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The evolution of the platyrrhine talus: A comparative analysis of the phenetic affinities of the Miocene platyrrhines with their modern relatives
Abstract
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.
Supplementary resources (3)
Data
October 2017
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October 2017
... In agreement with the traditional linear metrics described above, new techniques of whole-bone shape comparative morphometry have also supported an association between talar shape and locomotion behavior. In a study of platyrrhines, Püschel et al. (2017) demonstrated that the most suspensory species had features related to highly flexible subtalar and transverse tarsal joints: a broader talar head, greater trochlear wedging, a longer trochlea and a shorter anterior, and longer posterior calcaneal facet Figs. 3.5 and 3.6). ...
... Comparisons across subspecies of gorillas also suggest that talar shape differs in response to foot posture use on different substrates (Dunn et al., 2014;Knigge et al., 2015). Western lowland (Gorilla gorilla gorilla) and Cross River (G. g. diehli) gorillas, who may spend more time climbing with their foot in an inverted position (for the sole of their foot to be directed medially so that it can wrap around the tree trunk), have more mediolateral curvature of the talar trochlea and relative surface Püschel et al. (2017) area of the lateral malleolus than Eastern mountain (G. beringei beringei) and Grauer (G. ...
... Phylomorphospace of extant platyrrhine tali. Reproduced with permission fromPüschel et al. (2017) ...
The primate hindfoot consists of only two bones—the talus (ankle) and the calcaneus (heel bone). Yet, the hindfoot is a keystone of the foot that serves as a lever for multiple muscles. While many bony features of the hindfoot have been found to significantly covary with locomotor behavior, they also show a significant phylogenetic signal, indicating that closely related species tend to show similar traits due to common ancestry. As such, the hindfoot has been one of the most informative and diagnostic features for understanding foot function and inferring behavior in both extant and extinct primates.In this chapter, we discuss the anatomy of the hindfoot
from a proximal to distal direction, beginning with the distal tibia and fibula, passing through the talus
, and finally to the calcaneus
. We highlight the fact that, compared with other mammals, primates are characterized by elongation of the tarsal elements, including the neck of the talus
and distal calcaneus
. These traits are believed to relate to pedal grasping
and powerful leaping, locomotor behaviors which may have been important for the earliest euprimates. We compare the whole-bone morphology, projections and articular facets, and internal trabecular microstructure of each hindfoot
bone across primate species and locomotor mode.KeywordsTalusCalcaneusNavicularExternal anatomyFunctional anatomyJointsHindfootSubtalar jointCalcaneocuboid jointTalocrural jointTalonavicular jointHeelAchilles tendon
... Additionally, it remains unclear whether the older P. marianae exhibited any semi-terrestrial adaptations. Recently, Püschel et al. (2017Püschel et al. ( , 2018 inferred the main locomotor behavior of P. marianae as one comparable to alouattines (i.e., exhibiting different levels of arboreal quadrupedalism, clambering and climbing), but it is important to bear in mind that they were not able to rule out possible semi-terrestrial adaptations, since they had not consider this category in their analyses. ...
... They found that Paralouatta's talus is particularly distinct from the tali of other New World monkeys, especially because the absence of trochlear "wedging" distinguishes Paralouatta from all other large New World monkeys. In contrast, Püschel et al. (2017) performed a PCA of landmark data using geometric morphometrics (GM) and found that Paralouatta occupied a position in the resulting morphospace near Alouatta, as well as to some of the oldest platyrrhines from Patagonia (i.e., Dolichocebus, Soriacebus, and Carlocebus). Similarly, they applied a hierarchical clustering analysis that placed this fossil near Cebus/Sapajus and Dolichocebus, Soriacebus, and Carlocebus, hence showing that, at least from a morphological perspective, the talus of Paralouatta is not as unusual as initially thought (Püschel et al., 2017). ...
... In contrast, Püschel et al. (2017) performed a PCA of landmark data using geometric morphometrics (GM) and found that Paralouatta occupied a position in the resulting morphospace near Alouatta, as well as to some of the oldest platyrrhines from Patagonia (i.e., Dolichocebus, Soriacebus, and Carlocebus). Similarly, they applied a hierarchical clustering analysis that placed this fossil near Cebus/Sapajus and Dolichocebus, Soriacebus, and Carlocebus, hence showing that, at least from a morphological perspective, the talus of Paralouatta is not as unusual as initially thought (Püschel et al., 2017). ...
Currently, there are no living platyrrhine primates inhabiting the main Caribbean islands. Nevertheless, the fossil record of this area has provided outstanding findings of different New World monkeys that were part of a diverse radiation exhibiting remarkably unusual morphologies. Among these, the Cuban genus Paralouatta corresponds to one of the most enigmatic primates ever found in the Greater Antilles. Some researchers have argued that Paralouatta’s post-cranium shows evidence of semi-terrestriality, a locomotor adaptation that is unusual, if not unique, in platyrrhine evolutionary history. Whether or not Paralouatta was truly semi-terrestrial remains uncertain, however, due to a lack of more sophisticated functional analyses on its morphology. Using novel virtual morpho-functional techniques on a comparative sample of 3D talar models belonging to diverse primate species representing three substrate preferences, this study aims to further evaluate whether Paralouatta was a semi-terrestrial genus or not. Geometric morphometrics and finite element analysis were used to empirically assess shape and biomechanical performance, respectively, and then several machine-learning (ML) classification algorithms were trained using both morphometric and biomechanical data to elucidate the substrate preference of the fossils. The ML algorithms categorized the Paralouatta specimens as either arboreal or as species commonly active on both ground and in trees. These mixed results are suggestive of some level of semi-terrestriality, thus representing the only known example of this locomotor behavior in platyrrhine evolutionary history.
... After teeth, the talus is probably the most commonly preserved anatomical element in the platyrrhine fossil record [3], with several Miocene taxa possessing at least one conserved talus [6]. Importantly, talar morphology can provide insights about postural adaptations due to its interconnection with other foot bones [7,8]. ...
... There is a strong and significant association between talar shape and locomotor behaviour [6], and evidence shows that bone is functionally adapted to the mechanical demands that are imposed during life [11]. Therefore, it is logical to hypothesize that talar mechanical strength associated with biomechanical performance could also be used to distinguish and infer locomotor behaviours. ...
... Extant body mass data were obtained from Smith & Jungers [27], while the fossil body mass predictions were obtained from Pü schel et al. [6]. Among living platyrrhine species, male and female body mass are highly correlated [29]; therefore, average body mass was used in the subsequent analyses (tables 1 and 2). ...
The talus is one of the most commonly preserved post-cranial elements in the platyrrhine fossil record. Talar morphology can provide information about postural adaptations because it is the anatomical structure responsible for transmitting body mass forces from the leg to the foot. The aim of this study is to test whether the locomotor behaviour of fossil Miocene platyrrhines could be inferred from their talus morphology. The extant sample was classified into three different locomotor categories and then talar strength was compared using finite-element analysis. Geometric morphometrics were used to quantify talar shape and to assess its association with biomechanical strength. Finally, several machine-learning (ML) algorithms were trained using both the biomechanical and morphometric data from the extant taxa to infer the possible locomotor behaviour of the Miocene fossil sample. The obtained results show that the different locomotor categories are distinguishable using either biomechanical or morphometric data. The ML algorithms categorized most of the fossil sample as arboreal quadrupeds. This study has shown that a combined approach can contribute to the understanding of platyrrhine talar morphology and its relationship with locomotion. This approach is likely to be beneficial for determining the locomotor habits in other fossil taxa.
