An Early Oligocene age for the oldest known monkeys and rodents of South America.

The Santa Rosa fossil locality in eastern Perú produced the first Paleogene vertebrate fauna from the Amazon Basin, including the oldest known monkeys from South America. This diverse paleofauna was originally assigned an Eocene age based largely on the stage of evolution of the site's caviomorph rodents and marsupials. Here, we present detrital zircon dates that indicate that the maximum composite age of Santa Rosa is 29.6 ± 0.08 Ma (Lower Oligocene), although several zircons from Santa Rosa date to the Upper Oligocene. The first appearance datum for Caviomorpha in South America is purported to be the CTA-27 site in the Contamana region of Perú, which is hypothesized to be ∼41 Ma (Middle Eocene) in age. However, the presence of the same caviomorph species and/or genera at both CTA-27 and at Santa Rosa is now difficult to reconcile with a >11-My age difference. To further test the Middle Eocene age estimate for CTA-27, we ran multiple Bayesian tip-dating analyses of Caviomorpha, treating the ages of all Paleogene species from Perú as unknown. These analyses produced mean age estimates for Santa Rosa that closely approximate the maximum 29.6 ± 0.08 Ma composite date provided by detrital zircons, but predict that CTA-27 is much younger than currently thought (∼30 Ma). We conclude that the ∼41 Ma age proposed for CTA-27 is incorrect, and that there are currently no compelling Eocene records of either rodents or primates in the known fossil record of South America.

A new parapithecine (Primates: Anthropoidea) from the early Oligocene of Libya supports parallel evolution of large body size among parapithecids.

Parapithecines are an extinct subfamily of stem anthropoid primates previously known only from the Jebel Qatrani Formation in Egypt. Here, we describe isolated teeth pertaining to Simonsius harujensis sp. nov., a relatively small-bodied parapithecine from strata near Zallah Oasis in the Sirt Basin of central Libya that is estimated to date to ∼31 Ma on the basis of mammalian biostratigraphy. The dental morphology of S. harujensis sp. nov. is generally intermediate between that of the closely related parapithecines Parapithecus fraasi and Simonsius grangeri, highlighting some of the anatomical features distinguishing the latter taxa and providing further support for their generic separation. A phylogenetic analysis using parsimony methods was performed on a character-taxon matrix incorporating data from the new Libyan parapithecine, virtually all other parapithecids and the proteopithecid Proteopithecus sylviae. Results of this analysis suggest that parapithecids comprise a basal clade consisting of three species of Biretia and a more derived clade including Parapithecinae (Parapithecus and Simonsius) and Qatraniinae (Qatrania, Ucayalipithecus, and Apidium). Body mass estimates for parapithecids were calculated on the basis of regression equations generated to predict body mass from the occlusal area of upper and lower cheek teeth in extant anthropoids. The relatively small body mass of S. harujensis sp. nov. and its reconstructed phylogenetic position as the sister group of S. grangeri, which is the largest known parapithecid, support the convergent acquisition of body mass larger than 500 g among multiple clades of early Oligocene African anthropoids. The new Libyan parapithecine augments previously reported evidence supporting a substantial degree of faunal provincialism across northern Africa/Arabia during the early Oligocene.

A new identification of the monkeys depicted in a Bronze Age wall painting from Akrotiri, Thera.

Bronze Age Aegean (ca. 3500-1100 B.C.) wall paintings from the islands of Crete and Thera depict monkeys in a variety of roles such as running wild in nature, possibly following (trained) commands, and participating in sacred activities. These images, while stylistically Aegean, are traditionally considered closely related to-and descendant from-Egyptian, Near Eastern, and Mesopotamian monkey imagery. While monkey depictions in the latter regions may provide species-specific characteristics, Aegean wall paintings typically lack this level of detail. In an attempt to better understand the relationships between the monkeys depicted in Aegean wall paintings and the species that were encountered by the Aegean, Mesopotamian, and Egyptian peoples, a collaborative team of primatologists, a taxonomic illustrator, and an art historian/archaeologist identified species-indicative visual characteristics. This collaborative approach led us to identify a new region that serves as a source for monkey iconography: the Indus River Valley. With an emphasis on the primatological aspect and the growing corpus of possible Indus goods and possible species found in the Aegean, a broader iconographic and socioreligious sphere of interaction emerges. In this expanded system, Mesopotamia functions as an intermediary that enables the movement of goods, raw materials, people, and iconography between the east and west. Mesopotamia may have even afforded an opportunity for Aegean peoples to encounter the creatures themselves, first-hand. Of primary importance to the methodology employed for this project is the cooperation of scholars from disparate disciplines-the stitching together of various projects and experiences in attempt to answer both new and previously unanswerable questions. This type of interdisciplinary approach can be applied to other species, sites, paintings, and objects to hone our understanding of period, place, animal, movement, and trade.

