blood group and protein polymorphisms and 29 loci of DNA (microsatellite) polymorphisms. The loci have been assigned by linkage or synteny mapping to 20 autosomes and the X chromosome of the domestic horse (plus four loci unassigned to a chromosome). With cumulative data from tests of 568 Przewalski's horses using blood, hair or tooth samples, no species-defining markers were identified, however a few markers were present in the wild species but not in domestic horses. Inheritance patterns and linkage relationships reported in domestic horses appeared to be conserved in Przewalski's horses. A derived type for the last wild caught mare 231 Orlitza III provided evidence for markers apparently not found in (or not currently available by descent from) the other species founders that were captured at the end of the nineteenth century. This information has been critical to the development of parentage analyses in the studbook population of Przewalski's horses at Askania Nova, at one time the largest herd of captive animals and the source of stock for reintroduction efforts. Some horses in the study showed genetic incompatibilities with their sire or dam, contradicting published studbook information. In many cases alternative parentage could be assigned from living animals. To assist in identification of correct parentage, DNA marker types for deceased horses were established from archived materials (teeth) or derived from offspring. Genetic markers were present in pedigreed animals whose origin could not be accounted for from founders. Genetic distance analysis of erythrocyte protein, electrophoretic and microsatellite markers in Przewlaski's horses and ten breeds of domestic horse place the Przewalski's horse as an outgroup to domestic horses, introgression events from domestic horses not withstanding.     

An assessment of feral horse impacts on treeless drainage lines in the Australian Alps

The feral Horse (Equus caballus) is widespread across the Australian Alps. Feral horses degrade alpine and sub‐alpine ecosystems and damage habitat of a range of threatened species. Despite this, there is little published work to document the extent and severity of these impacts. This study investigated impacts of feral horses on treeless drainage lines at 186 sites across the Australian Alps. The study included sites in the Australian Capital Territory, New South Wales and Victoria. We assessed nine variables related to soil and stream stability and vegetation cover, which in turn influence ecosystem function and habitat quality. We found significant differences among horse‐occupied and horse‐free sites for all soil and stream stability variables assessed. For all variables assessed, the average score (and hence, condition) was worse in horse‐occupied areas. The sites in poorest condition were occupied by horses. Impacts from other mammalian herbivores species appeared to be minor. Management intervention is necessary if these impacts of feral horses are to be addressed.     

Horse domestication and conservation genetics of Przewalski's horse inferred from sex chromosomal and autosomal sequences

Despite their ability to interbreed and produce fertile offspring,there is continued disagreement about the genetic relationshipof the domestic horse (Equus caballus) to its endangered wildrelative, Przewalski's horse (Equus przewalskii). Analyses havediffered as to whether or not Przewalski's horse is placed phylogeneticallyas a separate sister group to domestic horses. Because Przewalski'shorse and domestic horse are so closely related, genetic datacan also be used to infer domestication-specific differencesbetween the two. To investigate the genetic relationship ofPrzewalski's horse to the domestic horse and to address whetherevolution of the domestic horse is driven by males or females,five homologous introns (a total of 3 kb) were sequenced onthe X and Y chromosomes in two Przewalski's horses and threebreeds of domestic horses: Arabian horse, Mongolian domestichorse, and Dartmoor pony. Five autosomal introns (a total of6 kb) were sequenced for these horses as well. The sequencesof sex chromosomal and autosomal introns were used to determinenucleotide diversity and the forces driving evolution in thesespecies. As a result, X chromosomal and autosomal data do notplace Przewalski's horses in a separate clade within phylogenetictrees for horses, suggesting a close relationship between domesticand Przewalski's horses. It was also found that there was alack of nucleotide diversity on the Y chromosome and highernucleotide diversity than expected on the X chromosome in domestichorses as compared with the Y chromosome and autosomes. Thissupports the hypothesis that very few male horses along withnumerous female horses founded the various domestic horse breeds.Patterns of nucleotide diversity among different types of chromosomeswere distinct for Przewalski's in contrast to domestic horses,supporting unique evolutionary histories of the two species.     

Autosomal genetic diversity in non‐breed horses from eastern Eurasia provides insights into historical population movements

Many events in the history of eastern Eurasia, including the process of domestication itself, the initial spread of domestic horses and subsequent movements, are believed to have affected the genetic structure of domestic horse populations in this area. We investigated levels of within‐ and between‐population genetic diversity in ‘non‐breed horses’ (working horses sampled in remote areas) from 17 locations in Asia and parts of Eastern Europe, using 26 autosomal microsatellite loci. Non‐breed horses have not been subject to the same intensity of artificial selection and closed breeding as have most breed animals and are thus expected to better reflect the population history of domestic horses. Despite geographic distances of between 300 and 7000 km between sampling locations, pairwise F _ST was very low (range: <0.001 to ?0.033), suggesting historically high levels of gene flow. Our analyses of non‐breed horses revealed a pattern of isolation by distance and a significant decline in genetic diversity (expected heterozygosity and allelic richness) from east to west, consistent with a westward expansion of horses out of East Asia. Although the timing of this putative expansion is unclear, our results highlight the benefit of studying animals that do not belong to particular breeds when investigating aspects of a population's history.     