... In a study focusing on fossils that sampled almost all living genera, Püschel et al. (2017) examined the 3DGM phenetics and phylogenetic significance of the platyrrhine talus using methods comparable to those of Aristide et al. (2016) and Tallman and Cooke (2016). The phenetic results contained in the informative first two PC axes showed Aotus overlapping with the morphology of Saimiri, Cebus, and Cacajao among the living forms (Fig. 4.12). ...
... Originally conceived (Rosenberger 1980) as a twozone ecological model that emphasized the insectivory vs. folivory options as major sources of dietary protein (Kay 1975), the significance of proteinaceous seeds was later recognized as a vital, phylogenetically and cladistically important strategy (Rosenberger 1992), leading to the understanding that the three main groups focus on either insects/fauna, leaves, or seeds as critical staple foods (Rosenberger 2020) in conjunction with their elemental adaptations to frugivory. Other studies employing a range of morphological evidence, genetics, fossils, and sophisticated evolutionary models looking at the processes of historical change (Perez et al. 2012;Aristide et al. 2016;Püschel et al. 2017) have corroborated the three-clade, threezone, ecological model. Having said that, another way of looking at the ecophylogenetic model is to consider what has not happened. ...
Phylogeny reconstruction is an estimation of genealogical history, not an exact rendering of it, and no method of phylogeny reconstruction is infallible. The cladistic relationships of the owl monkey, Aotus, are the most hotly contested node of New World monkey interrelationships. The alternative hypotheses can be described taxonomically: Aotus is monophyletically related to either cebids or pitheciids. As predictive propositions, each notion should be evaluated by its explanatory power. The cebid hypothesis predicts that Aotus broadly shares adaptations in morphology, behavior, and ecology with cebines and/or callitrichines, while the pitheciid hypothesis predicts extensive overlap with Callicebus and/or pitheciins. We find no support for the cebid hypothesis and commanding support for the pitheciid hypothesis in the form of integrated morphological and behavioral complexes that are likely to be homologously derived. More attention should be directed toward understanding why the morphology and molecules do not align, from both biological and methodological perspectives.
... of the bone have received considerable attention in several areas of research and practice. In biological anthropology, it is believed that anatomic variations of the talus provide information on foot function, postural and locomotor adaptations, and timing/sequence of functional evolution in the foot of human-like terrestrials (Knigge et al., 2015;Parr et al., 2014;Püschel et al., 2017;Sorrentino et al., 2020;Turley & Frost, 2013). From diagnostic perspectives, knowledge of anatomic variations of normal tali helps diagnosis of the bone pathologies (Feng et al., 2018;Seki et al., 2019;Tümer et al., 2016;Tümer, Vuurberg, et al., 2019). ...
... Visual recognition of biological LMs, that is, juxtapositions of tissues (denoted as type-I Bookstein, 1991;Cooke & Terhune, 2015) on the three-dimensional (3D) surface (particularly a digitized/ scanned surface) of the talus is difficult and non-reliable. Therefore, mathematical LMs and/or semi (pseudo) LMs have been utilized (Bookstein, 1991;Knigge et al., 2015;Püschel et al., 2017;Sorrentino et al., 2020;Turley & Frost, 2013). Mathematical LMs include type-II (extrema of curvature), type-III (extremal points or points defined based on the locations of other points); and semi LMs are points that are distributed (typically equally spaced) between the biological or mathematical LMs (Cooke & Terhune, 2015). ...
Statistical data pertaining to anatomic variations of the human talus contain valuable information for advances in biological anthropology, diagnosis of the talar pathologies, and designing talar prostheses. A statistical shape model (SSM) can be a powerful data analysis tool for the anatomic variations of the talus. The main concern in constructing an SSM for the talus is establishing the true geometric correspondence between the talar geometries. The true correspondence complies with biological and/or mathematical homologies on the talar surfaces. In this study, we proposed a semi-automatic approach to establish a dense correspondence between talar surfaces discretized by triangular meshes. Through our approach, homologous salient surface features in the form of crest lines were detected on 49 talar surfaces. Then, the point-wise correspondence information of the crest lines was recruited to create posterior Gaussian process morphable models that non-rigidly registered the talar meshes and consequently established inter-mesh dense correspondence. The resultant correspondence perceptually represented the true correspondence as per our visual assessments. Having established the correspondence, we computed the mean shape using full generalized Procrustes analysis and constructed an SSM by means of principal component analysis. Anatomical variations and the mean shape of the talus were predicted by the SSM. As a clinically related application, we considered the mean shape and investigated the feasibility of designing universal talar prostheses. Our results suggest that the mean shape of (the shapes of) tali can be used as a scalable shape template for designing universal talar prostheses.
... Neotropical primates, or New World monkeys, are non-human primates inhabiting Central and South America (NPC, 2021). They are also known as platyrrhines and include 139 species that occupy a wide range of tropical environments in the American continent (Püschel et al., 2017;NPC, 2021). These species are commonly traded illegally in Central and South America (Duarte-Quiroga and Estrada, 2003). ...
Thousands of trafficked Neotropical primates enter Latin American wildlife rehabilitation centres every year. There is a lack of research related to their health and behaviour and how these relate to personality. Moreover, the ethical issues on their reintroduction have not been discussed. The first aim of this dissertation was to investigate the health of capuchin monkeys in two Brazilian rescue centres and obtain their haematological and physiological values and parasitological status. Results showed that they had similar physiological and haematological values to previously published data. Five individuals were positive to Ancylostoma spp. The second aim was to analyse the behaviour of the capuchins to provide an initial assessment of their rehabilitation. This was performed by using changes in behaviours (activity budgets) and a behavioural diversity index. When comparing the baseline and final observational phases, behavioural diversity, affiliative behaviours and inactivity increased whilst human interaction decreased. The third aim was to assess the personality structure of the capuchins by utilising behavioural observations, tests and observer trait ratings. Four dimensions were obtained from trait ratings (Openness, Neuroticism, Assertiveness and Sociability) and five from tests (creative, aggressive, stereotypic, sociable to humans and risk-averse). The fourth aim was to investigate the association between personality and health (body condition and neutrophil-to-lymphocyte ratios) of the individuals. There was a significant negative correlation between Sociability and neutrophil-to-lymphocyte ratios and between stress-related behaviours and body condition. The fifth aim was to investigate the association of personality with behavioural changes during rehabilitation. Results suggested stereotypy, aggression and Assertiveness influenced vigilance behaviours and Neuroticism influenced space and substrate use. The sixth aim was to analyse the ethical issues related to the reintroduction of trafficked Neotropical primates. I developed an Ethical Matrix and suggested a set of recommendations as guidelines that may be used when confronted with these issues.
... Platyrrhines are commonly kept as pets in Latin American countries (Nunes et al., 2021). Platyrrhines inhabit Central and South America and include 204 taxa that occupy a wide range of tropical environments (Mittermeier et al., 2013;Püschel et al., 2017). Platyrrhine species accounted for approximately 4% of live primates traded between 2005 and 2014 (Estrada et al., 2017) and are frequently traded in Central and South America, including countries, such as Mexico, Peru, and Brazil (Duarte-Quiroga & Estrada, 2003;de Souza Fialho et al., 2016;Mitman et al., 2021;Nunes et al., 2021). ...
