Browsing by Author "Boyer, Doug M"

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    A digital collection of rare and endangered lemurs and other primates from the Duke Lemur Center.
    (PloS one, 2019-01) Yapuncich, Gabriel S; Kemp, Addison D; Griffith, Darbi M; Gladman, Justin T; Ehmke, Erin; Boyer, Doug M
    Scientific study of lemurs, a group of primates found only on Madagascar, is crucial for understanding primate evolution. Unfortunately, lemurs are among the most endangered animals in the world, so there is a strong impetus to maximize as much scientific data as possible from available physical specimens. MicroCT scanning efforts at Duke University have resulted in scans of more than 100 strepsirrhine cadavers representing 18 species from the Duke Lemur Center. An error study of the microCT scanner recovered less than 0.3% error at multiple resolution levels. Scans include specimen overviews and focused, high-resolution selections of complex anatomical regions (e.g., cranium, hands, feet). Scans have been uploaded to MorphoSource, an online digital repository for 3D data. As captive (but free ranging) individuals, these specimens have a wealth of associated information that is largely unavailable for wild populations, including detailed life history data. This digital collection maximizes the information obtained from rare and endangered animals with minimal degradation of the original specimens.
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    A new fully automated approach for aligning and comparing shapes.
    (Anatomical record (Hoboken, N.J. : 2007), 2015-01) Boyer, Doug M; Puente, Jesus; Gladman, Justin T; Glynn, Chris; Mukherjee, Sayan; Yapuncich, Gabriel S; Daubechies, Ingrid
    Three-dimensional geometric morphometric (3DGM) methods for placing landmarks on digitized bones have become increasingly sophisticated in the last 20 years, including greater degrees of automation. One aspect shared by all 3DGM methods is that the researcher must designate initial landmarks. Thus, researcher interpretations of homology and correspondence are required for and influence representations of shape. We present an algorithm allowing fully automatic placement of correspondence points on samples of 3D digital models representing bones of different individuals/species, which can then be input into standard 3DGM software and analyzed with dimension reduction techniques. We test this algorithm against several samples, primarily a dataset of 106 primate calcanei represented by 1,024 correspondence points per bone. Results of our automated analysis of these samples are compared to a published study using a traditional 3DGM approach with 27 landmarks on each bone. Data were analyzed with morphologika(2.5) and PAST. Our analyses returned strong correlations between principal component scores, similar variance partitioning among components, and similarities between the shape spaces generated by the automatic and traditional methods. While cluster analyses of both automatically generated and traditional datasets produced broadly similar patterns, there were also differences. Overall these results suggest to us that automatic quantifications can lead to shape spaces that are as meaningful as those based on observer landmarks, thereby presenting potential to save time in data collection, increase completeness of morphological quantification, eliminate observer error, and allow comparisons of shape diversity between different types of bones. We provide an R package for implementing this analysis.
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    Development and Assessment of Fully Automated and Globally Transitive Geometric Morphometric Methods, With Application to a Biological Comparative Dataset With High Interspecific Variation.
    (Anatomical record (Hoboken, N.J. : 2007), 2018-04) Gao, Tingran; Yapuncich, Gabriel S; Daubechies, Ingrid; Mukherjee, Sayan; Boyer, Doug M
    Automated geometric morphometric methods are promising tools for shape analysis in comparative biology, improving researchers' abilities to quantify variation extensively (by permitting more specimens to be analyzed) and intensively (by characterizing shapes with greater fidelity). Although use of these methods has increased, published automated methods have some notable limitations: pairwise correspondences are frequently inaccurate and pairwise mappings are not globally consistent (i.e., they lack transitivity across the full sample). Here, we reassess the accuracy of published automated methods-cPDist (Boyer et al. Proc Nat Acad Sci 108 () 18221-18226) and auto3Dgm (Boyer et al.: Anat Rec 298 () 249-276)-and evaluate several modifications to these methods. We show that a substantial percentage of alignments and pairwise maps between specimens of dissimilar geometries were inaccurate in the study of Boyer et al. (Proc Nat Acad Sci 108 () 18221-18226), despite a taxonomically partitioned variance structure of continuous Procrustes distances. We show these inaccuracies are remedied using a globally informed methodology within a collection of shapes, rather than relying on pairwise comparisons (c.f. Boyer et al.: Anat Rec 298 () 249-276). Unfortunately, while global information generally enhances maps between dissimilar objects, it can degrade the quality of correspondences between similar objects due to the accumulation of numerical error. We explore a number of approaches to mitigate this degradation, quantify their performance, and compare the generated pairwise maps (and the shape space characterized by these maps) to a "ground truth" obtained from landmarks manually collected by geometric morphometricians. Novel methods both improve the quality of the pairwise correspondences relative to cPDist and achieve a taxonomic distinctiveness comparable to auto3Dgm. Anat Rec, 301:636-658, 2018. © 2017 Wiley Periodicals, Inc.
