Bolstering geometric morphometrics sample sizes with damaged and pathologic specimens: Is near enough good enough?

Obtaining coordinate data for geometric morphometric studies often involves the sampling of dry skeletal specimens from museum collections. But many specimens exhibit damage and/or pathologic conditions. Such specimens can be considered inadequate for the analyses of shape and are excluded from study. However, the influences that damaged specimens may have on the assessment of normal shape variation have only been explored in two-dimensional coordinate data and no studies have addressed the inclusion of pathological specimens to date. We collected three-dimensional coordinate data from the cranium and mandible of 100 crab-eating macaques (Macaca fascicularis). Tests typically employed to analyze shape variation were performed on five datasets that included specimens with varying degrees of damage/pathology. We hypothesized that the inclusion of these specimens into larger datasets would strengthen statistical support for dominant biological predictors of shape, such as sex and size. However, we also anticipated that the analysis of only the most questionable specimens may confound statistical outputs. We then analyzed a small sample of good quality specimens bolstered by specimens that would generally be excluded due to damage or pathologic morphology and compared the results with previous analyses. The inclusion of damaged/pathologic specimens in a larger dataset resulted in increased variation linked to allometry, sexual dimorphism, and covariation, supporting our initial hypothesis. We found that analyzing the most questionable specimens alone gave consistent results for the most dominant aspects of shape but could affect outputs for less influential principal components and predictors. The small dataset bolstered with damaged/pathologic specimens provided an adequate assessment of the major components of shape, but finer scale differences were also identified. We suggest that normal and repeatable variation contributed by specimens exhibiting damage and/or pathology emphasize the dominant components and shape predictors in larger datasets, however, the various unique conditions may be more influential for limited sample sizes. Furthermore, we find that exclusion of damaged/pathologic specimens can, in some cases, omit important demographic-specific shape variation of groups of individuals more likely to exhibit these conditions. These findings provide a strong case for inclusion of these specimens into studies that focus on the dominant aspects of intraspecific shape variation. However, they may present issues when testing hypotheses relating to more fine-scale aspects of morphology.

Parvimico materdei gen. et sp. nov.: A new platyrrhine from the Early Miocene of the Amazon Basin, Peru.

Three field seasons of exploration along the Río Alto Madre de Dios in Peruvian Amazonia have yielded a fauna of micromammals from a new locality AMD-45, at ∼12.8°S. So far we have identified the new primate described here as well as small caviomorph rodents, cenolestoid marsupials, interatheriid notoungulates, xenarthrans, fish, lizards and invertebrates. The site is in the Bala Formation as exposed where the river transects a syncline. U-Pb dates on detrital zircons constrain the locality's age at between 17.1 ± 0.7 Ma and 18.9 ± 0.7 Ma, making the fauna age-equivalent to that from the Pinturas Formation and the older parts of the Santa Cruz Formation of Patagonian Argentina (Santacrucian). The primate specimen is an unworn M1 of exceptionally small size (equivalent in size to the extant callitrichine, Callithrix jacchus, among the smallest living platyrrhines and the smallest Eocene-Early Miocene platyrrhine yet recorded). Despite its small size it is unlike extant callitrichines in having a prominent cingulum hypocone. Based on the moderate development of the buccal crests, this animal likely had a diet similar to that of frugivorous callitrichines, and distinctly different from the more similarly-sized gummivores, Cebuella and C. jacchus. The phyletic position of the new taxon is uncertain, especially given the autapomorphic character of the tooth as a whole. Nevertheless, its unusual morphology hints at a wholly original and hitherto unknown Amazonian fauna, and reinforces the impression of the geographic separation of the Amazonian tropics from the more geographically isolated southerly parts of the continent in Early Miocene times.

Articular scaling and body mass estimation in platyrrhines and catarrhines: Modern variation and application to fossil anthropoids.

