A parapithecid stem anthropoid of African origin in the Paleogene of South America.

Phylogenetic evidence suggests that platyrrhine (or New World) monkeys and caviomorph rodents of the Western Hemisphere derive from source groups from the Eocene of Afro-Arabia, a landmass that was ~1500 to 2000 kilometers east of South America during the late Paleogene. Here, we report evidence for a third mammalian lineage of African origin in the Paleogene of South America-a newly discovered genus and species of parapithecid anthropoid primate from Santa Rosa in Amazonian Perú. Bayesian clock-based phylogenetic analysis nests this genus (Ucayalipithecus) deep within the otherwise Afro-Arabian clade Parapithecoidea and indicates that transatlantic rafting of the lineage leading to Ucayalipithecus likely took place between ~35 and ~32 million years ago, a dispersal window that includes the major worldwide drop in sea level that occurred near the Eocene-Oligocene boundary.

Characterizing and Comparing Phylogenetic Trait Data from Their Normalized Laplacian Spectrum.

The dissection of the mode and tempo of phenotypic evolution is integral to our understanding of global biodiversity. Our ability to infer patterns of phenotypes across phylogenetic clades is essential to how we infer the macroevolutionary processes governing those patterns. Many methods are already available for fitting models of phenotypic evolution to data. However, there is currently no comprehensive nonparametric framework for characterizing and comparing patterns of phenotypic evolution. Here, we build on a recently introduced approach for using the phylogenetic spectral density profile (SDP) to compare and characterize patterns of phylogenetic diversification, in order to provide a framework for nonparametric analysis of phylogenetic trait data. We show how to construct the SDP of trait data on a phylogenetic tree from the normalized graph Laplacian. We demonstrate on simulated data the utility of the SDP to successfully cluster phylogenetic trait data into meaningful groups and to characterize the phenotypic patterning within those groups. We furthermore demonstrate how the SDP is a powerful tool for visualizing phenotypic space across traits and for assessing whether distinct trait evolution models are distinguishable on a given empirical phylogeny. We illustrate the approach in two empirical data sets: a comprehensive data set of traits involved in song, plumage, and resource-use in tanagers, and a high-dimensional data set of endocranial landmarks in New World monkeys. Considering the proliferation of morphometric and molecular data collected across the tree of life, we expect this approach will benefit big data analyses requiring a comprehensive and intuitive framework.

The CENP-B box, a nucleotide motif involved in centromere formation, has multiple origins in New World monkeys.

Centromere protein B (CENP-B), a protein participating in centromere formation, binds to centromere satellite DNA by recognizing a 17-bp motif called the CENP-B box. This motif is found in hominids (humans and great apes) at an identical location in repeat units of their centromere satellite DNA. We have recently reported that the CENP-B box exists at diverse locations in three New World monkey species (marmoset, squirrel monkey and tamarin). However, the evolutionary origin of the CENP-B box in these species was not determined. It could have been present in a common ancestor, or emerged multiple times in different lineages. Here we present results of a phylogenetic analysis of centromere satellite DNA that support the multiple emergence hypothesis. Repeat units almost invariably formed monophyletic groups in each species and the CENP-B box location was unique for each species. The CENP-B box is not essential for the immediate survival of its host organism. On the other hand, it is known to be required for de novo centromere assembly. Our results suggest that the CENP-B box confers a long-term selective advantage. For example, it may play a pivotal role when a centromere is accidentally lost or impaired.

Cooperative evolution of two different TEs results in lineage-specific novel transcripts in the BLOC1S2 gene.

BACKGROUND: The BLOC1S2 gene encodes the multifunctional protein BLOS2, a shared subunit of two lysosomal trafficking complexes: i) biogenesis of lysosome-related organelles complex-1 and i) BLOC-1-related complex. In our previous study, we identified an intriguing unreported transcript of the BLOC1S2 gene that has a novel exon derived from two transposable elements (TEs), MIR and AluSp. To investigate the evolutionary footprint and molecular mechanism of action of this transcript, we performed PCR and RT-PCR experiments and sequencing analyses using genomic DNA and RNA samples from humans and various non-human primates. RESULTS: The results showed that the MIR element had integrated into the genome of our common ancestor, specifically in the BLOC1S2 gene region, before the radiation of all primate lineages and that the AluSp element had integrated into the genome of our common ancestor, fortunately in the middle of the MIR sequences, after the divergence of Old World monkeys and New World monkeys. The combined MIR and AluSp sequences provide a 3' splice site (AG) and 5' splice site (GT), respectively, and generate the Old World monkey-specific transcripts. Moreover, branch point sequences for the intron removal process are provided by the MIR and AluSp combination. CONCLUSIONS: We show for the first time that sequential integration into the same location and sequence divergence events of two different TEs generated lineage-specific transcripts through sequence collaboration during primate evolution.