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    Evolution of postural diversity in primates as reflected by the size and shape of the medial tibial facet of the talus.
    (American journal of physical anthropology, 2015-05) Boyer, Doug M; Yapuncich, Gabriel S; Butler, Jared E; Dunn, Rachel H; Seiffert, Erik R
    Comprehensive quantification of the shape and proportions of the medial tibial facet (MTF) of the talus (=astragalus) has been lacking for Primates and their closest relatives. In this study, aspects of MTF form were quantified and employed to test hypotheses about their functional and phylogenetic significance. The following hypotheses influence perceptions of primate evolutionary history but are due for more rigorous assessment: 1) A relatively large MTF distinguishes "prosimians" (strepsirrhines and tarsiers) from anthropoids and non-primate euarchontans; 2) the distinctive form of the "prosimian" MTF is a correlate of locomotor tendencies that emphasize use of vertical and small diameter supports in conjunction with inverted, abducted foot postures; and 3) the "prosimian" MTF form arose along the primate stem lineage and was present in the euprimate common ancestor.Three-dimensional (3D) scanning was used to create scale digital models of tali (n = 378 specimens, 122 species) from which three types of variables capturing aspects of MTF form were computed: 1) MTF area relative to body mass and ectal facet area; 2) MTF shape (elliptical vs. non-elliptical); and 3) MTF dorsal restriction on the talar body (i.e., extensive vs. minimal exposure of non-articular area). Data were analyzed using both phylogenetic and traditional comparative methods including Phylogenetic Generalized Least Squares, Ordinary Least Squares, ANCOVA, ANOVA, and Bayesian Ancestral State Reconstruction (ASR).Extant "prosimians" are generally distinct from anthropoids and non-primate euarchontans in our quantitative representations of MTF form. MTF area (but not shape or dorsal restriction) correlates with fibular facet angle (FFa) of the talus, which has also been argued to reflect habitual pedal inversion. Among strepsirrhines, taxa that engage in grasp-leaping more frequently/effectively appear to have a relatively larger MTF than less acrobatic taxa. Directional models of evolutionary change better describe the phylogenetic distribution of MTF variation than do other models. ASR shows 1) little change in the MTF along the primate stem, 2) independent evolution of relatively large and dorsoplantarly deep MTFs in basal haplorhines and strepsirrhines, and 3) re-evolution of morphologies similar to non-euprimates in anthropoids.Results support the hypothesis that differences in MTF form between anthropoids and "prosimians" reflect greater use of inverted foot postures and grasp-leaping in the latter group. Although fossil "prosimians" do not have the extreme MTF dimensions that characterize many extant acrobatic leapers, these variables by themselves provide little additional behavioral resolution at the level of individual fossils due to strong phylogenetic signal. ASR suggests that some specialization for use of inverted foot postures (as required in a fine-branch niche) and modifications for grasp-leaping evolved independently in basal strepsirrhine and haplorhine lineages.
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    First virtual endocasts of adapiform primates.