Cranial endocast of a stem platyrrhine primate and ancestral brain conditions in anthropoids.

Understanding of ancestral conditions for anthropoids has been hampered by the paucity of well-preserved early fossils. Here, we provide an unprecedented view of the cerebral morphology of the 20-million-year-old Chilecebus carrascoensis, the best-preserved early diverging platyrrhine known, obtained via high-resolution CT scanning and 3D digital reconstruction. These analyses are crucial for reconstructing ancestral brain conditions in platyrrhines and anthropoids given the early diverging position of Chilecebus. Although small, the brain of Chilecebus is not lissencephalic and presents at least seven pairs of sulci on its endocast. Comparisons of Chilecebus and other basal anthropoids indicate that the major brain subdivisions of these early anthropoids exhibit no consistent scaling pattern relative to the overall brain size. Many gross cerebral features appear to have transformed in a mosaic fashion and probably have originated in platyrrhine and catarrhine anthropoids independently, involving multiple, independent instances of size increase, as well as some secondary decreases.

Middle ear pneumatization in nonhuman primates: A comparative analysis.

OBJECTIVES: We test the effects of body mass and phylogeny on middle ear cavity pneumatization, and the role of pneumatization in hearing function, spanning the anatomical, ecological, and behavioral diversity of nonhuman primates. MATERIALS AND METHODS: All cavities were segmented in middle ear scans of 96 specimens, from 12 strepsirrhine and 15 haplorhine extant species. We measured the tympanic cavity (TC) separately, and all other middle ear spaces together (MES), calculating the degree of pneumatization with the surface area-to-volume ratio. We tested body mass effect with linear regression; we evaluated the phylogenetic signal and selection patterns, using a Kappa statistic test, and Ornstein-Uhlenbeck models (OU). We investigated the link between pneumatization and hearing sensitivity using phylogenetic regression. RESULTS: Testing body mass reveals an allometric pattern for both TC and MES dimensions. Degree of pneumatization in MES is dependent on body mass in haplorhines: larger animals have more pneumatized MES. Differences at various taxonomic ranks were observed for MES, while no phylogenetic influence was observed for TC. Infraorder selection patterns are different. Auditory performance is significantly related to degree of pneumatization, indicating that a pneumatized middle ear is associated with better perception of low frequencies. DISCUSSION: Pneumatization in MES is under differential selective pressure, indicating several optima for this trait. Pneumatization in MES probably modifies hearing sensitivity through pressure regulation mechanisms, auditory bulla size reduction, and frequency modulation. This could explain strepsirrhine adaptation to high-frequency perception, while haplorhine auditory perception is adapted to a broader sound range, including high and low frequencies.

New middle Eocene omomyines (Primates, Haplorhini) from San Diego County, California.

The Friars Formation of San Diego County, California, has yielded a middle Eocene mammalian fauna from the early part of the Uintan North American Land Mammal Age. Prior research on the primate fauna from the Friars Formation provides evidence of one notharctine and multiple omomyine species, but many specimens collected since the early 1980s remain unstudied. Here we describe three new omomyine genera from the Friars Formation. These new taxa range in estimated body mass from about 119 g to 757 g, and substantially expand the diversity of middle Eocene omomyoids known from Southern California. Resolution of the phylogenetic relationships of the new Friars Formation omomyines is complicated by the fact that different character-taxon matrices and tree building methods produce different results. Nevertheless, all preliminary phylogenetic analyses are congruent in recovering a close relationship between the three new genera and the omomyines Macrotarsius, Omomys, Ourayia, and Utahia. Prior research has documented a shift in omomyoid diversity in North America from the anantomophine-rich Bridgerian to the omomyine-rich Uintan. Our description of three new Uintan omomyine taxa from the Friars Formation further emphasizes these opposite trends in anaptomorphine and omomyine species richness during the middle Eocene. All three of the new taxa are currently known from only the Friars Formation in San Diego County, California. Four of the previously known omomyoid genera from Southern California (Dyseolemur, Chumashius, Yaquius, and Stockia) are also endemic to the region, further highlighting the provincial character of primate faunas in Utah, Southern California, and West Texas during the Uintan.

