Siobhán B. Cooke

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.

Platyrrhine Ecophylogenetics in Space and Time

We are far from developing an informed synthesis regarding the evolution of New World Monkeys – probably decades away. For even with the important strides made over the past 30–40 years regarding platyrrhine ecology and behavior, there are large gaps in our knowledge of the evolutionary and historical context. The scarceness of fossils is but one factor. Equally critical is our incomplete knowledge of largescale changes to the continent of South America (SAM), pertinent to the evolution of its fauna. An objective of this paper is to review some of this information as a basis for interpreting the platyrrhines from an ecophylogenetic point of view in space and time. Our goal is to integrate information on living and extinct forms in order to identify community or regional patterns of platyrrhine evolution, rather than examining the moderns and fossils as distinct entities or evolutionary problems. In keeping with the South American emphasis of this volume, we do not consider the primate fauna of the Middle American mainland but have elected to examine the Caribbean subfossil monkeys for reasons that will become clear below. We suggest that the casual way of thinking about New World Monkeys (NWM) as a monolithic radiation inhabiting a rainforest wonderland – South America – is a model that needs to be changed. The continent is about 2.5 times the size of today’s Amazonian rainforest in area, it contains diverse landscapes and habitats, and the Amazonian region changed vastly during the Cenozoic (e.g., Bigarella and Ferreira 1985). At present, more of the continent is grassland than rainforest (Fig. 4.1a), and the grasslands have been flourishing for 20–30 million years (see below). The first primates to arrive did not encounter the Amazonia we know, for it may have begun to take on its present character only about 15 Ma (Campbell et al. 2006). Thus, even though the NWM have a monophyletic, unitary origin, their

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.

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. Anat Rec, , 2011.

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. Anat Rec, 2011.

Form, Function, and Geometric Morphometrics

Geometric morphometrics (GM) has increasingly become an important tool in assessing and studying shape variation in a wide variety of taxa. While the GM toolkit has unparalleled power to quantify shape, its use in studies of functional morphology have been questioned. Here, we assess the state of the field of GM and provide an overview of the techniques available to assess shape, including aspects of visualization, statistical analysis, phylogenetic control, and more. Additionally, we briefly review the history of functional morphology and summarize the main tools available to the functional morphologist. We explore the intersection of geometric morphometrics and functional morphology and we suggest ways that we may be able to move forward in profitably combining these two research areas. Finally, this paper provides a brief introduction to the papers in this special issue and highlights the ways in which the contributing authors have approached the intersection of GM and functional morphology. Anat Rec, 298:5–28, 2015.

Quaternary Bat Diversity in the Dominican Republic

ABSTRACT The fossil record of bats is extensive in the Caribbean, but few fossils have previously been reported from the Dominican Republic. In this paper, we describe new collections of fossil bats from two flooded caves in the Dominican Republic, and summarize previous finds from the Island of Hispaniola. The new collections were evaluated in the context of extant and fossil faunas of the Greater Antilles to provide information on the evolution of the bat community of Hispaniola. Eleven species were identified within the new collections, including five mormoopids (Mormoops blainvillei, †Mormoops magna, Pteronotus macleayii, P. parnellii, and P. quadridens), five phyllostomids (Brachyphylla nana, Monophyllus redmani, Phyllonycteris poeyi, Erophylla bombifrons, and Phyllops falcatus), and one natalid (Chilonatalus micropus). All of these species today inhabitant Hispaniola with the exception of †Mormoops magna, an extinct species previously known only from the Quaternary of Cuba, and Pteronotus macleayii, which is currently known only from extant populations in Cuba and Jamaica, although Quaternary fossils have also been recovered in the Bahamas. Differences between the fossil faunas and those known from the island today suggest that dispersal and extirpation events, perhaps linked to climate change or stochastic events such as hurricanes, may have played roles in structuring the modern fauna of Hispaniola.

Fossil Alouattines and the Origins of Alouatta: Craniodental Diversity and Interrelationships

The howler monkey clade includes species of Alouatta and four extinct genera, Stirtonia, Paralouatta, Protopithecus, and probably Solimoea as well. Contrary to expectations, this radiation may have originated as a largely frugivorous group; advanced, Alouatta-like leaf-eating is a novelty well-developed in the Alouatta-Stirtonia sublineage only. Revised body mass estimates place Stirtonia and Paralouatta within the size range exhibited by the living forms and confirm the place of Protopithecus in a larger, baboon-like size range. While their dentitions are more primitive than the Alouatta-Stirtonia pattern, the cranial anatomy of Protopithecus and Paralouatta is distinctly similar to living howler monkeys in highly derived features relating to enlargement of the subbasal space in the neck and in head carriage, suggesting that ancestral alouattines may have had an enlarged hyolaryngeal apparatus. All alouattines also have relatively small brains, including Protopithecus, a genus that was probably quite frugivorous. The successful origins of the alouattine clade may owe more to key adaptations involving communication and energetics than dental or locomotor breakthroughs. While the fossil record confirms aspects of previous character-analysis reconstructions based on the living forms, alouattines experienced a complexity of adaptive shifts whose history cannot be recoverable without a more complete fossil record.*

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. Anat Rec, 298:29–47, 2015.

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.