    (Journal of human evolution, 2016-10) Harrington, Arianna R; Silcox, Mary T; Yapuncich, Gabriel S; Boyer, Doug M; Bloch, Jonathan I
    Well-preserved crania of notharctine adapiforms from the Eocene of North America provide the best direct evidence available for inferring neuroanatomy and encephalization in early euprimates (crown primates). Virtual endocasts of the notharctines Notharctus tenebrosus (n = 3) and Smilodectes gracilis (n = 4) from the middle Eocene Bridger formation of Wyoming, and the late Eocene European adapid adapiform Adapis parisiensis (n = 1), were reconstructed from high-resolution X-ray computed tomography (CT) data. While the three species share many neuroanatomical similarities differentiating them from plesiadapiforms (stem primates) and extant euprimates, our sample of N. tenebrosus displays more variation than that of S. gracilis, possibly related to differences in the patterns of cranial sexual dimorphism or within-lineage evolution. Body masses predicted from associated teeth suggest that N. tenebrosus was larger and had a lower encephalization quotient (EQ) than S. gracilis, despite their close relationship and similar inferred ecologies. Meanwhile, body masses predicted from cranial length of the same specimens suggest that the two species were more similar, with overlapping body mass and EQ, although S. gracilis exhibits a range of EQs shifted upwards relative to that of N. tenebrosus. While associated data from other parts of the skeleton are mostly lacking for specimens included in this study, measurements for unassociated postcrania attributed to these species yield body mass and EQ estimates that are also more similar to each other than those based on teeth. Regardless of the body mass prediction method used, results suggest that the average EQ of adapiforms was similar to that of plesiadapiforms, only overlapped the lower quadrant for the range of extant strepsirrhines, and did not overlap with the range of extant haplorhines. However, structural changes evident in these endocasts suggest that early euprimates relied more on vision than olfaction relative to plesiadapiforms, despite having relatively small endocranial volumes compared to extant taxa.
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    Hands of early primates.
    (American journal of physical anthropology, 2013-12) Boyer, Doug M; Yapuncich, Gabriel S; Chester, Stephen GB; Bloch, Jonathan I; Godinot, Marc
    Questions surrounding the origin and early evolution of primates continue to be the subject of debate. Though anatomy of the skull and inferred dietary shifts are often the focus, detailed studies of postcrania and inferred locomotor capabilities can also provide crucial data that advance understanding of transitions in early primate evolution. In particular, the hand skeleton includes characteristics thought to reflect foraging, locomotion, and posture. Here we review what is known about the early evolution of primate hands from a comparative perspective that incorporates data from the fossil record. Additionally, we provide new comparative data and documentation of skeletal morphology for Paleogene plesiadapiforms, notharctines, cercamoniines, adapines, and omomyiforms. Finally, we discuss implications of these data for understanding locomotor transitions during the origin and early evolutionary history of primates. Known plesiadapiform species cannot be differentiated from extant primates based on either intrinsic hand proportions or hand-to-body size proportions. Nonetheless, the presence of claws and a different metacarpophalangeal [corrected] joint form in plesiadapiforms indicate different grasping mechanics. Notharctines and cercamoniines have intrinsic hand proportions with extremely elongated proximal phalanges and digit rays relative to metacarpals, resembling tarsiers and galagos. But their hand-to-body size proportions are typical of many extant primates (unlike those of tarsiers, and possibly Teilhardina, which have extremely large hands). Non-adapine adapiforms and omomyids exhibit additional carpal features suggesting more limited dorsiflexion, greater ulnar deviation, and a more habitually divergent pollex than observed plesiadapiforms. Together, features differentiating adapiforms and omomyiforms from plesiadapiforms indicate increased reliance on vertical prehensile-clinging and grasp-leaping, possibly in combination with predatory behaviors in ancestral euprimates.
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    Internal carotid arterial canal size and scaling in Euarchonta: Re-assessing implications for arterial patency and phylogenetic relationships in early fossil primates.