The illegal primate trade is one of the major drivers of the decline of nonhuman primate populations and a threat to their wellbeing. Thousands of trafficked primates enter rescue centers every year, and their destiny (release back into the wild, long-term captivity, or euthanasia) involves controversial decisions and complex ethical considerations. To navigate these issues, we developed an ethical matrix, an ethical framework previously used to address conservation-related issues. We gathered information from studies on the reintroduction of trafficked platyrrhines in Latin America from 1990 to 2022 to develop the matrix. We found 22 studies performed in eight Latin American countries, which included howler monkeys, spider monkeys, woolly monkeys, capuchin monkeys, squirrel monkeys, marmosets, and tamarins. We found that the reintroduction of trafficked platyrrhines may yield positive results for the welfare of individuals and for the conservation of their taxa and some of the potential negative effects, such as spillover of infectious agents to free-ranging populations or to human populations, or competition for resources between reintroduced monkeys and resident conspecifics have not yet been documented in the scientific literature, although this does not mean that they do not occur. We conclude that the ethical matrix is a useful method to consider the interests of all potential stakeholders and that the reintroduction of trafficked primates may be a viable management option if the individual welfare of the animals is considered, programs comply with the IUCN and government guidelines, and the objective and justification of the reintroduction are clear.
... Talar and calcaneal morphologies indicative of leaping and arboreal quadrupedalism largely overlapped for all primates included in this sample and only separated among locomotor groups within taxonomic groups (Figs. 3 and 9). It is well established that morphological differences among species are due to a combination of phylogenetic history and other variables, including locomotor behavior and body mass (e.g., Szalay and Dagosto, 1980;Demes and Günther, 1989;Demes and Jungers, 1993;Püschel et al., 2017;Granatosky, 2018). Our PC variables capture both types of traits: those with a strong phylogenetic signal and those with a strong functional signal. ...
Early Eocene primate postcranial bones from the Vastan lignite mine of Gujarat, India, have proven useful for understanding the haplorhine and strepsirrhine divergence. Previous analyses of material assigned to Asiadapidae supported interpretations that these primates were generalized arboreal quadrupeds, while the omomyid Vastanomys was likely to have been more proficient leaper than asiadapids. More recent examinations of long bone cross-sectional properties and calcaneal elongation have complicated the behavioral interpretations of these fossils. This study examines whole talar and calcaneal morphology of the Vastan material to refine the locomotor reconstructions of these fossils. A comparative sample of extant primate species representing various locomotor behaviors was obtained by accessing surface models from MorphoSource.org. Surface models of fossil specimens attributed to Asiadapis cambayensis, Marcgodinotius indicus, and Vastanomys major were generated from micro-computed tomography scans. A morphological analysis was carried out using weighted spherical harmonics, a Fourier-based method that represents surfaces using coefficients associated with a common set of spherical harmonic functions. The coefficients describing each surface were then used as shape variables in a principal components analysis. Significant differences between locomotor groups were assessed using nonparametric tests. Results from extant comparative samples show that locomotor behavior can be predicted from both talar and calcaneal morphology when phylogenetic relationships are known. Consistent with previous analyses, our results indicate that Asiadapis cambayensis and Marcgodinotius indicus were likely arboreal quadrupeds with some leaping capabilities. Vastanomys major is reconstructed as an arboreal quadruped with greater leaping proficiency than its asiadapid counterparts based on its talar morphology.
... We used linear regressions to model the relationship between IMI and each of the environmental measures. We also assessed the strength of phylogenetic signal in IMI under a recent primate phylogenetic hypothesis (Sehner et al., 2018;Püschel et al., 2017;Aristide et al., 2015). Phylogenetic signal was estimated using Pagel's lambda with the function phylosig in the R package phytools (Revell, 2012) and phylogenetic data data downloaded from VertLife (a maximum clade credibility tree derived from a random sample of 500 trees, Upham et al. (2019); http://vertlife.org/). ...
Ecometric modelling assesses how the functional morphology of ecogeographic communities relates to environmental variables. This improves understanding of how the interaction between organism and environment can result in morphological adaptation. This technique has mainly been used to model paleoenvironments, but has the capacity to aid conservation by quantifying how communities are structured through space and time. Here we test the relationship between limb proportions and the habitat ecology of South American non-human primates. There is a significant but weak fit between limb proportions and habitat, consistent with the environment exerting weak selective pressure on limb proportions. In contrast, body size and phylogeny are strongly correlated with IMI. Together, these findings suggest that habitat was a selection pressure that shaped how New World monkeys' limb proportions evolved but this selection pressure was secondary to that of body size. Research into these functional relationships is important not only to improve scientific understanding of their evolutionary pathways but also in order to aid their protection by informing conservation practices. Ensuring these species have the capacity to move with their niche is an immediate concern, as they face mounting pressure due to deforestation of the Amazon basin.
... We used linear regressions to model the relationship between IMI and each of the environmental measures. We also assessed the strength of phylogenetic signal in IMI under a recent primate phylogenetic hypothesis (Sehner et al., 2018;Püschel et al., 2017;Aristide et al., 2015). Phylogenetic signal was estimated using Pagel's lambda with the function "phylosig" in the R package "phytools" (Revell, 2012) and phylogenetic data downloaded from VertLife (a maximum clade credibility tree derived from a random sample of 500 trees, Upham et al., 2019; http://vertlife.org/). ...
Ecometric modelling assesses how the functional morphology of ecogeographic communities relates to environmental variables. This improves understanding of how the interaction between organism and environment can result in morphological adaptation. This technique has mainly been used to model paleoenvironments, but has the capacity to aid conservation by quantifying how communities are structured through space and time. Here, we test the relationship between limb proportions and the habitat ecology of South American non-human primates. There is a significant but weak fit between limb proportions and habitat, consistent with the environment exerting weak selective pressure on limb proportions. In contrast, body size and phylogeny are strongly correlated with IMI. Together, these findings suggest that habitat was a selection pressure that shaped how New World monkeys' limb proportions evolved but this selection pressure was secondary to that of body size. Research into these functional relationships is important not only to improve scientific understanding of their evolutionary pathways but also in order to aid their protection by informing conservation practices. Ensuring these species have the capacity to move with their niche is an immediate concern, as they face mounting pressure due to deforestation of the Amazon basin.
... Talar and calcaneal morphologies indicative of leaping and arboreal quadrupedalism largely overlapped for all primates included in this sample and only separated among locomotor groups within taxonomic groups (Figs. 3 and 9). It is well established that morphological differences among species are due to a combination of phylogenetic history and other variables, including locomotor behavior and body mass (e.g., Szalay and Dagosto, 1980;Demes and Günther, 1989;Demes and Jungers, 1993;Püschel et al., 2017;Granatosky, 2018). Our PC variables capture both types of traits: those with a strong phylogenetic signal and those with a strong functional signal. ...
Postcrania dating back to the early Eocene from the Cambay Shale Formation of Gujarat, India, provide a unique window for understanding early primate behavior. Previous metric analyses of postcrania assigned to Asiadapinae indicate that these primates were generalized arboreal quadrupeds. Examination of long bone cross‐sectional properties, however, complicates the initial behavioral interpretations because it shows that these fossils overlap with primates of differing locomotor behaviors. The purpose of this study is to re‐examine calcaneal morphology of the Indian material in order to refine the locomotor reconstructions of these fossils.