The role of indirect evidence and traditional ecological knowledge in the discovery and description of new ape and monkey species since 1980.

Although empirical data are necessary to describe new species, their discoveries can be guided from the survey of the so-called circumstantial evidence (that indirectly determines the existence or nonexistence of a fact). Yet this type of evidence, generally linked to traditional ecological knowledge (TEK), is often disputed by field biologists due to its uncertain nature and, on account of that, generally untapped by them. To verify this behavior and the utility of circumstantial evidence, we reviewed the existing literature about the species of apes and monkeys described or rediscovered since January 1, 1980 and submitted a poll to the authors. The results show that circumstantial evidence has proved to be useful in 40.5% of the examined cases and point to the possibility that its use could speed up the process at the heart of the discovery and description of new species, an essential step for conservation purposes.

Nasolacrimal anatomy and haplorhine origins.

Computed tomography X-ray imaging of the internal face in well-preserved primate fossil crania permits reconstruction of the nature of their nasal anatomy, including some soft-tissue features. These features are diagnostic of the primate suborder Haplorhini, and allow reevaluation of the phylogenetic status of several purported early members of the group. Here we examine the nasolacrimal morphology of a broad sample of extant primates, as well as a number of Paleogene fossils. The extant sample confirms the distinctiveness of the two suborders. Of the fossils studied, only Shoshonius cooperi from the late-early Eocene exhibits evidence of a haplorhine nose. This suggests that the haplorhine oronasal complex may have evolved before the postorbital septum, and strengthens the claim that Shoshonius is a close relative of tarsiers and anthropoids. These results indicate that Omomyiformes is not a monophyletic group, and that few of its members possessed the derived oronasal morphology that characterizes crown haplorhines.

New euprimate postcrania from the early Eocene of Gujarat, India, and the strepsirrhine-haplorhine divergence.

The oldest primates of modern aspect (euprimates) appear abruptly on the Holarctic continents during a brief episode of global warming known as the Paleocene-Eocene Thermal Maximum, at the beginning of the Eocene (∼56 Ma). When they first appear in the fossil record, they are already divided into two distinct clades, Adapoidea (basal members of Strepsirrhini, which includes extant lemurs, lorises, and bushbabies) and Omomyidae (basal Haplorhini, which comprises living tarsiers, monkeys, and apes). Both groups have recently been discovered in the early Eocene Cambay Shale Formation of Vastan lignite mine, Gujarat, India, where they are known mainly from teeth and jaws. The Vastan fossils are dated at ∼54.5 Myr based on associated dinoflagellates and isotope stratigraphy. Here, we describe new, exquisitely preserved limb bones of these Indian primates that reveal more primitive postcranial characteristics than have been previously documented for either clade, and differences between them are so minor that in many cases we cannot be certain to which group they belong. Nevertheless, the small distinctions observed in some elements foreshadow postcranial traits that distinguish the groups by the middle Eocene, suggesting that the Vastan primates-though slightly younger than the oldest known euprimates-may represent the most primitive known remnants of the divergence between the two great primate clades.

Sexual selection on male vocal fundamental frequency in humans and other anthropoids.

In many primates, including humans, the vocalizations of males and females differ dramatically, with male vocalizations and vocal anatomy often seeming to exaggerate apparent body size. These traits may be favoured by sexual selection because low-frequency male vocalizations intimidate rivals and/or attract females, but this hypothesis has not been systematically tested across primates, nor is it clear why competitors and potential mates should attend to vocalization frequencies. Here we show across anthropoids that sexual dimorphism in fundamental frequency (F0) increased during evolutionary transitions towards polygyny, and decreased during transitions towards monogamy. Surprisingly, humans exhibit greater F0 sexual dimorphism than any other ape. We also show that low-F0 vocalizations predict perceptions of men's dominance and attractiveness, and predict hormone profiles (low cortisol and high testosterone) related to immune function. These results suggest that low male F0 signals condition to competitors and mates, and evolved in male anthropoids in response to the intensity of mating competition.