Effects of substrate and phylogeny on quadrupedal gait in free-ranging platyrrhines.

OBJECTIVES: Primate diagonal sequence (DS) gaits are often argued to be an adaptation for moving and foraging in the fine-branch niche; however, existing data have come predominantly from laboratory studies that are limited in taxonomic breadth and fail to account for the structural and ecological variation of natural substrates. We test the extent to which substrate diameter and orientation influence gait sequence type and limb phase in free-ranging primates, as well as how phylogenetic relatedness might condition response patterns. MATERIALS AND METHODS: We filmed quadrupedal locomotion in 11 platyrrhine species at field sites in Ecuador and Costa Rica and measured the diameter and orientation of locomotor substrates using remote sensors. We quantified limb phase values and classified strides by gait sequence type (N = 988 strides). RESULTS: Our results show that most of the species in our sample consistently used DS gaits, regardless of substrate diameter or orientation; however, all taxa also used asymmetrical and/or lateral sequence gaits. By incorporating phylogenetic eigenvectors into our models, we found significant differences in gait sequence patterns and limb phase values among the major platyrrhine clades, suggesting that phylogeny may be a better predictor of gait than substrate diameter or orientation. DISCUSSION: Our field data generally corroborate locomotor patterns from laboratory studies but capture additional aspects of gait variability and flexibility in response to the complexity of natural environments. Overall, our results suggest that DS gaits are not exclusively tailored to narrow or oblique substrates but are used on arboreal substrates in general.

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.

A Penalized Likelihood Framework for High-Dimensional Phylogenetic Comparative Methods and an Application to New-World Monkeys Brain Evolution.

Working with high-dimensional phylogenetic comparative data sets is challenging because likelihood-based multivariate methods suffer from low statistical performances as the number of traits $p $ approaches the number of species $n $ and because some computational complications occur when $p $ exceeds $n$. Alternative phylogenetic comparative methods have recently been proposed to deal with the large $p $ small $n $ scenario but their use and performances are limited. Herein, we develop a penalized likelihood (PL) framework to deal with high-dimensional comparative data sets. We propose various penalizations and methods for selecting the intensity of the penalties. We apply this general framework to the estimation of parameters (the evolutionary trait covariance matrix and parameters of the evolutionary model) and model comparison for the high-dimensional multivariate Brownian motion (BM), Early-burst (EB), Ornstein-Uhlenbeck (OU), and Pagel's lambda models. We show using simulations that our PL approach dramatically improves the estimation of evolutionary trait covariance matrices and model parameters when $p$ approaches $n$, and allows for their accurate estimation when $p$ equals or exceeds $n$. In addition, we show that PL models can be efficiently compared using generalized information criterion (GIC). We implement these methods, as well as the related estimation of ancestral states and the computation of phylogenetic principal component analysis in the R package RPANDA and mvMORPH. Finally, we illustrate the utility of the new proposed framework by evaluating evolutionary models fit, analyzing integration patterns, and reconstructing evolutionary trajectories for a high-dimensional 3D data set of brain shape in the New World monkeys. We find a clear support for an EB model suggesting an early diversification of brain morphology during the ecological radiation of the clade. PL offers an efficient way to deal with high-dimensional multivariate comparative data.

Early Arrival and Climatically-Linked Geographic Expansion of New World Monkeys from Tiny African Ancestors.

New World Monkeys (NWM) (platyrrhines) are one of the most diverse groups of primates, occupying today a wide range of ecosystems in the American tropics and exhibiting large variations in ecology, morphology, and behavior. Although the relationships among the almost 200 living species are relatively well understood, we lack robust estimates of the timing of origin, ancestral morphology, and geographic range evolution of the clade. Herein, we integrate paleontological and molecular evidence to assess the evolutionary dynamics of extinct and extant platyrrhines. We develop novel analytical frameworks to infer the evolution of body mass, changes in latitudinal ranges through time, and species diversification rates using a phylogenetic tree of living and fossil taxa. Our results show that platyrrhines originated 5-10 million years earlier than previously assumed, dating back to the Middle Eocene. The estimated ancestral platyrrhine was small-weighing 0.4 kg-and matched the size of their presumed African ancestors. As the three platyrrhine families diverged, we recover a rapid change in body mass range. During the Miocene Climatic Optimum, fossil diversity peaked and platyrrhines reached their widest latitudinal range, expanding as far South as Patagonia, favored by warm and humid climate and the lower elevation of the Andes. Finally, global cooling and aridification after the middle Miocene triggered a geographic contraction of NWM and increased their extinction rates. These results unveil the full evolutionary trajectory of an iconic and ecologically important radiation of monkeys and showcase the necessity of integrating fossil and molecular data for reliably estimating evolutionary rates and trends.