Surface models of fossil calcanei (n=6) were generated from micro‐computed tomography scans while those (n=73) representing 23 extant primate species were downloaded from MorphoSource. A weighted spherical harmonics analysis was carried out on the total sample. This morphological analysis represents genus‐zero surfaces using a common set of spherical harmonic functions. The harmonic coefficients associated with each calcaneus serve as shape descriptors that can be summarized via principal components (PC) analysis. Bivariate plots and models representing plus and minus two standard deviations of each PC were created to visualize morphological differences.
The first three PCs explain 52.4%, 9.7%, and 9.3% of the morphological variation in the sample respectively (71.4% combined). The first PC differentiates primates with elongated calcanei that are more likely to engage in vertical clinging and leaping, from more quadrupedal primates. The second PC distinguishes calcanei of slow climbers from primates that engage in other forms of locomotion (e.g., leaping and quadrupedalism). Extant primate morphology seems to follow a continuum in which relative anteroposterior calcaneal elongation negatively correlates with slow climber calcaneal morphology. As expected, the calcaneal morphology of Marcgodinotius indicus aligns with that of extant lemuriforms, and most closely resembles that of a generalized arboreal quadruped with some leaping ability. There are two fossils tentatively attributed to Asiadapis cambayensis included in the analysis. One groups with other generalized arboreal quadrupeds, while the other falls outside the range of calcaneal variation observed in extant primates. The outlier does not follow the general pattern of calcaneal morphology observed in extant primates; instead it is characterized by some aspects of slow climber morphology, but with a relative anteroposterior calcaneal elongation. These results may reflect the generalized morphology of this fossil, and consequently the behavior of this primitive euprimate.
Support or Funding Information
Supported by NSF DGE‐1746891, National Geographic Society, Leakey Foundation
... The results of this study show the importance of considering both extant and fossil species when exploring diversification in complex traits, such as endocranial and cranial shape variation. Several recent studies analyzed cranial and mandibular shape variation in extant and fossil species of primates and other mammalian clades (e.g., Alvarez, Perez, & Verzi, 2011;Fleagle et al., 2016;Gunz et al., 2009;Püschel, Gladman, Bobe, & Sellers, 2017;Rocatti et al., 2017), and they also show the importance of fossil variation for understanding clade evolution. In particular, the joint use of data from fossil and extant species allows us to consider variation from periods predating or concomitant with events of mass extinction. ...
Objectives
Platyrrhines constitute a diverse clade, with the modern Atelidae exhibiting the most variation in cranial and endocast morphology. The processes responsible for this diversification are not well understood. Here, we present a geometric morphometric study describing variation in cranial and endocranial shape of 14 species of Alouatta, Ateles, Brachyteles, and Lagothrix and two extinct taxa, Cartelles and Caipora.
Methods
We examined cranial and endocranial shape variation among species using images reconstructed from CT scans and geometric morphometric techniques based on three‐dimensional landmarks and semilandmarks. Principal components analyses were used to explore variation, including the Procrustes shape coordinates, summing the logarithm of the Centroid Size, the common allometric component, and residual shape components.
Results
Differences in endocranial shape are related to a relative increase or decrease in the volume of the neocortex region with respect to brainstem and cerebellum regions. The relative position of the brainstem varies from a posterior position in Alouatta to a more ventral position in Ateles. The shape of both the cranium and endocast of Caipora is within the observed variation of Brachyteles. Cartelles occupies the most differentiated position relative to the extant taxa, especially in regards to its endocranial shape.
Conclusions
The pattern of variation in the extant species in endocranial shape is similar to the variation observed in previous cranial studies, with Alouatta as an outlier. The similarities between Caipora and Brachyteles were unexpected and intriguing given the frugivorous adaptations inferred from the fossil's dentition. Our study shows the importance of considering both extant and fossil species when studying diversification of complex traits.
... Some skepticism regarding the use of casts, even high-resolution, research-quality casts like those used here, is warranted. The use of 3D models derived from casts remains common, however (see refs [45][46][47][48][49][50] for recent examples). Extant models were processed and smoothed to correct imperfections stemming from the scanning process, osteochondral defects, or other issues of pathology or preservation to ensure comparability across the sample. ...
... Some skepticism regarding the use of casts, even high-resolution, research-quality casts like those used here, is warranted. The use of 3D models derived from casts remains common, however (see refs [45][46][47][48][49][50] for recent examples). Extant models were processed and smoothed to correct imperfections stemming from the scanning process, osteochondral defects, or other issues of pathology or preservation to ensure comparability across the sample. ...
Considerable taxonomic diversity has been recognised among early Miocene catarrhines (apes, Old World monkeys, and their extinct relatives). However, locomotor diversity within this group has eluded characterization, bolstering a narrative that nearly all early catarrhines shared a primitive locomotor repertoire resembling that of the well-described arboreal quadruped Ekembo heseloni. Here we describe and analyse seven catarrhine capitates from the Tinderet Miocene sequence of Kenya, dated to ~20 Ma. 3D morphometrics derived from these specimens and a sample of extant and fossil capitates are subjected to a series of multivariate comparisons, with results suggesting a variety of locomotor repertoires were present in this early Miocene setting. One of the fossil specimens is uniquely derived among early and middle Miocene capitates, representing the earliest known instance of great ape-like wrist morphology and supporting the presence of a behaviourally advanced ape at Songhor. We suggest Rangwapithecus as this catarrhine’s identity, and posit expression of derived, ape-like features as a criterion for distinguishing this taxon from Proconsul africanus. We also introduce a procedure for quantitative estimation of locomotor diversity and find the Tinderet sample to equal or exceed large extant catarrhine groups in this metric, demonstrating greater functional diversity among early catarrhines than previously recognised.
... Scatterplots were computed in R (R Core Team). Finally, we subjected the group mean configurations to a new GPA and computed dendrograms for morphological affinity using UPGMA and Ward's method as recommended for morphometric data (Hammer and Harper, 2008;Püschel et al., 2017). Euclidean distances were used as a similarity index. ...
Most authors recognize six baboon species: hamadryas (Papio hamadryas), Guinea (Papio papio), olive (Papio anubis), yellow (Papio cynocephalus), chacma (Papio ursinus), and Kinda (Papio kindae). However, there is still debate regarding the taxonomic status, phylogenetic relationships, and the amount of gene flow occurring between species. Here, we present ongoing research on baboon morphological diversity in Gorongosa National Park (GNP), located in central Mozambique, south of the Zambezi River, at the southern end of the East African Rift System. The park exhibits outstanding ecological diversity and hosts more than 200 baboon troops. Gorongosa National Park baboons have previously been classified as chacma baboons (P. ursinus). In accordance with this, two mtDNA samples from the park have been placed in the same mtDNA clade as the northern chacma baboons. However, GNP baboons exhibit morphological features common in yellow baboons (e.g., yellow fur color), suggesting that parapatric gene flow between chacma and yellow baboons might have occurred in the past or could be ongoing. We investigated the phenostructure of the Gorongosa baboons using two approaches: 1) description of external phenotypic features, such as coloration and body size, and 2) 3D geometric morphometric analysis of 43 craniofacial landmarks on 11 specimens from Gorongosa compared to a pan-African sample of 352 baboons. The results show that Gorongosa baboons exhibit a mosaic of features shared with southern P. cynocephalus and P. ursinus griseipes. The GNP baboon phenotype fits within a geographic clinal pattern of replacing allotaxa. We put forward the hypothesis of either past and/or ongoing hybridization between the gray-footed chacma and southern yellow baboons in Gorongosa or an isolation-by-distance scenario in which the GNP baboons are geographically and morphologically intermediate. These two scenarios are not mutually exclusive. We highlight the potential of baboons as a useful model to understand speciation and hybridization in early human evolution.
