A Pleistocene assemblage of near-modern Papio hamadryas from the Middle Awash study area, Afar Rift, Ethiopia.

OBJECTIVES: The aim of this study is to assess a new assemblage of papionin fossils (n = 143) recovered from later Pleistocene sediments in the Middle Awash study area in the Afar Rift of Ethiopia. MATERIALS AND METHODS: We collected metric and qualitative data to compare the craniodental and postcranial anatomy of the papionin fossils with subspecies of modern Papio hamadryas and with Plio-Pleistocene African papionins. We also estimated sex and ontogenetic age. RESULTS: The new fossils fit well within the range of morphological variation observed for extant P. hamadryas, overlapping most closely in dental size and proportions with the P. h. cynocephalus individuals in our extant samples, and well within the ranges of P. h. anubis and P. h. hamadryas. The considerable overlap in craniodental anatomy with multiple subspecies precludes subspecific diagnosis. We therefore referred 143 individuals to P. hamadryas ssp. The majority of the individuals assessed for ontogenetic age fell into middle- and old-adult age categories based on the degree of dental wear. Males (26%) were better represented than females (12%) among individuals preserving the canine-premolar honing complex. DISCUSSION: These new near-modern P. hamadryas fossils provide a window into population-level variation in the later Pleistocene. Our findings echo previous suggestions from genomic studies that the papionin family tree may have included a ghost population and provide a basis for future testing of hypotheses regarding hybridization in the recent evolutionary history of this taxon.

Teeth, prenatal growth rates, and the evolution of human-like pregnancy in later Homo.

Evidence of how gestational parameters evolved is essential to understanding this fundamental stage of human life. Until now, these data seemed elusive given the skeletal bias of the fossil record. We demonstrate that dentition provides a window into the life of neonates. Teeth begin to form in utero and are intimately associated with gestational development. We measured the molar dentition for 608 catarrhine primates and collected data on prenatal growth rate (PGR) and endocranial volume (ECV) for 19 primate genera from the literature. We found that PGR and ECV are highly correlated (R2 = 0.93, P < 0.001). Additionally, we demonstrated that molar proportions are significantly correlated with PGR (P = 0.004) and log-transformed ECV (P = 0.001). From these correlations, we developed two methods for reconstructing PGR in the fossil record, one using ECV and one using molar proportions. Dental proportions reconstruct hominid ECV (R2 = 0.81, P < 0.001), a result that can be extrapolated to PGR. As teeth dominate fossil assemblages, our findings greatly expand our ability to investigate life history in the fossil record. Fossil ECVs and dental measurements from 13 hominid species both support significantly increasing PGR throughout the terminal Miocene and Plio-Pleistocene, reflecting known evolutionary changes. Together with pelvic and endocranial morphology, reconstructed PGRs indicate the need for increasing maternal energetics during pregnancy over the last 6 million years, reaching a human-like PGR (i.e., more similar to humans than to other extant apes) and ECV in later Homo less than 1 million years ago.

Keeping 21st Century Paleontology Grounded: Quantitative Genetic Analyses and Ancestral State Reconstruction Re-Emphasize the Essentiality of Fossils.

Advances in genetics and developmental biology are revealing the relationship between genotype and dental phenotype (G:P), providing new approaches for how paleontologists assess dental variation in the fossil record. Our aim was to understand how the method of trait definition influences the ability to reconstruct phylogenetic relationships and evolutionary history in the Cercopithecidae, the Linnaean Family of monkeys currently living in Africa and Asia. We compared the two-dimensional assessment of molar size (calculated as the mesiodistal length of the crown multiplied by the buccolingual breadth) to a trait that reflects developmental influences on molar development (the inhibitory cascade, IC) and two traits that reflect the genetic architecture of postcanine tooth size variation (defined through quantitative genetic analyses: MMC and PMM). All traits were significantly influenced by the additive effects of genes and had similarly high heritability estimates. The proportion of covariate effects was greater for two-dimensional size compared to the G:P-defined traits. IC and MMC both showed evidence of selection, suggesting that they result from the same genetic architecture. When compared to the fossil record, Ancestral State Reconstruction using extant taxa consistently underestimated MMC and PMM values, highlighting the necessity of fossil data for understanding evolutionary patterns in these traits. Given that G:P-defined dental traits may provide insight to biological mechanisms that reach far beyond the dentition, this new approach to fossil morphology has the potential to open an entirely new window onto extinct paleobiologies. Without the fossil record, we would not be able to grasp the full range of variation in those biological mechanisms that have existed throughout evolution.