    (J Hum Evol, 2016-08) Boyer, Doug M; Kirk, E Christopher; Silcox, Mary T; Gunnell, Gregg F; Gilbert, Christopher C; Yapuncich, Gabriel S; Allen, Kari L; Welch, Emma; Bloch, Jonathan I; Gonzales, Lauren A; Kay, Richard F; Seiffert, Erik R
    Primate species typically differ from other mammals in having bony canals that enclose the branches of the internal carotid artery (ICA) as they pass through the middle ear. The presence and relative size of these canals varies among major primate clades. As a result, differences in the anatomy of the canals for the promontorial and stapedial branches of the ICA have been cited as evidence of either haplorhine or strepsirrhine affinities among otherwise enigmatic early fossil euprimates. Here we use micro X-ray computed tomography to compile the largest quantitative dataset on ICA canal sizes. The data suggest greater variation of the ICA canals within some groups than has been previously appreciated. For example, Lepilemur and Avahi differ from most other lemuriforms in having a larger promontorial canal than stapedial canal. Furthermore, various lemurids are intraspecifically variable in relative canal size, with the promontorial canal being larger than the stapedial canal in some individuals but not others. In species where the promontorial artery supplies the brain with blood, the size of the promontorial canal is significantly correlated with endocranial volume (ECV). Among species with alternate routes of encephalic blood supply, the promontorial canal is highly reduced relative to ECV, and correlated with both ECV and cranium size. Ancestral state reconstructions incorporating data from fossils suggest that the last common ancestor of living primates had promontorial and stapedial canals that were similar to each other in size and large relative to ECV. We conclude that the plesiomorphic condition for crown primates is to have a patent promontorial artery supplying the brain and a patent stapedial artery for various non-encephalic structures. This inferred ancestral condition is exhibited by treeshrews and most early fossil euprimates, while extant primates exhibit reduction in one canal or another. The only early fossils deviating from this plesiomorphic condition are Adapis parisiensis with a reduced promontorial canal, and Rooneyia and Mahgarita with reduced stapedial canals.
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    Interspecific scaling patterns of talar articular surfaces within primates and their closest living relatives.
    (Journal of anatomy, 2014-02) Yapuncich, Gabriel S; Boyer, Doug M
    The articular facets of interosseous joints must transmit forces while maintaining relatively low stresses. To prevent overloading, joints that transmit higher forces should therefore have larger facet areas. The relative contributions of body mass and muscle-induced forces to joint stress are unclear, but generate opposing hypotheses. If mass-induced forces dominate, facet area should scale with positive allometry to body mass. Alternatively, muscle-induced forces should cause facets to scale isometrically with body mass. Within primates, both scaling patterns have been reported for articular surfaces of the femoral and humeral heads, but more distal elements are less well studied. Additionally, examination of complex articular surfaces has largely been limited to linear measurements, so that 'true area' remains poorly assessed. To re-assess these scaling relationships, we examine the relationship between body size and articular surface areas of the talus. Area measurements were taken from microCT scan-generated surfaces of all talar facets from a comprehensive sample of extant euarchontan taxa (primates, treeshrews, and colugos). Log-transformed data were regressed on literature-derived log-body mass using reduced major axis and phylogenetic least squares regressions. We examine the scaling patterns of muscle mass and physiological cross-sectional area (PCSA) to body mass, as these relationships may complicate each model. Finally, we examine the scaling pattern of hindlimb muscle PCSA to talar articular surface area, a direct test of the effect of mass-induced forces on joint surfaces. Among most groups, there is an overall trend toward positive allometry for articular surfaces. The ectal (= posterior calcaneal) facet scales with positive allometry among all groups except 'sundatherians', strepsirrhines, galagids, and lorisids. The medial tibial facet scales isometrically among all groups except lemuroids. Scaling coefficients are not correlated with sample size, clade inclusivity or behavioral diversity of the sample. Muscle mass scales with slight positive allometry to body mass, and PCSA scales at isometry to body mass. PCSA generally scales with negative allometry to articular surface area, which indicates joint surfaces increase faster than muscles' ability to generate force. We suggest a synthetic model to explain the complex patterns observed for talar articular surface area scaling: whether 'muscles or mass' drive articular facet scaling is probably dependent on the body size range of the sample and the biological role of the facet. The relationship between 'muscle vs. mass' dominance is likely bone- and facet-specific, meaning that some facets should respond primarily to stresses induced by larger body mass, whereas others primarily reflect muscle forces.
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    Predicting euarchontan body mass: A comparison of tarsal and dental variables.