... Estudios referidos a la evolución de los Platyrrhini muestran como el comportamiento locomotor influyó en la morfología del talus en este parvorder (Püschel et al., 2017); observándose en el presente estudio que el esqueleto de Callimico goeldii tiene proporciones que difieren de otras especies de la misma familia. Las mediciones indicaron que brazos, piernas y pies se encuentran por debajo de las proporciones descritas por Ankel-Simons (2007), concluyendo que los miembros de esta especie son más cortos. ...
El estudio tuvo como objetivo describir radiológicamente la osteología del mono tití de Goeldi (Callimico goeldii). Se emplearon cinco individuos en estado de cautiverio, en aparente buen estado de salud, del Parque Zoológico Huachipa (Lima, Perú). Se les realizó un examen clínico previo para constatar el buen estado de salud. Los animales fueron anestesiados y posicionados en decúbito dorsal y lateral para la evaluación radiológica. Asimismo, se obtuvo vistas del esqueleto apendicular y se hizo un registro de distintos valores de exposición para determinar los valores óptimos de estos. Los resultados mostraron que los valores de exposición óptimos para obtener imágenes radiográficas en esta especie para cabeza y tórax-abdomen fueron en posición dorso ventral y lateral 50Kv, 20 mA, 0.03s y para las extremidades en vista medio lateral de 50 kV, 20 mA, 0.02 s. Se evidenció que la tibia y el peroné se encuentran fusionados en su tercio inferior y poseen una curvatura hacia distal, ancho máximo de la pelvis es a nivel de las eminencias iliopúbicas, y las proporciones de las cuatro extremidades de esta especie son menores a las proporciones de otros primates neotropicales. Del presente estudio se puede concluir que existen diferencias morfológicas a nivel de la pelvis y las extremidades posteriores con relación a otras especies de primates, posiblemente debidas al patrón de locomoción por saltos verticales en Callimico goeldii.
The lower molars of the early Miocene New World monkey Dolichocebus gaimanensis from Patagonia, considered by some to be a stem platyrrhine, are for all intents and purposes indistinguishable from the same teeth preserved in the type specimen of the middle Miocene Laventiana annectens from Colombia. Canine morphology further indicates that Dolichocebus is a cebine, closely related to living Saimiri. The phenetic and phyletic continuity of these extinct species, here classified as congeners, means they are the first fossil platyrrhines that link South America’s southern and northern Miocene monkey faunas, possibly as vicariant communities or with ancestral-descendant species that evolved by phyletic evolution. These findings further refute the hypothesis that early Miocene platyrrhines are (1) monophyletic and (2) outside the so-called crown platyrrhine radiation. The connection between these species is additional evidence supporting the hypothesis that the pattern of platyrrhine evolution is notably distinct for the predominance of low-level taxonomic clades (genera, tribes, subfamilies) of prolonged ecophylogenetic stability, which is the essence of the Long-Lineage Hypothesis.
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.
Significance
The evolutionary diversification of brain morphology is one of the most prominent features of the primate adaptive radiation and a likely determinant of primate evolutionary success. However, the ecological factors responsible for the diversification of the primate brain are largely unknown. In this work, we use a comparative approach to study brain diversification during the adaptive radiation of a major primate clade—the New World monkeys. We show that brain morphology evolved in association with the occupation of several ecological niches, and that convergence in brain morphology among clades may be associated with an evolutionary increase in the complexity of social behaviors.
A dataset of high-resolution microCT scans of primate skulls (crania and mandibles) and certain postcranial elements was collected to address questions about primate skull morphology. The sample consists of 489 scans taken from 431 specimens, representing 59 species of most Primate families. These data have transformative reuse potential as such datasets are necessary for conducting high power research into primate evolution, but require significant time and funding to collect. Similar datasets were previously only available to select research groups across the world. The physical specimens are vouchered at Harvard's Museum of Comparative Zoology. The data collection took place at the Center for Nanoscale Systems at Harvard. The dataset is archived on MorphoSource.org. Though this is the largest high fidelity comparative dataset yet available, its provisioning on a web archive that allows unlimited researcher contributions promises a future with vastly increased digital collections available at researchers' finger tips.
The anthropoids from the Fayum Province, Egypt, represent the best-preserved and most diverse assemblage of early anthropoids found anywhere in the world. However, the best known of the Fayum primates—Aegyptopithecus zeuxis, Propliopithecus chirabates, Apidium phiomense, and Parapithecus grangeri— occur near the top of the 340m-deep Jebel Qatrani Formation (Simons, 1965, 1967, 1974, 1987; Kay, 1977; Fleagle and Simons, 1978, 1982a,b; Gebo and Simons, 1987; Kay et al., 1981; Fleagle and Kay, 1983, 1985, 1987). Fossil primates millions of years older have been found at lower stratigraphic levels, and these older species differ appreciably from the primates of the uppermost quarries, reflecting significant evolutionary changes that took place during the time represented by the deposition of the Jebel Qatrani Formation (Simons, 1962; Simons and Kay, 1983; Rasmussen and Simons, 1988). The oldest primates yet found in the Fayum have been described recently on the basis of dental and cranial specimens found at quarry L-41, which lies near the base of the Jebel Qatrani Formation (Simons, 1989, 1990, 1992; Rasmussen and Simons, 1992). These L-41 primates are among the most ancient and structurally most primitive anthropoids found anywhere in the world.
Phenotype-environment correlations and the evolution of trait interactions in adaptive radiations have been widely studied to gain insight into the dynamics underpinning rapid species diversification. In this study we explore the phenotype-environment correlation and evolution of operculum shape in cichlid fishes using an outline-based geometric morphometric approach combined with stable isotope indicators of macrohabitat and trophic niche. We then apply our method to a sample of extinct saurichthyid fishes, a highly diverse and near globally distributed group of actinopterygians occurring throughout the Triassic, to assess the utility of extant data to inform our understanding of ecomorphological evolution in extinct species flocks. A series of comparative methods were used to analyze shape data for 54 extant species of cichlids (N = 416), and 6 extinct species of saurichthyids (N = 44). Results provide evidence for a relationship between operculum shape and feeding ecology, a concentration in shape evolution towards present along with evidence for convergence in form, and significant correlation between the major axes of shape change and measures of gut length and body elongation. The operculum is one of few features that can be compared in extant and extinct groups, enabling reconstruction of phenotype-environment interactions and modes of evolutionary diversification in deep time.