Contrasting patterns of RUNX2 repeat variations are associated with palate shape in phyllostomid bats and New World primates.

Establishing the genetic basis that underlies craniofacial variability in natural populations is one of the main topics of evolutionary and developmental studies. One of the genes associated with mammal craniofacial variability is RUNX2, and in the present study we investigated the association between craniofacial length and width and RUNX2 across New World bats (Phyllostomidae) and primates (Catarrhini and Platyrrhini). Our results showed contrasting patterns of association between the glutamate/alanine ratios (Q/A ratio) and palate shape in these highly diverse groups. In phyllostomid bats, we found an association between shorter/broader faces and increase of the Q/A ratio. In New World monkeys (NWM) there was a positive correlation of increasing Q/A ratios to more elongated faces. Our findings reinforced the role of the Q/A ratio as a flexible genetic mechanism that would rapidly change the time of skull ossification throughout development. However, we propose a scenario in which the influence of this genetic adjustment system is indirect. The Q/A ratio would not lead to a specific phenotype, but throughout the history of a lineage, would act along with evolutionary constraints, as well as other genes, as a facilitator for adaptive morphological changes.

The evolution of the platyrrhine talus: A comparative analysis of the phenetic affinities of the Miocene platyrrhines with their modern relatives.

Platyrrhines are a diverse group of primates that presently occupy a broad range of tropical-equatorial environments in the Americas. However, most of the fossil platyrrhine species of the early Miocene have been found at middle and high latitudes. Although the fossil record of New World monkeys has improved considerably over the past several years, it is still difficult to trace the origin of major modern clades. One of the most commonly preserved anatomical structures of early platyrrhines is the talus. This work provides an analysis of the phenetic affinities of extant platyrrhine tali and their Miocene counterparts through geometric morphometrics and a series of phylogenetic comparative analyses. Geometric morphometrics was used to quantify talar shape affinities, while locomotor mode percentages (LMPs) were used to test if talar shape is associated with locomotion. Comparative analyses were used to test if there was convergence in talar morphology, as well as different models that could explain the evolution of talar shape and size in platyrrhines. Body mass predictions for the fossil sample were also computed using the available articular surfaces. The results showed that most analyzed fossils exhibit a generalized morphology that is similar to some 'generalist' modern species. It was found that talar shape covaries with LMPs, thus allowing the inference of locomotion from talar morphology. The results further suggest that talar shape diversification can be explained by invoking a model of shifts in adaptive peak to three optima representing a phylogenetic hypothesis in which each platyrrhine family occupied a separate adaptive peak. The analyses indicate that platyrrhine talar centroid size diversification was characterized by an early differentiation related to a multidimensional niche model. Finally, the ancestral platyrrhine condition was reconstructed as a medium-sized, generalized, arboreal, quadruped.

Variation in ligand responses of the bitter taste receptors TAS2R1 and TAS2R4 among New World monkeys.

BACKGROUND: New World monkeys (NWMs) are unique in that they exhibit remarkable interspecific variation in color vision and feeding behavior, making them an excellent model for studying sensory ecology. However, it is largely unknown whether non-visual senses co-vary with feeding ecology, especially gustation, which is expected to be indispensable in food selection. Bitter taste, which is mediated by bitter taste receptors (TAS2Rs) in the tongue, helps organisms avoid ingesting potentially toxic substances in food. In this study, we compared the ligand sensitivities of the TAS2Rs of five species of NWMs by heterologous expression in HEK293T cells and calcium imaging. RESULTS: We found that TAS2R1 and TAS2R4 orthologs differ in sensitivity among the NWM species for colchicine and camphor, respectively. We then reconstructed the ancestral receptors of NWM TAS2R1 and TAS2R4, measured the evolutionary shift in ligand sensitivity, and identified the amino acid replacement at residue 62 as responsible for the high sensitivity of marmoset TAS2R4 to colchicine. CONCLUSIONS: Our results provide a basis for understanding the differences in feeding ecology among NWMs with respect to bitter taste.