    (American journal of physical anthropology, 2015-07) Yapuncich, Gabriel S; Gladman, Justin T; Boyer, Doug M
    Multiple meaningful ecological characterizations of a species revolve around body mass. Because body mass cannot be directly measured in extinct taxa, reliable body mass predictors are needed. Many published body mass prediction equations rely on dental dimensions, but certain skeletal dimensions may have a more direct and consistent relationship with body mass. We seek to evaluate the reliability of prediction equations for inferring euarchontan body mass based on measurements of the articular facet areas of the astragalus and calcaneus.Surface areas of five astragalar facets (n = 217 specimens) and two calcaneal facets (n = 163) were measured. Separate ordinary least squares and multiple regression equations are presented for different levels of taxonomic inclusivity, and the reliability of each equation is evaluated with the coefficient of determination, standard error of the estimate, mean prediction error, and the prediction sum of squares statistic. We compare prediction errors to published prediction equations that utilize dental and/or tarsal measures. Finally, we examine the effects of taxonomically specific regressions and apply our equations to a diverse set of non-primates.Our results reveal that predictions based on facet areas are more reliable than most linear dental or tarsal predictors. Multivariate approaches are often better than univariate methods, but require more information (making them less useful for fragmentary fossils). While some taxonomically specific regressions improve predictive ability, this is not true for all primate groups.Among individual facets, the ectal and fibular facets of the astragalus and the calcaneal cuboid facet are the best body mass predictors. Since these facets have primarily concave curvature and scale with positive allometry relative to body mass, it appears that candidate skeletal proxies for body mass can be identified based on their curvature and scaling coefficients.
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    Quantification of the position and depth of the flexor hallucis longus groove in euarchontans, with implications for the evolution of primate positional behavior.
    (American journal of physical anthropology, 2017-06) Yapuncich, Gabriel S; Seiffert, Erik R; Boyer, Doug M
    On the talus, the position and depth of the groove for the flexor hallucis longus tendon have been used to infer phylogenetic affinities and positional behaviors of fossil primates. This study quantifies aspects of the flexor hallucis longus groove (FHLG) to test if: (1) a lateral FHLG is a derived strepsirrhine feature, (2) a lateral FHLG reflects inverted and abducted foot postures, and (3) a deeper FHLG indicates a larger muscle.We used linear measurements of microCT-generated models from a sample of euarchontans (n = 378 specimens, 125 species) to quantify FHLG position and depth. Data are analyzed with ANOVA, Ordinary and Phylogenetic Generalized Least Squares, and Bayesian Ancestral State Reconstruction (ASR).Extant strepsirrhines, adapiforms, plesiadapiforms, dermopterans, and Ptilocercus exhibit lateral FHLGs. Extant anthropoids, subfossil lemurs, and Tupaia have medial FHLGs. FHLGs of omomyiforms and basal fossil anthropoids are intermediate between those of strepsirrhines and extant anthropoids. FHLG position has few correlations with pedal inversion features. Relative FHLG depth is not significantly correlated with body mass. ASRs support a directional model for FHLG position and a random walk model for FHLG depth.The prevalence of lateral FHLGs in many non-euprimates suggests a lateral FHLG is not a derived strepsirrhine feature. The lack of correlations with pedal inversion features suggests a lateral FHLG is not a sufficient indicator of strepsirrhine-like foot postures. Instead, a lateral FHLG may reduce the risk of tendon displacement in abducted foot postures on large diameter supports. A deep FHLG does not indicate a larger muscle, but likely reduces bowstringing during plantarflexion.
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    Stem members of Platyrrhini are distinct from catarrhines in at least one derived cranial feature.
    (Journal of human evolution, 2016-11) Fulwood, Ethan L; Boyer, Doug M; Kay, Richard F
    The pterion, on the lateral aspect of the cranium, is where the zygomatic, frontal, sphenoid, squamosal, and parietal bones approach and contact. The configuration of these bones distinguishes New and Old World anthropoids: most extant platyrrhines exhibit contact between the parietal and zygomatic bones, while all known catarrhines exhibit frontal-alisphenoid contact. However, it is thought that early stem-platyrrhines retained the apparently primitive catarrhine condition. Here we re-evaluate the condition of key fossil taxa using μCT (micro-computed tomography) imaging. The single known specimen of Tremacebus and an adult cranium of Antillothrix exhibit the typical platyrrhine condition of parietal-zygomatic contact. The same is true of one specimen of Homunculus, while a second specimen has the 'catarrhine' condition. When these new data are incorporated into an ancestral state reconstruction, they support the conclusion that pterion frontal-alisphenoid contact characterized the last common ancestor of crown anthropoids and that contact between the parietal and zygomatic is a synapomorphy of Platyrrhini.
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    The effect of differences in methodology among some recent applications of shearing quotients.