Mohanamico hershkovitzi was about the size of the living squirrel monkey Saimiri sciureus. Its molars are low-crowned and the molar crests are not pronounced suggesting a frugivorous diet like Aotus. The lateral incisor is large and high-crowned, which foreshadows living Pitheciinae. The canines and P2 were large and sharp like Callimico. Our analysis of the mandible and teeth suggest that Mohanamico is a primitive member of the Pitheciinae. Some similarities with Callimico and Saguinus are also noted raising the possibility that pithecines and callitrichids are monophyletic. (Introduction in French but main article in English).-from Authors
Phylogenetic comparative analysis is an approach to inferring evolutionary process from a combination of phylogenetic and phenotypic data. The last few years have seen increasingly sophisticated models employed in the evaluation of more and more detailed evolutionary hypotheses, including adaptive hypotheses with multiple selective optima and hypotheses with rate variation within and across lineages. The statistical performance of these sophisticated models has received relatively little systematic attention, however. We conducted an extensive simulation study to quantify the statistical properties of a class of models toward the simpler end of the spectrum that model phenotypic evolution using Ornstein-Uhlenbeck processes. We focused on identifying where, how, and why these methods break down so that users can apply them with greater understanding of their strengths and weaknesses. Our analysis identifies three key determinants of performance: a discriminability ratio, a signal-to-noise ratio, and the number of taxa sampled. Interestingly, we find that model-selection power can be high even in regions that were previously thought to be difficult, such as when tree size is small. On the other hand, we find that model parameters are in many circumstances difficult to estimate accurately, indicating a relative paucity of information in the data relative to these parameters. Nevertheless, we note that accurate model selection is often possible when parameters are only weakly identified. Our results have implications for more sophisticated methods inasmuch as the latter are generalizations of the case we study.
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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.
Fossils in Peru raise questions about the early evolution of monkeys in South America
The platyrrhine primates, or New World monkeys, are immigrant mammals whose fossil record comes from Tertiary and Quaternary sediments of South America and the Caribbean Greater Antilles. The time and place of platyrrhine origins are some of the most controversial issues in primate palaeontology, although an African Palaeogene ancestry has been presumed by most primatologists. Until now, the oldest fossil records of New World monkeys have come from Salla, Bolivia, and date to approximately 26 million years ago, or the Late Oligocene epoch. Here we report the discovery of new primates from the ?Late Eocene epoch of Amazonian Peru, which extends the fossil record of primates in South America back approximately 10 million years. The new specimens are important for understanding the origin and early evolution of modern platyrrhine primates because they bear little resemblance to any extinct or living South American primate, but they do bear striking resemblances to Eocene African anthropoids, and our phylogenetic analysis suggests a relationship with African taxa. The discovery of these new primates brings the first appearance datum of caviomorph rodents and primates in South America back into close correspondence, but raises new questions about the timing and means of arrival of these two mammalian groups.
Mesoamerican spider monkeys (Ateles geoffroyi sensu lato) are widely distributed from Mexico to northern Colombia. This group of primates includes many allopatric forms with morphologically distinct pelage color and patterning, but its taxonomy and phylogenetic history are poorly understood. We explored the genetic relationships among the different forms of Mesoamerican spider monkeys using mtDNA sequence data, and we offer a new hypothesis for the evolutionary history of the group. We collected up to ∼800 bp of DNA sequence data from hypervariable region 1 (HV1) of the control region, or D-loop, of the mitochondrion for multiple putative subspecies of Ateles geoffroyi sensu lato. Both maximum likelihood and Bayesian reconstructions, using Ateles paniscus as an outgroup, showed that (1) A. fusciceps and A. geoffroyi form two different monophyletic groups and (2) currently recognized subspecies of A. geoffroyi are not monophyletic. Within A. geoffroyi, our phylogenetic analysis revealed little concordance between any of the classifications proposed for this taxon and their phylogenetic relationships, therefore a new classification is needed for this group. Several possible clades with recent divergence times (1.7–0.8 Ma) were identified within Ateles geoffroyi sensu lato. Some previously recognized taxa were not separated by our data (e.g., A. g. vellerosus and A. g. yucatanensis), while one distinct clade had never been described as a different evolutionary unit based on pelage or geography (Ateles geoffroyi ssp. indet. from El Salvador). Based on well-supported phylogenetic relationships, our results challenge previous taxonomic arrangements for Mesoamerican spider monkeys. We suggest a revised arrangement based on our data and call for a thorough taxonomic revision of this group.
A significat event in the early evolution of Primates is the origin and radiation of anthropoids, with records in North Africa and Asia. The New World Primates, Infraorder Platyrrhini, have probably originated among these earliest anthropoids morphologically and temporally previous to the catarrhine/platyrrhine branching. The platyrrhine fossil record comes from distant regions in the Neotropics. The oldest are from the late Oligocene of Bolivia, with difficult taxonomic attribution. The two richest fossiliferous sites are located in the middle Miocene of La Venta, Colombia, and to the south in early to middle Miocene sites from the Argentine Patagonia and Chile. The absolute ages of these sedimentary deposits are ranging from 12 to 20 Ma, the oldest in Patagonia and Chile. These northern and southern regions have a remarkable taxonomic diversity and several extinct taxa certainly represent living clades. In addition, in younger sediments ranging from late Miocene through Pleistocene, three genera have been described for the Greater Antilles, two genera in eastern Brazil, and at least three forms for Río Acre. In general, the fossil record of South American primates sheds light on the old radiations of the Pitheciinae, Cebinae, and Atelinae. However, several taxa are still controversial. RESUMO: Origem e evolução dos primatas neotropicais. Um evento significativo durante o início da evolução dos primatas é a origem e a radiação dos antropóides, com registros no norte da África e da Ásia. Os representantes dos Primates do Novo Mundo, Infraordem Platyrrhini, provavelmente se originaram a partir dos antropóides mais primitivos, morfologica e temporalmente anteriores ao ramo Catarrhini/Platyrrhini. O registro fóssil dos Platyrrhini procede de regiões distantes no Neotrópico. Os mais antigos procedem do Oligoceno Superior da Bolívia, com atribuições taxonômicas difíceis. Os dois sítios fossilíferos mais ricos estão localizados no Mioceno Médio de La Venta, Colômbia, e ao sul, em sítios do Mioceno Inferior à Médio da Patagônia Argentina e Chile. A idade absoluta desses depósitos sedimentares varia de 12 a 20 Ma sendo os mais antigos depósitos os da Patagônia e do Chile. Essas regiões, ao norte e ao sul, tem uma notável diversidade taxonômica e os diversos táxons extintos certamente representam clados viventes. Somado a isto, três gêneros foram descritos para as Grandes Antilhas em sedimentos mais recentes, variando do Mioceno Superior ao Pleistoceno, dois gêneros para o leste do Brasil, e pelo menos três formas para o Río Acre. Em geral, o registro fóssil dos primatas sul-americanos permite de certa forma esclarecer as antigas radiações dos Pitheciinae, Cebinae e Atelinae. Contudo, vários táxons ainda são controversos. Palavras-chave: Primatas neotropicais. Origem. Evolução.
Studies of evolutionary correlations commonly utilize phylogenetic regression (i.e., independent contrasts and phylogenetic generalized least squares) to assess trait covariation in a phylogenetic context. However, while this approach is appropriate for evaluating trends in one or a few traits, it is incapable of assessing patterns in highly-multivariate data, as the large number of variables relative to sample size prohibits parametric test statistics from being computed. This poses serious limitations for comparative biologists, who must either simplify how they quantify phenotypic traits, or alter the biological hypotheses they wish to examine. In this article, I propose a new statistical procedure for performing ANOVA and regression models in a phylogenetic context that can accommodate high-dimensional datasets. The approach is derived from the statistical equivalency between parametric methods utilizing covariance matrices and methods based on distance matrices. Using simulations under Brownian motion, I show that the method displays appropriate Type I error rates and statistical power, whereas standard parametric procedures have decreasing power as data dimensionality increases. As such, the new procedure provides a useful means of assessing trait covariation across a set of taxa related by a phylogeny, enabling macroevolutionary biologists to test hypotheses of adaptation and phenotypic change in high-dimensional datasets. This article is protected by copyright. All rights reserved.