Stem members of Platyrrhini are distinct from catarrhines in at least one derived cranial feature.

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.

Neotropics provide insights into the emergence of New World monkeys: New dental evidence from the late Oligocene of Peruvian Amazonia.

Recent field efforts in Peruvian Amazonia (Contamana area, Loreto Department) have resulted in the discovery of a late Oligocene (ca. 26.5 Ma; Chambira Formation) fossil primate-bearing locality (CTA-61). In this paper, we analyze the primate material consisting of two isolated upper molars, the peculiar morphology of which allows us to describe a new medium-sized platyrrhine monkey: Canaanimico amazonensis gen. et sp. nov. In addition to the recent discovery of Perupithecus ucayaliensis, a primitive anthropoid taxon of African affinities from the alleged latest Eocene Santa Rosa locality (Peruvian Amazonia), the discovery of Canaanimico adds to the evidence that primates were well-established in the Amazonian Basin during the Paleogene. Our phylogenetic results based on dental evidence show that none of the early Miocene Patagonian taxa (Homunculus, Carlocebus, Soriacebus, Mazzonicebus, Dolichocebus, Tremacebus, and Chilecebus), the late Oligocene Bolivian Branisella, or the Peruvian Canaanimico, is nested within a crown platyrrhine clade. All these early taxa are closely related and considered here as stem Platyrrhini. Canaanimico is nested within the Patagonian Soriacebinae, and closely related to Soriacebus, thereby extending back the soriacebine lineage to 26.5 Ma. Given the limited dental evidence, it is difficult to assess if Canaanimico was engaged in a form of pitheciine-like seed predation as is observed in Soriacebus and Mazzonicebus, but dental microwear patterns recorded on one upper molar indicate that Canaanimico was possibly a fruit and hard-object eater. If Panamacebus, a recently discovered stem cebine from the early Miocene of Panama, indicates that the crown platyrrhine radiation was already well underway by the earliest Miocene, Canaanimico indicates in turn that the "homunculid" radiation (as a part of the stem radiation) was well underway by the late Oligocene. These new data suggest that the stem radiation likely occurred in the Neotropics during the Oligocene, and that several stem lineages independently reached Patagonia during the early Miocene. Finally, we are still faced with a "layered" pattern of platyrrhine evolution, but modified in terms of timing of cladogeneses. If the crown platyrrhine radiation occurred in the Neotropics around the Oligocene-Miocene transition (or at least during the earliest Miocene), it was apparently concomitant with the diversification of the latest stem forms in Patagonia.

Formation of functional CENP-B boxes at diverse locations in repeat units of centromeric DNA in New World monkeys.

Centromere protein B, which is involved in centromere formation, binds to centromeric repetitive DNA by recognizing a nucleotide motif called the CENP-B box. Humans have large numbers of CENP-B boxes in the centromeric repetitive DNA of their autosomes and X chromosome. The current understanding is that these CENP-B boxes are located at identical positions in the repeat units of centromeric DNA. Great apes also have CENP-B boxes in locations that are identical to humans. The purpose of the present study was to examine the location of CENP-B box in New World monkeys. We recently identified CENP-B box in one species of New World monkeys (marmosets). In this study, we found functional CENP-B boxes in CENP-A-assembled repeat units of centromeric DNA in 2 additional New World monkeys (squirrel monkeys and tamarins) by immunostaining and ChIP-qPCR analyses. The locations of the 3 CENP-B boxes in the repeat units differed from one another. The repeat unit size of centromeric DNA of New World monkeys (340-350 bp) is approximately twice that of humans and great apes (171 bp). This might be, associated with higher-order repeat structures of centromeric DNA, a factor for the observed variation in the CENP-B box location in New World monkeys.

Lower molar shape and size in prosimian and platyrrhine primates.