Facial hair whorls (trichoglyphs) and the incidence of motor laterality in the horse

Several species demonstrate obvious motor laterality (sidedness, handedness) in their motor function. Motor laterality in the horse affects locomotion and subsequently equine performance during training and may have inherent safety implications for equitation. Some of the most commonly used identification features in the horse are hair whorls (trichoglyphs), since their specific location and character vary to some degree in every horse. We investigated the relationship between the hair flow of single facial hair whorls and the incidence of lateralised motor bias in 219 horses when under saddle in ridden work. The horses exhibited significant differences in motor preferences with 104 left-lateralised (LL) horses, 95 right-lateralised (RL) horses compared to only 20 well-balanced (WB) horses (chi(2)=36.9, d.f.=2, P<0.01). There was also a significant difference in the frequency distribution of single facial hair whorl patterns in the horses consisting of 114 horses with counter-clockwise (CC) whorls, 82 horses with clockwise (C) whorls and 23 horses, which had radial (R) whorls (chi(2)=38.87, d.f.=2, P<0.01). Overall there was a statistically significant association between motor behaviour and facial hair whorl patterns in the horses (chi(2)=69.4, d.f.=4, P>0.001). The RL horses had significantly more C facial hair whorls and the LL horses had significantly more CC facial hair whorls than would be expected purely by chance alone (P<0.05). The findings may provide trainers with a useful tool when attempting to identify simple, non-invasive and reliable predictors of motor laterality in the horse. Furthermore, given that efficient targeted training of performance horses during ridden work may produce WB equine athletes, the findings could assist trainers when designing individual-specific training programmes for young horses.     

家马的驯化起源与遗传演化特征

人类文明发展历史中, 家马(Equus ferus caballus)曾是推动文化交流、促进人类社会发展的主要动力。关于家马何时、何地被驯化以及在此过程中其遗传演化如何被人类影响等一直备受关注。近年来随着遗传学技术的发展, 人们对该问题有了更为深入的理解。本文回顾了近二十年来相关研究所取得的成果, 探讨了家马的驯化起源中心和驯化过程中的遗传演化特征, 并对未来的研究方向以及遗传资源保护提出了建议。分子标记遗传学和考古学研究认为家马可能来自多个驯化起源地种群, 然而最近的古DNA研究结果表明, 现代家马的驯化起源可能比之前人们所猜测的更加复杂, 古代博泰马被认为是最早被驯化的家马, 然而最近被证实并不是现代家马的直系祖先。如此复杂的驯化问题可能从多学科的层次才能解析清楚。人类社会活动直接或间接影响了家马的演化历程, 特别是工业革命以来家马的遗传基础发生了巨大变化, 其遗传多样性开始急剧衰退, 不少地方品种正逐渐走向衰落甚至灭绝。为确保农业生态安全不受威胁, 建议加强家马遗传资源保护与动物遗传学和文化地理之间的联系研究。     

Copy Number Variation in the Horse Genome

We constructed a 400K WG tiling oligoarray for the horse and applied it for the discovery of copy number variations (CNVs) in 38 normal horses of 16 diverse breeds, and the Przewalski horse. Probes on the array represented 18,763 autosomal and X-linked genes, and intergenic, sub-telomeric and chrY sequences. We identified 258 CNV regions (CNVRs) across all autosomes, chrX and chrUn, but not in chrY. CNVs comprised 1.3% of the horse genome with chr12 being most enriched. American Miniature horses had the highest and American Quarter Horses the lowest number of CNVs in relation to Thoroughbred reference. The Przewalski horse was similar to native ponies and draft breeds. The majority of CNVRs involved genes, while 20% were located in intergenic regions. Similar to previous studies in horses and other mammals, molecular functions of CNV-associated genes were predominantly in sensory perception, immunity and reproduction. The findings were integrated with previous studies to generate a composite genome-wide dataset of 1476 CNVRs. Of these, 301 CNVRs were shared between studies, while 1174 were novel and require further validation. Integrated data revealed that to date, 41 out of over 400 breeds of the domestic horse have been analyzed for CNVs, of which 11 new breeds were added in this study. Finally, the composite CNV dataset was applied in a pilot study for the discovery of CNVs in 6 horses with XY disorders of sexual development. A homozygous deletion involving AKR1C gene cluster in chr29 in two affected horses was considered possibly causative because of the known role of AKR1C genes in testicular androgen synthesis and sexual development. While the findings improve and integrate the knowledge of CNVs in horses, they also show that for effective discovery of variants of biomedical importance, more breeds and individuals need to be analyzed using comparable methodological approaches.     