Body mass is an important component of any paleobiological reconstruction. Reliable skeletal dimensions for making estimates are desirable but extant primate reference samples with known body masses are rare. We estimated body mass in a sample of extinct platyrrhines and Fayum anthropoids based on four measurements of the articular surfaces of the humerus and femur. Estimates were based on a large extant reference sample of wild-collected individuals with associated body masses, including previously published and new data from extant platyrrhines, cercopithecoids, and hominoids. In general, scaling of joint dimensions is positively allometric relative to expectations of geometric isometry, but negatively allometric relative to expectations of maintaining equivalent joint surface areas. Body mass prediction equations based on articular breadths are reasonably precise, with %SEEs of 17-25%. The breadth of the distal femoral articulation yields the most reliable estimates of body mass because it scales similarly in all major anthropoid taxa. Other joints scale differently in different taxa; therefore, locomotor style and phylogenetic affinity must be considered when calculating body mass estimates from the proximal femur, proximal humerus, and distal humerus. The body mass prediction equations were applied to 36 Old World and New World fossil anthropoid specimens representing 11 taxa, plus two Haitian specimens of uncertain taxonomic affinity. Among the extinct platyrrhines studied, only Cebupithecia is similar to large, extant platyrrhines in having large humeral (especially distal) joints. Our body mass estimates differ from each other and from published estimates based on teeth in ways that reflect known differences in relative sizes of the joints and teeth. We prefer body mass estimators that are biomechanically linked to weight-bearing, and especially those that are relatively insensitive to differences in locomotor style and phylogenetic history. Whenever possible, extant reference samples should be chosen to match target fossils in joint proportionality.

Dental topography of platyrrhines and prosimians: convergence and contrasts.

Dental topographic analysis is the quantitative assessment of shape of three-dimensional models of tooth crowns and component features. Molar topographic curvature, relief, and complexity correlate with aspects of feeding behavior in certain living primates, and have been employed to investigate dietary ecology in extant and extinct primate species. This study investigates whether dental topography correlates with diet among a diverse sample of living platyrrhines, and compares platyrrhine topography with that of prosimians. We sampled 111 lower second molars of 11 platyrrhine genera and 121 of 20 prosimian genera. For each tooth we calculated Dirichlet normal energy (DNE), relief index (RFI), and orientation patch count (OPCR), quantifying surface curvature, relief, and complexity respectively. Shearing ratios and quotients were also measured. Statistical analyses partitioned effects of diet and taxon on topography in platyrrhines alone and relative to prosimians. Discriminant function analyses assessed predictive diet models. Results indicate that platyrrhine dental topography correlates to dietary preference, and platyrrhine-only predictive models yield high rates of accuracy. The same is true for prosimians. Topographic variance is broadly similar among platyrrhines and prosimians. One exception is that platyrrhines display higher average relief and lower relief variance, possibly related to lower relative molar size and functional links between relief and tooth longevity distinct from curvature or complexity. Explicitly incorporating phylogenetic distance matrices into statistical analyses of the combined platyrrhine-prosimian sample results in loss of significance of dietary effects for OPCR and SQ, while greatly increasing dietary significance of RFI.

An extinct monkey from Haiti and the origins of the Greater Antillean primates.

A new extinct Late Quaternary platyrrhine from Haiti, Insulacebus toussaintiana, is described here from the most complete Caribbean subfossil primate dentition yet recorded, demonstrating the likely coexistence of two primate species on Hispaniola. Like other Caribbean platyrrhines, I. toussaintiana exhibits primitive features resembling early Middle Miocene Patagonian fossils, reflecting an early derivation before the Amazonian community of modern New World anthropoids was configured. This, in combination with the young age of the fossils, provides a unique opportunity to examine a different parallel radiation of platyrrhines that survived into modern times, but is only distantly related to extant mainland forms. Their ecological novelty is indicated by their unique dental proportions, and by their relatively large estimated body weights, possibly an island effect, which places the group in a size class not exploited by mainland South American monkeys. Several features tie the new species to the extinct Jamaican monkey Xenothrix mcgregori, perhaps providing additional evidence for an inter-Antillean clade.

Rethinking Antillothrix: the mandible and its implications.

A mandible of the Hispaniolan primate Antillothrix bernensis, virtually complete and providing the only definitive evidence of the species' lower dentition, has been discovered in a submerged Dominican Republic cave. The new specimen enables a more certain assessment of the species' phylogenetic position than previously possible. It belongs to the same individual as the nearly complete young adult cranium and postrcranial elements found earlier at the same site. Of the extinct Caribbean platyrrhines, the jaw compares well with partial mandibles representing Xenothrix mcgregori, from Jamaica. Among living platyrrhines, it closely resembles Callicebus and Aotus, as documented in a biometric analysis employing three-dimensional geometric morphometrics of Callicebus, Aotus, Pithecia, Chiropotes, Cacajao, Cebus, and Saimiri. The jaw falls within the morphological variability of Callicebus and Aotus in this three-dimensional analysis, is otherwise most similar to Pithecia, and is distinct from cebines. Lower molars resemble the Haitian primate, Insulacebus, a genus known by a full dentition and gnathic fragments with a pattern of derived features also present in Xenothrix. Considering the available craniodental and postcranial evidence, we conclude that Antillothrix is not properly classified as cebid but rather is best grouped with Pitheciidae, an idea long central to discussions of the phylogenetic affinities of the Greater Antillean primates. Since Antillothrix and Insulacebus are more primitive anatomically than the highly modified Xenothrix, it is tempting to surmise that the origins of the latter involved a vicariance or dispersal event via Hispaniola isolating it on Jamaica.