The papers collected in this volume summarize the state of our knowledge about the origins of Anthropoidea—monkeys, apes, and humans. Considering how important this group is for understanding human evolution, and the enormous literature that has grown up around the questions of where anthropoids may have originated and from what group, there is remarkably little consensus on any aspect of this topic. As will be seen in the following review, there are proponents for an African, Asian, or, ultimately, North American or European origin for anthropoids. And different scientists believe the closest relatives of anthropoids to be the extinct Eocene groups Omomyidae or Adapidae or living Tarsius from South Asia. In this final chapter we try to pull together the major arguments put forth in earlier chapters, to summarize what we see as the major points of agreement and disagreement over anthropoid origins, to identify major gaps or confusing lines of evidence in current knowledge, and finally to lay out what we see as the most fruitful directions for future research in this area. As we hope to make clear, just because the problem of anthropoid origins remains unresolved, it is not from a lack of data relevant to the issues being addressed. Quite the contrary, we know a lot more about this topic than we did a decade ago, or even 5 years ago.
One of the goals of paleoprimatology is to provide adaptive explanations for the origins of evolutionary novelties of the order and its major groups. For such scenarios to be more than,“just-so stories,” like Kipling’s story of how the leopard got its spots, we need to develop and test ideas about the adaptive significance of particular morphological character states that are likely to be preserved in the fossil record. Once the adaptive context of the morphology is fully appreciated, we can go on to make inferences about the behavior of extinct primate species that possessed similar character states. But even when we know with some confidence the adaptive “meaning” of a particular morphological character state and use it to infer the behavior of an extinct species, we must be able to place that extinct species into its phylogenetic context. What is the distribution of the newly identified morphological peculiarity? Is it found in just one extinct species or does it characterize some larger group of species? And what does the distribution of the character state tell us about the ancestral morphological (and inferred behavioral) pattern of primate clades? Therefore, in parallel with the effort to understand adaptation of character states, there must be an effort to reconstruct the phylogenetic pattern of primates.
The mathematical/statistical software platform R has seen an immense increase in popularity within the last decade. Its main advantages are its flexibility, a large repository of freely available extensions, its open-source nature and a thriving community. This tutorial gives an introduction into landmark/surface-mesh based statistical shape analysis in R – specifically using the packages Morpho and Rvcg . Beginning with examples based on sparse sets of anatomical landmarks, the tutorial will go on dealing with surface and curve landmarks and more challenging tasks such as mesh manipulations and surface registration. Apart from statistical analyses, emphasis will also be put on comprehensive visualization of the results. Extensive examples and code snippets are provided to allow the reader to easily replicate the analyses.
Objectives:
Undoubted fossil Cebidae have so far been primarily documented from the late middle Miocene of Colombia, the late Miocene of Brazilian Amazonia, the early Miocene of Peruvian Amazonia, and very recently from the earliest Miocene of Panama. The evolutionary history of cebids is far from being well-documented, with notably a complete blank in the record of callitrichine stem lineages until and after the late middle Miocene (Laventan SALMA). Further documenting their evolutionary history is therefore of primary importance.
Material:
Recent field efforts in Peruvian Amazonia (Contamana area, Loreto Department) have allowed for the discovery of an early late Miocene (ca. 11 Ma; Mayoan SALMA) fossil primate-bearing locality (CTA-43; Pebas Formation). In this study, we analyze the primate material, which consists of five isolated teeth documenting two distinct Cebidae: Cebus sp., a medium-sized capuchin (Cebinae), and Cebuella sp., a tiny marmoset (Callitrichinae).
Results:
Although limited, this new fossil material of platyrrhines contributes to documenting the post-Laventan evolutionary history of cebids, and besides testifies to the earliest occurrences of the modern Cebuella and Cebus/Sapajus lineages in the Neotropics. Regarding the evolutionary history of callitrichine marmosets, the discovery of an 11 Ma-old fossil representative of the modern Cebuella pushes back by at least 6 Ma the age of the Mico/Cebuella divergence currently proposed by molecular biologists (i.e., ca. 4.5 Ma). This also extends back to > 11 Ma BP the divergence between Callithrix and the common ancestor (CA) of Mico/Cebuella, as well as the divergence between the CA of marmosets and Callimico (Goeldi's callitrichine).
Discussion:
This discovery from Peruvian Amazonia implies a deep evolutionary root of the Cebuella lineage in the northwestern part of South America (the modern western Amazon basin), slightly before the recession of the Pebas mega-wetland system (PMWS), ca. 10.5 Ma, and well-before the subsequent establishment of the Amazon drainage system (ca. 9-7 Ma). During the late middle/early late Miocene interval, the PMWS was seemingly not a limiting factor for dispersals and widespread distribution of terrestrial mammals, but it was also likely a source of diversification via a complex patchwork of submerged/emerged lands varying through time.
Reconstructing the paleobiology of fossil non-human primates, this book is intended as an exposition of non-human primate evolution that includes information about evolutionary theory and processes, paleobiology, paleoenvironment, how fossils are formed, how fossils illustrate evolutionary processes, the reconstruction of life from fossils, the formation of the primate fossil record, functional anatomy, and the genetic bases of anatomy. Throughout, the emphasis of the book is on the biology of fossil primates, not their taxonomic classification or systematics, or formal species descriptions. The author draws detailed pictures of the paleoenvironment of fossil primates, including contemporary animals and plants, and ancient primate communities, emphasizing our ability to reconstruct lifeways from fragmentary bones and teeth, using functional anatomy, stable isotopes from enamel and collagen, and high resolution CT-scans of the cranium. Fossil Primates will be essential reading for advanced undergraduates and graduate students in evolutionary anthropology, primatology and vertebrate paleobiology.
The name Platyrrhini has been erected to designate the extant neotropical monkeys (including marmosets), which zoologists agree to group into a super-family Ceboidea. Living in the tropical forests of South and Central America, they are distinguished from the recent Old World monkeys by the presence of three premolars (instead of two), their ring-shaped ectotympanic (not developed into a bony tube), their inflated auditory bulla, several details of cranial architecture (notably the parietal-jugal contact, which must have been constant in the group at its origin), placentation (no cytotrophoblastic shell, trabecular condition of the placental disk: see Luckett, 1975) and also by platyrrhiny [which, as redefined by Hofer (1976), is diagnostic for the group]. Practically all fossil primates known from South America and the West Indies are referred to this group: late Pleistocene or Holocene of Brazil (five recent genera), Hispaniola (Saimiri: see Rimoli, 1977) and Jamaica (Xenothrix); middle Miocene of Colombia (Neosaimiri, Cebupithecia, Stirtonia); early Miocene (Homunculus) and latest Oligocene (Dolichocebus, Tremacebus) of Patagonia, and also early Oligocene of Bolivia (Branisella). However, Hershkovitz (1974a) has expressed doubts as to the n of Branisella within the Platyrrhini and even within the Haplorhini. According to him, the small single-rooted P2 of this fossil would indicate a trend toward the disappearance of this tooth, and the quadritubercular pattern of its upper molars (provided with a hypocone) would prevent this genus from being placed among the ancestors of the marmosets (whose triangular molars lack a hypocone). In my opinion (Hoffstetter,1969), Branisella has retained the ancestral characters of the Haplorhini in both respects (these characters are also found in the earliest Tarsiiformes: Omomyidae), and the Callitrichidae have secondarily lost their hypocones (a loss also observed in ancient Tarsiiformes such as Chumashius and modern ones such as Tarsius). This question will be returned to later.