Multiple maternal origins of native modern and ancient horse populations in China

To obtain more knowledge of the origin and genetic diversity of domestic horses in China, this study provides a comprehensive analysis of mitochondrial DNA (mtDNA) D-loop sequence diversity from nine horse breeds in China in conjunction with ancient DNA data and evidence from archaeological and historical records. A 247-bp mitochondrial D-loop sequence from 182 modern samples revealed a total of 70 haplotypes with a high level of genetic diversity. Seven major mtDNA haplogroups (A–G) and 16 clusters were identified for the 182 Chinese modern horses. In the present study, nine 247-bp mitochondrial D-loop sequences of ancient remains of Bronze Age horse from the Chifeng region of Inner Mongolia in China ( c. 4000–2000a bp ) were used to explore the origin and diversity of Chinese modern horses and the phylogenetic relationship between ancient and modern horses. The nine ancient horses carried seven haplotypes with rich genetic diversity, which were clustered together with modern individuals among haplogroups A, E and F. Modern domestic horse and ancient horse data support the multiple origins of domestic horses in China. This study supports the argument that multiple successful events of horse domestication, including separate introductions of wild mares into the domestic herds, may have occurred in antiquity, and that China cannot be excluded from these events. Indeed, the association of Far Eastern mtDNA types to haplogroup F was highly significant using Fisher's exact test of independence ( P  = 0.00002), lending support for Chinese domestication of this haplogroup. High diversity and all seven mtDNA haplogroups (A–G) with 16 clusters also suggest that further work is necessary to shed more light on horse domestication in China.     

Predictors of biting fly harassment and its impact on habitat use by feral horses (Equus caballus) on a barrier island

Feral horses on Assateague Island, Maryland, were observed in June and August 2000 to determine what behavioral and ecological factors affect the intensity of biting fly harassment and whether habitat use by horses was influenced by biting flies. Fly counts and frequencies of comfort movements (i.e., movements designed to dislodge insects) were recorded during focal animal samples, as well as data on sex, group size, habitat type, temperature, humidity, wind speed, and behavior. Seasonal habitat use patterns were assessed using 7 years of monthly census data on the horses. The number of biting flies on the horse was affected by horse sex, habitat, temperature, and group size. The number of comfort movements a horse showed was affected by habitat, temperature, wind speed, group size, and number of horses within one body length of the focal. The number of comfort movements made by a horse was found to be highly correlated with fly numbers. Though marshes were used most throughout the year, the pattern of use of dune, scrub, and human-altered habitats reflects a pattern of biting fly avoidance and refuge-seeking by the horses.     

Do Facial Expressions Develop before Birth?

Background

Fetal facial development is essential not only for postnatal bonding between parents and child, but also theoretically for the study of the origins of affect. However, how such movements become coordinated is poorly understood. 4-D ultrasound visualisation allows an objective coding of fetal facial movements.

Methodology/Findings

Based on research using facial muscle movements to code recognisable facial expressions in adults and adapted for infants, we defined two distinct fetal facial movements, namely “cry-face-gestalt” and “laughter- gestalt,” both made up of up to 7 distinct facial movements. In this conceptual study, two healthy fetuses were then scanned at different gestational ages in the second and third trimester. We observed that the number and complexity of simultaneous movements increased with gestational age. Thus, between 24 and 35 weeks the mean number of co-occurrences of 3 or more facial movements increased from 7% to 69%. Recognisable facial expressions were also observed to develop. Between 24 and 35 weeks the number of co-occurrences of 3 or more movements making up a “cry-face gestalt” facial movement increased from 0% to 42%. Similarly the number of co-occurrences of 3 or more facial movements combining to a “laughter-face gestalt” increased from 0% to 35%. These changes over age were all highly significant.

Significance

This research provides the first evidence of developmental progression from individual unrelated facial movements toward fetal facial gestalts. We propose that there is considerable potential of this method for assessing fetal development: Subsequent discrimination of normal and abnormal fetal facial development might identify health problems in utero.     