Body proportions according to stature groups in elite athletes.

The aim of this study was to investigate whether body proportions change as stature increases in elite Spanish athletes. The sample includes a total of 2,030 participants, comprised of 1,357 adult males, and 673 adult females. The male athletes were classified into five groups by stature, and the female athletes were classified separately into four stature groups. Ten anthropometric measurements were collected, and eleven body proportions were calculated. The body proportions with significant differences between stature groups in males were relative arm length (0.53-1.60%), relative forearm length (0.69-2.08%), relative thigh length (1.17-1.56%), relative tibial length (1.37-6.39%), cormic index (-0.94 - -4.49%), Manouvrier index (1.60-9.60%), and crural index (1.05-4.79%). In females, the body proportions with significant differences were relative forearm length (1.43%), relative thigh length (1.94-3.88%), relative tibial length (2.74-4.56%), cormic index (-0.74 - -3.72%), and Manouvrier index (1.97-8.71%). The distal parts of the upper and lower limbs increase proportionally as stature increases, whereas relative hand and foot lengths, which are the most distal parts of the extremities, remain constant in elite athletes.

Neutral evolution of human enamel-dentine junction morphology.

Teeth have been studied for decades and continue to reveal information relevant to human evolution. Studies have shown that many traits of the outer enamel surface evolve neutrally and can be used to infer human population structure. However, many of these traits are unavailable in archaeological and fossil individuals due to processes of wear and taphonomy. Enamel-dentine junction (EDJ) morphology, the shape of the junction between the enamel and the dentine within a tooth, captures important information about tooth development and vertebrate evolution and is informative because it is subject to less wear and thus preserves more anatomy in worn or damaged specimens, particularly in mammals with relatively thick enamel like hominids. This study looks at the molar EDJ across a large sample of human populations. We assessed EDJ morphological variation in a sample of late Holocene modern humans (n = 161) from archaeological populations using µ-CT biomedical imaging and geometric morphometric analyses. Global variation in human EDJ morphology was compared to the statistical expectations of neutral evolution and "Out of Africa" dispersal modeling of trait evolution. Significant correlations between phenetic variation and neutral genetic variation indicate that EDJ morphology has evolved neutrally in humans. While EDJ morphology reflects population history, its global distribution does not follow expectations of the Out of Africa dispersal model. This study increases our knowledge of human dental variation and contributes to our understanding of dental development more broadly, with important applications to the investigation of population history and human genetic structure.

A genotype:phenotype approach to testing taxonomic hypotheses in hominids.

Paleontology has long relied on assumptions about the genetic and developmental influences on skeletal variation. The last few decades of developmental genetics have elucidated the genetic pathways involved in making teeth and patterning the dentition. Quantitative genetic analyses have refined this genotype:phenotype map even more, especially for primates. We now have the ability to define dental traits with a fair degree of fidelity to the underlying genetic architecture; for example, the molar module component (MMC) and the premolar-molar module (PMM) that have been defined through quantitative genetic analyses. We leverage an extensive dataset of extant and extinct hominoid dental variation to explore how these two genetically patterned phenotypes have evolved through time. We assess MMC and PMM to test the hypothesis that these two traits reveal a more biologically informed taxonomy at the genus and species levels than do more traditional measurements. Our results indicate that MMC values for hominids fall into two categories and that Homo is derived compared with earlier taxa. We find a more variable, species-level pattern for PMM. These results, in combination with previous research, demonstrate that MMC reflects the phenotypic output of a more evolutionarily stable, or phylogenetically congruent, genetic mechanism, and PMM is a reflection of a more evolutionarily labile mechanism. These results suggest that the human lineage since the split with chimpanzees may not represent as much genus-level variation as has been inferred from traits whose etiologies are not understood.