Temporomandibular joint shape in anthropoid primates varies widely and is patterned by size and phylogeny.

The temporomandibular joint is the direct interface between the mandible and the cranium and is critical for transmitting joint reaction forces and determining mandibular range of motion. As a consequence, understanding variation in the morphology of this joint and how it relates to other aspects of craniofacial form is important for better understanding masticatory function. Here, we present a detailed three-dimensional (3D) geometric morphometric analysis of the cranial component of this joint, the glenoid fossa, across a sample of 17 anthropoid primates, and we evaluate covariation between the glenoid and the cranium and mandible. We find high levels of intraspecific variation in glenoid shape that is likely linked to sexual dimorphism and joint remodeling, and we identify differences in mean glenoid shape across taxonomic groups and in relation to size. Analyses of covariation reveal strong relationships between glenoid shape and a variety of aspects of cranial and mandibular form. Our findings suggest that intraspecific variation in glenoid shape in primates could further be reflective of high levels of functional flexibility in the masticatory apparatus, as has also been suggested for primate jaw kinematics and muscle activation patterns. Conversely, interspecific differences likely reflect larger scale differences between species in body size and/or masticatory function. Results of the covariation analyses dovetail with those examining covariation in the cranium of canids and may be indicative of larger patterns across mammals.

First skull of Antillothrix bernensis, an extinct relict monkey from the Dominican Republic.

The nearly pristine remains of Antillothrix bernensis, a capuchin-sized (Cebus) extinct platyrrhine from the Dominican Republic, have been found submerged in an underwater cave. This represents the first specimen of an extinct Caribbean primate with diagnostic craniodental and skeletal parts in association, only the second example of a skull from the region, and one of the most complete specimens of a fossil platyrrhine cranium yet discovered. Cranially, it closely resembles living cebines but is more conservative. Dentally, it is less bunodont and more primitive than Cebus, with crowns resembling Saimiri (squirrel monkeys) and one of the oldest definitive cebines, the late Early Miocene Killikaike blakei from Argentina. The tricuspid second molar also resembles the enigmatic marmosets and tamarins, whose origins continue to present a major gap in knowledge of primate evolution. While the femur is oddly short and stout, the ulna, though more robust, compares well with Cebus. As a member of the cebid clade, Antillothrix demonstrates that insular Caribbean monkeys are not monophyletically related and may not be the product of a single colonizing event. Antillothrix bernensis is an intriguing mosaic whose primitive characters are consistent with an early origin, possibly antedating the assembly of the modern primate fauna in greater Amazonia during the La Venta horizon. While most Greater Antillean primate specimens are quite young geologically, this vanished radiation, known from Cuba (Paralouatta) and Jamaica (Xenothrix) as well as Hispaniola, appears to be composed of long-lived lineages like several other mainland clades.

Form and function in the platyrrhine skull: a three-dimensional analysis of dental and TMJ morphology.

Cranial and temporomandibular joint (TMJ) form has been shown to reflect masticatory forces and mandibular range of motion, which vary in relation to feeding strategy. Similarly, the dentition, as the portion of the masticatory apparatus most directly involved in triturating food items, strongly reflects dietary profile. Fine control over condylar and mandibular movements guides the teeth into occlusion, while the topography and position of the dental arcade mediate mandibular movements. We hypothesize that masticatory, and particularly TMJ, morphology and dental form covary in predictable ways with one another and with diet. We employed three-dimensional geometric morphometric techniques to examine inter-specific variation in ten platyrrhine species. Landmarks were collected on six datasets describing the upper and lower molars, cranium, glenoid fossa, mandible, and mandibular condyle; two-block partial least squares analyses were performed to assess covariation between cranial morphology, dentition, and diet. Significant relationships were identified between the molars and the cranium, mandible, and glenoid fossa. Some of these shape complexes reflect feeding strategy; for example, higher crowned/cusped dentitions, as found in primates consuming larger quantities of structural carbohydrates (e.g., Alouatta and Saimiri), correspond to anteroposterior longer and deeper glenoid fossae. These results indicate strong covariance between dental and TMJ form, aspects of which are related to feeding behavior. However, other aspects of morphological variation display a strong phylogenetic signal; we must therefore examine further ways in which to control for phylogeny when examining covariation in interspecific masticatory form.