Functional recovery following manipulation of muscles and sense organs in the stick insect leg

We studied functional recovery of leg posture and walking behaviour in the femur-tibia joint control system of stick insects. Leg extensions in resting animals and during walking are produced by different parts of a single extensor muscle. (a) Ablation of the muscle part responsible for fast movements prevented leg extension during the swing phase. Resting posture remained unaffected. Within a few post-operative days, extension movements recovered, provided that sensory feedback was available. Extension movements were now driven by the muscle part which in intact animals controls the resting posture only. (b) Selective ablation of this (slow) muscle part affected the resting posture, while walking was unaffected. The resting posture partly recovered during subsequent days. To test the range of functional recovery and underlying mechanisms, we additionally transected muscle motor innervation, or we inverted or ablated sensory feedback. We found that recovery was based on both muscular and neuronal mechanisms. The latter required appropriate sensory feedback for the process of recovery, but not for the maintenance of the recovered state. Our results thus indicate the existence of a sensory template that guides recovery. Recovery was limited to a behavioural range that occurs naturally in intact animals, though in different behavioural contexts.     

Electromyographic activity of mystacial pad musculature during whisking behavior in the rat

Cinematographic measurements of whisker movements generated by behaving rats were compared with electromyographic (EMG) activity recorded simultaneously from mystacial pad musculature. Muscle activity consisted of repetitive bursts, each of which initiated a "whisking" cycle consisting of a protraction followed by a retraction. Protraction amplitude and velocity were directly proportional to the amount of EMG activity during forward whisker movement. Overtime, the intensity of muscle discharge determined the set point about which the vibrissae moved; higher levels of muscle activity resulted in a greater degree of overall whisker protraction. These findings are consistent with the known anatomy of the facial musculature and underscore the importance of whisker protraction in the acquisition of tactile information by the vibrissae.     

Population genetics of Great Basin feral horses

The genetic make-up of Great Basin wild (feral) horses was investigated by blood typing studies. Blood samples of 975 feral horses from seven trap sites in Nevada and Oregon were tested by serological and electrophoretic techniques for genetic markers at 19 polymorphic loci. The average number of variants for the seven feral populations [72·1 ± 3·2 (SEM), range 62–85] was not significantly different from that of 16 domestic breeds (75·0 ± 11·5, range 58–105). The expected average frequency of heterozygotes per locus (average heterozygosity) for the feral populations (0·402 ± 0·009, range 0·368–0·442) was not significantly different from the domestic breeds (0·389 ± 0·045, range 0·295–0·443). Dendrograms constructed using pairwise comparisons of Nei's distance measurements substantiated anecdotal accounts of the origins of Great Basin horses from Iberian, American saddle horse and draft horse breeds.     

Social Use of Facial Expressions in Hylobatids

Non-human primates use various communicative means in interactions with others. While primate gestures are commonly considered to be intentionally and flexibly used signals, facial expressions are often referred to as inflexible, automatic expressions of affective internal states. To explore whether and how non-human primates use facial expressions in specific communicative interactions, we studied five species of small apes (gibbons) by employing a newly established Facial Action Coding System for hylobatid species (GibbonFACS). We found that, despite individuals often being in close proximity to each other, in social (as opposed to non-social contexts) the duration of facial expressions was significantly longer when gibbons were facing another individual compared to non-facing situations. Social contexts included grooming, agonistic interactions and play, whereas non-social contexts included resting and self-grooming. Additionally, gibbons used facial expressions while facing another individual more often in social contexts than non-social contexts where facial expressions were produced regardless of the attentional state of the partner. Also, facial expressions were more likely ‘responded to’ by the partner’s facial expressions when facing another individual than non-facing. Taken together, our results indicate that gibbons use their facial expressions differentially depending on the social context and are able to use them in a directed way in communicative interactions with other conspecifics.     

Multifactorial inheritance of common white markings in the Arabian horse

The results of a previous study were compatible with the hypothesis that common white facial markings in the Arabian horse have a multifactorial mode of inheritance. I expanded that study to (1) include the legs and therefore obtain insight into the heritability of common white markings in all peripheral regions (face and legs) of the Arabian horse and (2) investigate the influence of sex and the genotypes that produce the bay and chestnut phenotypes on the variation in common white markings. Both studies were based on computerized data obtained from the Arabian Horse Registry of America, Inc. Each leg of a horse was scored from 0 to 5 depending on the amount of whiteness present, and the four leg scores were added to obtain the total leg score for each horse. The facial region was divided into five areas, and each horse was given a score from 0 to 5 according to the number of areas with whiteness. Sire families were analyzed in which each sire family consisted of a sire, his foals, and the dams of those foals. There was a correlation between white facial scores and white leg scores, suggesting that both types of white markings are influenced by the same genetic mechanism. Sire-foal and dam-foal regression analyses were compatible with the hypothesis that common white leg markings also show multifactorial inheritance. Although the results support the model that additively acting genes (polygenes) influence the presence and extent of common white markings, the results also show that males are slightly more marked than are females and that chestnut horses are more heavily marked than are bay horses.(ABSTRACT TRUNCATED AT 250 WORDS)