Piecewise regression equations for estimating stature: an anthropometric study in Spanish females.

In forensic anthropology, generic equations are generally preferred for estimation of stature. However, recent studies have demonstrated that regression equations specific to stature groups yield more accurate predictions. Almost all previous studies have been conducted on male subjects, and it is not currently known how well such equations work for females. Therefore, this study aims to test whether regression equations specific to stature groups work for females as well. To this end, a cross-sectional study was conducted to estimate stature on a sample of 351 Spanish adult females. The participants were randomized into a calibration group (n = 185) and a validation group (n = 166). Equations for stature estimation based on tibial length were developed in the calibration group, which was categorized according to stature (short, medium, and tall) using the 15th and 85th percentiles as cut-off points. The standard errors of the estimations (SEEs) for the group-specific regression equations (SEE = 2.35-2.66 cm) were lower than for the general formula derived for all participants of the calibration group (SEE = 3.46 cm). The specific equations resulted in smaller differences between estimated and recorded statures than the generic equation when we tested the equations with the validation group. Additionally, the SEE values of the stature-specific equations are lower compared to generic equations applied to other human populations. In conclusion, the group-specific equations from tibial length have high accuracy compared with previously derived equations for Spanish females and other populations. This procedure for estimating stature thereby improves the tools available to forensic scientists.

Patterns and magnitudes of craniofacial covariation in extant cercopithecids.

The cranium contains almost all of the vertebrate sensory organs and plays an essential role in vertebrate evolution. Research on the primate cranium has revealed that it is both highly integrated and modular, but studies have historically focused on covariance between the neurocranium and facial skeleton rather than on bones specific to special senses such as vision. The goal of this work is to investigate patterns and magnitudes of craniofacial covariation in extant cercopithecids with particular attention to the orbits. This study takes a quantitative approach using data collected from 38 homologous cranial landmarks across 11 genera of cercopithecid monkeys (Cercopithecidae, N = 291). These data demonstrate that both patterns and magnitudes of craniofacial covariation differ across Cercopithecidae at subfamily, tribe, and genus levels, with the strongest integration in the papionins (and specifically Papio) and significantly weaker covariation in the colobines, particularly Presbytis. Orbital height does not covary with other measurements of the cranium to the same degree as other cranial traits in Cercopithecidae and is highly constrained across the family. This study has important implications for our understanding of the evolution and development of morphological diversity in the cercopithecid cranium and evolution of the primate eye. This study also highlights the potential error of broad assumptions about generalizing patterns and magnitudes of modularity and integration across primates. Additionally, these findings reiterate the importance of trait selection for interpreting fossil taxonomy, as craniofacial covariation may impact phenotypes commonly used to differentiate fossil primate species.

Evidence of strong stabilizing effects on the evolution of boreoeutherian (Mammalia) dental proportions.