    (Am J Phys Anthropol, 2015-01) Boyer, Doug M; Winchester, Julia; Kay, Richard F
    A shearing quotient (SQ) is a way of quantitatively representing the Phase I shearing edges on a molar tooth. Ordinary or phylogenetic least squares regression is fit to data on log molar length (independent variable) and log sum of measured shearing crests (dependent variable). The derived linear equation is used to generate an 'expected' shearing crest length from molar length of included individuals or taxa. Following conversion of all variables to real space, the expected value is subtracted from the observed value for each individual or taxon. The result is then divided by the expected value and multiplied by 100. SQs have long been the metric of choice for assessing dietary adaptations in fossil primates. Not all studies using SQ have used the same tooth position or crests, nor have all computed regression equations using the same approach. Here we focus on re-analyzing the data of one recent study to investigate the magnitude of effects of variation in 1) shearing crest inclusion, and 2) details of the regression setup. We assess the significance of these effects by the degree to which they improve or degrade the association between computed SQs and diet categories. Though altering regression parameters for SQ calculation has a visible effect on plots, numerous iterations of statistical analyses vary surprisingly little in the success of the resulting variables for assigning taxa to dietary preference. This is promising for the comparability of patterns (if not casewise values) in SQ between studies. We suggest that differences in apparent dietary fidelity of recent studies are attributable principally to tooth position examined.
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    Vertical support use and primate origins.
    (Scientific reports, 2019-08) Yapuncich, Gabriel S; Feng, Henry J; Dunn, Rachel H; Seiffert, Erik R; Boyer, Doug M
    Adaptive scenarios of crown primate origins remain contentious due to uncertain order of acquisition and functional significance of the clade's diagnostic traits. A feature of the talus bone in the ankle, known as the posterior trochlear shelf (PTS), is well-regarded as a derived crown primate trait, but its adaptive significance has been obscured by poorly understood function. Here we propose a novel biomechanical function for the PTS and model the talus as a cam mechanism. By surveying a large sample of primates and their closest relatives, we demonstrate that the PTS is most strongly developed in extant taxa that habitually grasp vertical supports with strongly dorsiflexed feet. Tali of the earliest fossils likely to represent crown primates exhibit more strongly developed PTS cam mechanisms than extant primates. As a cam, the PTS may increase grasping efficiency in dorsiflexed foot postures by increasing the path length of the flexor fibularis tendon, and thus improve the muscle's ability to maintain flexed digits without increasing energetic demands. Comparisons are made to other passive digital flexion mechanisms suggested to exist in other vertebrates. These results provide robust anatomical evidence that the habitual vertical support use exerted a strong selective pressure during crown primate origins.
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    Wear and its effects on dental topography measures in howling monkeys (Alouatta palliata).
    (Am J Phys Anthropol, 2016-12) Pampush, James D; Spradley, Jackson P; Morse, Paul E; Harrington, Arianna R; Allen, Kari L; Boyer, Doug M; Kay, Richard F
    OBJECTIVES: Three dental topography measurements: Dirichlet Normal Energy (DNE), Relief Index (RFI), and Orientation Patch Count Rotated (OPCR) are examined for their interaction with measures of wear, within and between upper and lower molars in Alouatta palliata. Potential inferences of the "dental sculpting" phenomenon are explored. MATERIALS AND METHODS: Fifteen occluding pairs of howling monkey first molars (15 upper, 15 lower) opportunistically collected from La Pacifica, Costa Rica, were selected to sample wear stages ranging from unworn to heavily worn as measured by the Dentine Exposure Ratio (DER). DNE, RFI, and OPCR were measured from three-dimensional surface reconstructions (PLY files) derived from high-resolution CT scans. Relationships among the variables were tested with regression analyses. RESULTS: Upper molars have more cutting edges, exhibiting significantly higher DNE, but have significantly lower RFI values. However, the relationships among the measures are concordant across both sets of molars. DER and EDJL are curvilinearly related. DER is positively correlated with DNE, negatively correlated with RFI, and uncorrelated with OPCR. EDJL is not correlated with DNE, or RFI, but is positively correlated with OPCR among lower molars only. DISCUSSION: The relationships among these metrics suggest that howling monkey teeth adaptively engage macrowear. DNE increases with wear in this sample presumably improving food breakdown. RFI is initially high but declines with wear, suggesting that the initially high RFI safeguards against dental senescence. OPCR values in howling monkey teeth do not show a clear relationship with wear changes.