The goal of this research is to evaluate the relative strength of the influences of diet, size, and phylogenetic signal on dental geometric shape. Accurate comprehension of these factors and their interaction is important for reconstructing diet and deriving characters for a cladistic analysis in fossil primates. Geometric morphometric analysis is used to identify axes of shape variation in the lower second molars of (a) prosimian primates and (b) platyrrhines. Landmarks were placed on µCT-generated surface renderings. Landmark configurations were aligned using generalized Procrustes analysis. Principal components analysis and phylogenetic principal components analysis (pPCA) were performed on species average landmark co-ordinates. pPCs were examined with phylogenetic generalized least squares analysis for association with size and with diet. PCs from both phylogenetic and non-phylogenetic analyses were sufficient to separate species by broad dietary categories, including insectivores and folivores. In neither analysis was pPC1 correlated with tooth size, but some other pPCs were significantly correlated with size. The pattern of association between pPCs and size altered when centroid size and dietary variables were combined in the model; effects of diet factors typically exceeded effects of size. These results indicate a dominant phylogenetic and dietary signal in molar shape but also show some shape change correlated with size in the absence of obvious dietary associations. Geometric morphometric analysis appears to be useful for tracking functional traits in molars, particularly in tracking differences between folivorous and insectivorous species.

First North American fossil monkey and early Miocene tropical biotic interchange.

New World monkeys (platyrrhines) are a diverse part of modern tropical ecosystems in North and South America, yet their early evolutionary history in the tropics is largely unknown. Molecular divergence estimates suggest that primates arrived in tropical Central America, the southern-most extent of the North American landmass, with several dispersals from South America starting with the emergence of the Isthmus of Panama 3-4 million years ago (Ma). The complete absence of primate fossils from Central America has, however, limited our understanding of their history in the New World. Here we present the first description of a fossil monkey recovered from the North American landmass, the oldest known crown platyrrhine, from a precisely dated 20.9-Ma layer in the Las Cascadas Formation in the Panama Canal Basin, Panama. This discovery suggests that family-level diversification of extant New World monkeys occurred in the tropics, with new divergence estimates for Cebidae between 22 and 25 Ma, and provides the oldest fossil evidence for mammalian interchange between South and North America. The timing is consistent with recent tectonic reconstructions of a relatively narrow Central American Seaway in the early Miocene epoch, coincident with over-water dispersals inferred for many other groups of animals and plants. Discovery of an early Miocene primate in Panama provides evidence for a circum-Caribbean tropical distribution of New World monkeys by this time, with ocean barriers not wholly restricting their northward movements, requiring a complex set of ecological factors to explain their absence in well-sampled similarly aged localities at higher latitudes of North America.

Brain shape convergence in the adaptive radiation of New World monkeys.

Primates constitute one of the most diverse mammalian clades, and a notable feature of their diversification is the evolution of brain morphology. However, the evolutionary processes and ecological factors behind these changes are largely unknown. In this work, we investigate brain shape diversification of New World monkeys during their adaptive radiation in relation to different ecological dimensions. Our results reveal that brain diversification in this clade can be explained by invoking a model of adaptive peak shifts to unique and shared optima, defined by a multidimensional ecological niche hypothesis. Particularly, we show that the evolution of convergent brain phenotypes may be related to ecological factors associated with group size (e.g., social complexity). Together, our results highlight the complexity of brain evolution and the ecological significance of brain shape changes during the evolutionary diversification of a primate clade.

New endemic platyrrhine humerus from Haiti and the evolution of the Greater Antillean platyrrhines.

Much debate surrounds the phylogenetic affinities of the endemic Greater Antillean platyrrhines. Thus far, most phylogenetic analyses have been constructed and tested using craniodental characters. We add to this dialog by considering how features of the distal humerus support or refute existing hypotheses for the origins of fossil Caribbean primates, utilizing three-dimensional geometric morphometric data in combination with character based cladistic analyses. We also add to the sample of fossil platyrrhine humeri with the description of UF 114718, a new distal humerus from Haiti. We reconstruct UF 114718 to be a generalized, arboreal quadruped attributed to the species Insulacebus toussantiana. Our results from phylogenetic analyses lend some support to the idea that some Greater Antillean fossil taxa including Xenothrix mcgregori, Antillothrix bernensis, and Insulacebus toussaintiana could form a monophyletic clade that is sister to either extant Platyrrhini or basal pitheciids. Based on the distal humeral data, we reconstruct the earliest ancestral platyrrhine to be a generalized, arboreal quadruped that potentially emphasized pronated arm postures during locomotion and may have engaged in some limited climbing, most similar in shape to early anthropoids and some of the earliest Antillean forms. However, aspects of shape and standard qualitative characters relating to the distal humerus seem to be variable and prone to both homoplasy and reversals; thus these results must be interpreted cautiously and (where possible) within the context provided by other parts of the skeleton.