Adaptive radiation, which results when a single ancestral species gives rise to many descendants, each adapted to a different part of the environment, is possibly the single most important source of biological diversity in the living world. One of the best-studied examples involves Caribbean Anolis lizards. With about 400 species, Anolis has played an important role in the development of ecological theory and has become a model system exemplifying the integration of ecological, evolutionary, and behavioral studies to understand evolutionary diversification. This major work, written by one of the best-known investigators of Anolis, reviews and synthesizes an immense literature. Jonathan B. Losos illustrates how different scientific approaches to the questions of adaptation and diversification can be integrated and examines evolutionary and ecological questions of interest to a broad range of biologists.
The concept of “living fossil” as employed by Simpson (1953) and others has been somewhat altered for the purposes of this volume. As we understand it, the implication is of a living taxon that differs only slightly if at all in known morphology from an early fossil member of its clade, at whatever taxonomic rank. In this spirit, we will examine the “higher” or anthropoid primates to determine if any taxa, including some previously suggested, qualify for this status. Following Szalay and Delson (1979), the Order Primates is divided into three suborders, the extinct Plesiadapiformes, the Strepsirhini (lower primates), and the Haplorhini, including the infraorders Tarsiiformes (tarsiers and fossil relatives—see Schwartz, this volume), Platyrrhini (New World anthropoids), and Catarrhini (Old World anthropoids).
The neotropical primate family Pitheciidae consists of four genera Cacajao (uacaris), Callicebus (titis), Chiropotes (bearded sakis) and Pithecia (sakis), whose 40+ species display a range of sizes, social organisations, ecologies and habitats. Few are well known and the future survival of many is threatened, yet pitheciines have been little studied. This book is the first to review the biology of this fascinating and diverse group in full. It includes fossil history, reviews of the biology of each genus and, among others, specific treatments of vocalisations and foraging ecology. These studies are integrated into considerations of current status and future conservation requirements on a country-by-country basis for each species. A state-of-the-art summary of current knowledge, Evolutionary Biology and Conservation of Titis, Sakis and Uacaris is a collective effort from all the major researchers currently working on these remarkable animals.
Convergent evolution is an important phenomenon in the history of life. Despite this, there is no common definition of convergence used by biologists. Instead, several conceptually different definitions are employed. The primary dichotomy is between pattern-based definitions, where independently evolved similarity is sufficient for convergence, and process-based definitions, where convergence requires a certain process to produce this similarity. The unacknowledged diversity of definitions can lead to problems in evolutionary research. Process-based definitions may bias researchers away from studying or recognizing other sources of independently-evolved similarity, or lead researchers to interpret convergent patterns as necessarily caused by a given process. Thus, pattern-based definitions are recommended. Existing measures of convergence are reviewed, and two new measures are developed. Both are pattern-based and conceptually minimal, quantifying nothing but independently-evolved similarity. One quantifies the amount of phenotypic distance between two lineages that is closed by subsequent evolution; the other simply counts the number of lineages entering a region of phenotypic space. The behavior of these measures is explored in simulations; both show acceptable Type I and Type II error. The study of convergent evolution will be facilitated if researchers are explicit about working definitions of convergence and adopt a standard toolbox of convergence measures. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
1. We present mvMORPH, a package of multivariate phylogenetic comparative methods for the R statistical environment. mvMORPH is freely available on the CRAN package repository (http://cran.r-project.org/web/packages/mvMORPH/).
2. mvMORPH allows fitting a range of multivariate evolutionary models under a maximum-likelihood criterion. Initially developed in the context of phylogenetic analysis of multiple morphometric traits, its use can be extended to any biological dataset with one or multiple covarying continuous traits. All the fitting models include the possibility to use SIMMAP-like mapping, which may be useful for fitting changes along lineages at a given point in time. All models provide diagnostic metrics for convergence and reliability of estimates, as well as the possibility to include trait measurement errors in model estimates.
3. New features provided by the mvMORPH package include the possibility of fitting models with changes in the mode of evolution along the phylogeny, which will be particularly meaningful in comparative analyses that include extinct taxa, e.g., when testing changes in evolutionary mode associated with global biotic/abiotic events.
4. We briefly describe the models already included in mvMORPH, and provide some demonstration of the use of the package with two simulated worked examples.
Objectives:
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.
Methods:
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).
Results:
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.
Conclusions:
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.
A direct algorithm is described to reconstruct on a phylogenetic tree the ancestral states of a continuous-valued character, using a parsimony criterion that minimizes the sum of squared changes along the branches. It is shown that when the squared changes are inversely weighted by the lengths of the branches, the squared-change parsimony reconstruction is that which has maximum posterior probability under a Brownian motion model of evolution. The squared-change parsimony estimates are also closely related to the contrasts in Felsenstein's test of character correlation.
George Gaylord Simpson famously postulated that much of life’s diversity originated as adaptive radiations—more or less simulta- neous divergences of numerous lines from a single ancestral adaptive type. However, identifying adaptive radiations has proven difficult due to a lack of broad-scale comparative datasets. Here, we use phylogenetic comparative data on body size and shape in a diversity of animal clades to test a key model of adaptive radiation, in which initially rapid morphological evolution is followed by relative stasis. We compared the fit of this model to both single selective peak and random walk models. We found little support for the early-burst model of adaptive radiation, whereas both other models, particularly that of selective peaks, were commonly supported. In addition, we found that the net rate of morphological evolution varied inversely with clade age. The youngest clades appear to evolve most rapidly because long-term change typically does not attain the amount of divergence predicted from rates measured over short time scales. Across our entire analysis, the dominant pattern was one of constraints shaping evolution continually through time rather than rapid evolution followed by stasis. We suggest that the classical model of adaptive radiation, where morphological evolution is initially rapid and slows through time, may be rare in comparative data.
Modern phylogenetic comparative biology uses data from the relationships between species (phylogeny) combined with comparative information for phenotypic traits to draw model‐based statistical inferences about the evolutionary past. Recent years have seen phylogeny methods for evolutionary inference become central in the study of organic evolution.
Here, I present two different graphical methods for visualizing phenotypic evolution on the tree. Method 1 is a new approach for plotting the posterior density of stochastically mapped character histories for a binary (two‐state) phenotypic trait on a phylogeny. Method 2 is a closely related technique that uses ancestral character estimation to visualize historical character states for a continuous trait along the branches of a tree.
One shortcoming of Method 2 is that by mapping the point estimates of ancestral states along the branches of the tree, we have effectively ignored the uncertainty associated with ancestral character estimation of continuous traits. To alleviate this issue, I propose a new method for visualizing ancestral state uncertainty using a type of projection of the tree into morphospace called a ‘traitgram.’
All of these approaches should prove useful in summarizing complex comparative inferences about ancestral character reconstruction. They are implemented in the freely available and open‐source R phylogenetics package ‘phytools.’