Dietary inference from upper and lower molar morphology in platyrrhine primates.

The correlation between diet and dental topography is of importance to paleontologists seeking to diagnose ecological adaptations in extinct taxa. Although the subject is well represented in the literature, few studies directly compare methods or evaluate dietary signals conveyed by both upper and lower molars. Here, we address this gap in our knowledge by comparing the efficacy of three measures of functional morphology for classifying an ecologically diverse sample of thirteen medium- to large-bodied platyrrhines by diet category (e.g., folivore, frugivore, hard object feeder). We used Shearing Quotient (SQ), an index derived from linear measurements of molar cutting edges and two indices of crown surface topography, Occlusal Relief (OR) and Relief Index (RFI). Using SQ, OR, and RFI, individuals were then classified by dietary category using Discriminate Function Analysis. Both upper and lower molar variables produce high classification rates in assigning individuals to diet categories, but lower molars are consistently more successful. SQs yield the highest classification rates. RFI and OR generally perform above chance. Upper molar RFI has a success rate below the level of chance. Adding molar length enhances the discriminatory power for all variables. We conclude that upper molar SQs are useful for dietary reconstruction, especially when combined with body size information. Additionally, we find that among our sample of platyrrhines, SQ remains the strongest predictor of diet, while RFI is less useful at signaling dietary differences in absence of body size information. The study demonstrates new ways for inferring the diets of extinct platyrrhine primates when both upper and lower molars are available, or, for taxa known only from upper molars. The techniques are useful in reconstructing diet in stem representatives of anthropoid clade, who share key aspects of molar morphology with extant platyrrhines.

Paleodiet of extinct platyrrhines with emphasis on the Caribbean forms: three-dimensional geometric morphometrics of mandibular second molars.

A three-dimensional geometric morphometric approach was employed to examine shape variation in laser-scan generated models of lower second molars and its relationship to diet in a sample of 9 extant and 16 extinct platyrrhine genera. Principal component analysis of twenty-three x,y,z landmarks describing the occlusal table and sidewalls showed that dental relief was the main contributing factor to variation along the first axis. Discriminant function analysis (DFA) of PC 1 scores and centroid size accurately classified extant platyrrhines according to dietary preference; however, without centroid size, the DFA was less successful. Within this framework, most of the fossil platyrrhines, including specimens from Patagonia, Colombia, Brazil, and the Caribbean, were predicted to have had a frugivorous diet, but several taxa were classified as having a frugivorous/insectivorous diet, the middle Miocene Neosaimiri, Patasola, and Laventiana, all from La Venta. Alouattins, including the La Ventan Stirtonia and the Cuban Paralouatta, showed variable classification as either frugivores or folivore/frugivores. Xenothrix, from Jamaica, was classified either as a frugivore or frugivore/omnivore. Dietary profiles across different extinct platyrrhine communities are compared and discussed in a paleoecological context.

The making of platyrrhine semifolivores: models for the evolution of folivory in primates.

Among living New World monkeys, Howlers and Muriquis are by far the most folivorous. We examine how well the morphology and behavior of Alouatta and Brachyteles conform to leaf-eating adaptational models derived from other studies. Both genera match these expectations unevenly, which suggests a broader conception of primate folivory is in order. Hence the notion of "semifolivory." While their dentitions prove highly sensitive to selection for leaf-eating, core features relating to body size, brain size, ranging behavior and presumed energy budgets are less predictable corollaries. Leaf-eating in atelines and colobines may have evolved from a preadaptive reliance on seed-eating, which would have necessitated comparable gastric adaptations. Fossils suggest semifolivory in the low-energy Howler lineage may have begun with an increase in body size, a relatively small brain and, possibly, a concomitantly enlarged gut, followed by dental adaptations. It may have advanced via body-size reduction, part of a pioneering adaptation in marginal ecologies on the periphery of rich Amazonian habitats or as a strategy to minimize competition among an abundance of frugivores within the lowland forest-perhaps not as a fallback scheme. In the high-energy Muriqui, semifolivory may have evolved in more intensely seasonal, low-yield forests where frugivores were constrained and rare, a model more consistent with the fallback paradigm. The seed-to-leaves evolutionary pathway hypothesized for anthropoid leaf-eaters may be a widespread phenomenon in primates. We propose it is ultimately rooted in a pre-euprimate reliance on the seeds and seed coats of primitive angiosperms before the latter evolved attractive sugary fruits to coax primates into becoming dispersers of seeds, instead consumers.