Gabriel S. Yapuncich

A new fully automated approach for aligning and comparing shapes.

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 morphologika2.5 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. Anat Rec, 298:249–276, 2015.

Hands of early primates

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.

Predicting euarchontan body mass: A comparison of tarsal and dental variables.

OBJECTIVE 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. METHODS 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. RESULTS 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. CONCLUSIONS 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.

Internal carotid arterial canal size and scaling in Euarchonta: Re-assessing implications for arterial patency and phylogenetic relationships in early fossil primates.

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.

Quantification of the position and depth of the flexor hallucis longus groove in euarchontans, with implications for the evolution of primate positional behavior

OBJECTIVE 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. METHODS 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). RESULTS 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. CONCLUSIONS 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.

Development and Assessment of Fully Automated and Globally Transitive Geometric Morphometric Methods, With Application to a Biological Comparative Dataset With High Interspecific Variation: ASSESSMENT OF AUTOMATED TRANSITIVE GM METHODS

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.

Catarrhine hallucal metatarsals from the early Miocene site of Songhor, Kenya

Songhor is an early Miocene fossil locality in Kenya known for its diverse primate assemblage that includes catarrhine species belonging to the genera Kalepithecus, Limnopithecus, Dendropithecus, Rangwapithecus, and Proconsul. Expeditions to Songhor since the 1930s have recovered unassociated catarrhine postcranial remains from both the fore- and hindlimbs, including multiple elements from the feet. In this study, we describe KNM-SO 31233, a complete left hallucal metatarsal (Mt1), along with several other fragmentary Mt1 specimens (KNM-SO 1080, 5129, 5141, 22235). These fossils were compared to extant catarrhines and platyrrhines, as well as available fossil Miocene catarrhine Mt1s. Morphometric data were obtained from 3D surface renderings and subjected to a number of analyses to assess their phenetic affinity with the comparative sample, make predictions of body mass, and to infer their functional morphology. The size and shape of the Songhor Mt1s are diverse, exhibiting a large robust morph (KNM-SO 5141) similar in size but not in shape to extant African apes, medium-sized morphs (KNM-SO 1080, 5129 and 22235), and a smaller, slender one (KNM-SO 31233) that has a shape resembling arboreal quadrupedal leaping monkeys and suspensory atelines and hylobatids. KNM-SO 31233 is unlike other known fossil Mt1s, and in general, none of the Songhor Mt1s resembled any single extant anthropoid clade or species. The morpho-functional diversity of Songhor Mt1s is consistent with an extensive morphological and phylogenetic catarrhine diversity in the early part of the Miocene epoch.

Alternative methods for calculating percentage prediction error and their implications for predicting body mass in fossil taxa

Since body mass covaries with many ecological aspects of an animal, body mass prediction of fossil taxa is a frequent goal of paleontologists. Body mass prediction often relies on a body mass prediction equation (BMPE): a bivariate relationship between a predictor variable (e.g., molar occlusal area, femoral head breadth) and body mass as observed in extant taxa. A variety of metrics have been used to assess the reliability of BMPEs, including percentage prediction error (%PE), which involves predicting body masses of a test sample comprising individuals with associated masses. A mean %PE can be calculated in two ways: 1) as the mean %PE of multiple individual predictions (%MPE), or 2) as the %PE of mean body mass generated from the mean predictor value of multiple individuals (here termed %PEM). Differences between these two approaches have never been formally examined and no formal protocols have been recommended. Using a large sample of cercopithecoid primates (406 individuals from 50 species/subspecies) with associated body masses, body mass is predicted with six previously published interspecific BMPEs. Both %MPE and %PEM are calculated and compared. For all BMPEs, the distributions of differences between %MPE and %PEM exhibit positive skew and have medians significantly greater than zero, indicating that the examined prediction equations are more accurate at predicting mean body mass when they are applied to mean predictor values. The decreased predictive accuracy of %MPE relative to %PEM likely stems from changing the unit of analysis from mean values (in the reference sample) to individual values (in the test sample) when calculating %MPE. Empirical results are supported with a simulated dataset. Implications for body mass prediction in fossil species are discussed.

Hands of Paleogene Primates

To understand the hand of living primates from an adaptive perspective, data on the morphological pattern of the earliest primates is required. This chapter discusses what is known about the early evolution of primate hands based on fossils of Paleogene plesiadapiforms (potential stemprimates), adapiforms, omomyiforms, and anthropoids. Implications of these data for understanding locomotor transitions during the origin and early evolutionary history of primates is considered.

The Independent Evolution Method Is Not a Viable Phylogenetic Comparative Method.

Phylogenetic comparative methods (PCMs) use data on species traits and phylogenetic relationships to shed light on evolutionary questions. Recently, Smaers and Vinicius suggested a new PCM, Independent Evolution (IE), which purportedly employs a novel model of evolution based on Felsenstein’s Adaptive Peak Model. The authors found that IE improves upon previous PCMs by producing more accurate estimates of ancestral states, as well as separate estimates of evolutionary rates for each branch of a phylogenetic tree. Here, we document substantial theoretical and computational issues with IE. When data are simulated under a simple Brownian motion model of evolution, IE produces severely biased estimates of ancestral states and changes along individual branches. We show that these branch-specific changes are essentially ancestor-descendant or “directional” contrasts, and draw parallels between IE and previous PCMs such as “minimum evolution”. Additionally, while comparisons of branch-specific changes between variables have been interpreted as reflecting the relative strength of selection on those traits, we demonstrate through simulations that regressing IE estimated branch-specific changes against one another gives a biased estimate of the scaling relationship between these variables, and provides no advantages or insights beyond established PCMs such as phylogenetically independent contrasts. In light of our findings, we discuss the results of previous papers that employed IE. We conclude that Independent Evolution is not a viable PCM, and should not be used in comparative analyses.