The dentition is an extremely important organ in mammals with variation in timing and sequence of eruption, crown morphology, and tooth size enabling a range of behavioral, dietary, and functional adaptations across the class. Within this suite of variable mammalian dental phenotypes, relative sizes of teeth reflect variation in the underlying genetic and developmental mechanisms. Two ratios of postcanine tooth lengths capture the relative size of premolars to molars (premolar-molar module, PMM), and among the three molars (molar module component, MMC), and are known to be heritable, independent of body size, and to vary significantly across primates. Here, we explore how these dental traits vary across mammals more broadly, focusing on terrestrial taxa in the clade of Boreoeutheria (Euarchontoglires and Laurasiatheria). We measured the postcanine teeth of N = 1,523 boreoeutherian mammals spanning six orders, 14 families, 36 genera, and 49 species to test hypotheses about associations between dental proportions and phylogenetic relatedness, diet, and life history in mammals. Boreoeutherian postcanine dental proportions sampled in this study carry conserved phylogenetic signal and are not associated with variation in diet. The incorporation of paleontological data provides further evidence that dental proportions may be slower to change than is dietary specialization. These results have implications for our understanding of dental variation and dietary adaptation in mammals.

Craniodental Allometry, Prenatal Growth Rates, and the Evolutionary Loss of the Third Molars in New World Monkeys.

A growing body of literature demonstrates that genetic patterning mechanisms underlie the relative proportions of the mammalian postcanine dentition with the third molar being key to understanding variation within the molar row. With this relatively recent insight, there has been renewed interest in mammalian taxa that have lost the third molars. Within platyrrhines, the marmosets and tamarins (Callitrichidae family) are characterized by small body size, claw-like nails, twinning, and reduced molar number. Small body size is hypothesized to have resulted in the third molar being crowded out of the jaws leading to its evolutionary loss in this family. To further explore this hypothesis, we measured the cranium and dentition of 142 individuals spanning all five platyrrhine families. These data reveal that callitrichids have a significantly smaller proportion of mandibular postcanine tooth row length relative to other platyrrhines, refuting the "crowding out" hypothesis. However, postcanine tooth row length is significantly correlated with mandibular length and cranial length (P < 0.01) across all platyrrhines providing evidence for a strong allometric association between postcanine tooth row length and body size more generally. The small body size that characterizes callitrichids results in part from slower prenatal growth rates. Given the allometric relationship between postcanine tooth row length and body size, reported here and in previous studies, we hypothesize that the evolutionary loss of the third molars in callitrichids results from the inhibition of third molar development as a consequence of the slower prenatal growth rates associated with small body size in this family. Anat Rec, 302:1419-1433, 2019. © 2018 Wiley Periodicals, Inc.

Breaking the rules: Phylogeny, not life history, explains dental eruption sequence in primates.

OBJECTIVES: Although a great deal is known about the biology of tooth development and eruption, there remains disagreement about the factors driving the evolution of dental eruption sequence. We assessed postcanine eruption sequence across a large sample of primates to test two hypotheses: (1) Dental eruption sequence is significantly correlated with life history and body size variables that capture postnatal growth and longevity (Schultz's Rule), and (2) Dental eruption sequence is conserved phylogenetically. MATERIALS AND METHODS: We assessed postcanine dental eruption sequence for 194 individuals representing 21 primate genera spanning eight families. With the inclusion of an additional 29 primate genera from the literature, this is the most comprehensive report on dental eruption sequence in primates to date. We used a series of phylogenetic analyses to statistically compare dental eruption sequence to life history and body size and test for phylogenetic signal in these traits. RESULTS: Dental eruption sequence is conserved phylogenetically in primates, and body and brain size are both significantly associated with dental eruption sequence. Ancestral state reconstruction supports the hypothesis that the third molar erupted before one or more of the premolars in the ancestor of primates and derived clades within primates evolved an eruption sequence in which the third molar erupts after the premolars. DISCUSSION: Schultz's Rule, as it is currently written and applied, is not supported by this extended data set. Our results demonstrate that dental eruption sequence is a far better predictor of phylogeny and will likely prove useful in phylogenetic hypotheses about relationships between extinct and extant mammalian taxa. The evolution of dental eruption sequence is likely driven by factors that significantly influence body size and mandibular symphyseal fusion.

Environmental selection during the last ice age on the mother-to-infant transmission of vitamin D and fatty acids through breast milk.

Because of the ubiquitous adaptability of our material culture, some human populations have occupied extreme environments that intensified selection on existing genomic variation. By 32,000 years ago, people were living in Arctic Beringia, and during the Last Glacial Maximum (LGM; 28,000-18,000 y ago), they likely persisted in the Beringian refugium. Such high latitudes provide only very low levels of UV radiation, and can thereby lead to dangerously low levels of biosynthesized vitamin D. The physiological effects of vitamin D deficiency range from reduced dietary absorption of calcium to a compromised immune system and modified adipose tissue function. The ectodysplasin A receptor (EDAR) gene has a range of pleiotropic effects, including sweat gland density, incisor shoveling, and mammary gland ductal branching. The frequency of the human-specific EDAR V370A allele appears to be uniquely elevated in North and East Asian and New World populations due to a bout of positive selection likely to have occurred circa 20,000 y ago. The dental pleiotropic effects of this allele suggest an even higher occurrence among indigenous people in the Western Hemisphere before European colonization. We hypothesize that selection on EDAR V370A occurred in the Beringian refugium because it increases mammary ductal branching, and thereby may amplify the transfer of critical nutrients in vitamin D-deficient conditions to infants via mothers' milk. This hypothesized selective context for EDAR V370A was likely intertwined with selection on the fatty acid desaturase (FADS) gene cluster because it is known to modulate lipid profiles transmitted to milk from a vitamin D-rich diet high in omega-3 fatty acids.

The integration of quantitative genetics, paleontology, and neontology reveals genetic underpinnings of primate dental evolution.

Developmental genetics research on mice provides a relatively sound understanding of the genes necessary and sufficient to make mammalian teeth. However, mouse dentitions are highly derived compared with human dentitions, complicating the application of these insights to human biology. We used quantitative genetic analyses of data from living nonhuman primates and extensive osteological and paleontological collections to refine our assessment of dental phenotypes so that they better represent how the underlying genetic mechanisms actually influence anatomical variation. We identify ratios that better characterize the output of two dental genetic patterning mechanisms for primate dentitions. These two newly defined phenotypes are heritable with no measurable pleiotropic effects. When we consider how these two phenotypes vary across neontological and paleontological datasets, we find that the major Middle Miocene taxonomic shift in primate diversity is characterized by a shift in these two genetic outputs. Our results build on the mouse model by combining quantitative genetics and paleontology, and thereby elucidate how genetic mechanisms likely underlie major events in primate evolution.

Identification of a derived dental trait in the papionini relative to other old world monkeys.

Variation in the shape of teeth provides an immense amount of information about the evolutionary history and adaptive strategy of a mammalian lineage. Here, we explore variation in the expression of a purported molar lingual remnant (the interconulus) across the Old World Monkeys (Primates: Cercopithecidae) with the aim of elucidating a component of the adaptive radiation of this family. This radiation is characterized by a wide geographic range (Asia and Africa) as well as diverse dietary niches. While all of the cercopithecids are distinguished by their derived bilophodont molars, the colobines have evolved taller and more pointed cusps compared with the cercopithecines. We investigate whether the interconulus also correlates with phylogenetic affinity and/or dietary adaptation. We assess the frequency and range of interconulus expression in 522 specimens representing seven species of Old World Monkeys (Cercopithecus mitis, n = 78; Macaca fascicularis, n = 85; Macaca mulatta, n = 70; Papio hamadryas, n = 55; Colobus guereza, n = 76; Presbytis melalophos, n = 82; Presbytis rubicunda, n = 76). Results show that the interconulus has a significantly higher frequency and degree of expression in Tribe Papionini and exhibits ordered metameric variation with greatest expression in the third molars. Given the rarity of the interconulus in other closely related taxa, and its morphological distinction from the purportedly homologous features in other primates, we interpret the high degree of expression of the interconulus to be a trait derived in papionins that originated in the Miocene baboon/macaque ancestor.