A new species of Apidium (Anthropoidea, Parapithecidae) from the Sirt Basin, central Libya: First record of Oligocene primates from Libya.

A new species of Apidium is the most common primate currently known from a newly discovered site near Zallah Oasis in the Sirt Basin of central Libya. Based on current knowledge of the associated fauna, this new species of Apidium is early Oligocene in age, being roughly contemporaneous with faunas from Quarries G and V in the upper part of the Jebel Qatrani Formation in Egypt that also contain species of Apidium. A phylogenetic analysis based on dental characters indicates that the new species of Apidium from Libya is the sister group of Apidium phiomense. Apidium bowni and Apidium moustafai from the Jebel Qatrani Formation in the Fayum are similar in age to the new species of Apidium from Libya, but both of these Egyptian species are more distantly related to A. phiomense from younger stratigraphic levels in the Fayum. This phylogenetic pattern underscores the benefit of enhanced geographic sampling of the fossil record, even in cases where local records are thought to be reasonably comprehensive and well documented. Oligocene parapithecids can be partitioned into two clades corresponding to the subfamilies Parapithecinae (containing Parapithecus and Simonsius) and Qatraniinae (including Qatrania and Apidium). Climatic deterioration during the early Oligocene may have impacted the macroevolutionary dynamics of early Afro-Arabian anthropoids by fostering the fragmentation of forest habitats, thereby promoting allopatric speciation among widespread populations of Apidium and other arboreal taxa.

Upper molar morphology of the early oligocene egyptian anthropoid Qatrania wingi.

OBJECTIVES: Qatrania wingi is a poorly documented fossil anthropoid known only from Quarry E in the Jebel Qatrani Formation, Fayum Depression, Egypt. This report augments our knowledge of the dental morphology of Qatrania in order to clarify its phylogenetic relationships with other early African anthropoids. MATERIALS AND METHODS: YPM 18008 from Quarry E is the first example of an upper molar fragment that can reasonably be assigned to Qatrania wingi. Maximum parsimony phylogenetic analyses incorporating the new data from YPM 18008 were performed. RESULTS: If YPM 18008 is treated as a separate OTU, it is reconstructed as a member of Qatraniinae (the parapithecid clade containing Qatrania and Apidium). The only qatraniine known to occur at Quarry E is Qatrania wingi, and YPM 18008 is allocated to this species based on its size, provenance, and morphology. Despite its small size and early stratigraphic occurrence, the upper molar morphology of Qatrania wingi is highly derived with respect to that of other parapithecids aside from Apidium. Like that of Apidium, the upper molar morphology of Qatrania bears multiple neomorphic cusps and cuspules. These features appear to be synapomorphies linking Apidium and Qatrania to the exclusion of other parapithecids for which upper molar morphology is known, namely Simonsius grangeri and Biretia spp. DISCUSSION: YPM 18008 supports the recent proposal of a Qatrania + Apidium clade within Parapithecidae. This conflicts with earlier hypotheses, in which Qatrania was reconstructed as being phylogenetically basal to a clade including the younger, larger-bodied parapithecid taxa Apidium, Parapithecus, and Simonsius.

A morphological intermediate between eosimiiform and simiiform primates from the late middle Eocene of Tunisia: Macroevolutionary and paleobiogeographic implications of early anthropoids.

Although advanced anthropoid primates (i.e., Simiiformes) are recorded at the end of the Eocene in North Africa (Proteopithecidae, Parapithecidae, and Oligopithecidae), the origin and emergence of this group has so far remained undocumented. The question as to whether these primates are the result of a monophyletic radiation of endemic anthropoids in Africa, or several Asian clades colonizing Africa, is a current focus of paleoprimatology. In this article, we report the discovery of a new anthropoid from Djebel el Kébar in central Tunisia, dating from the late middle Eocene (Bartonian). This taxon, Amamria tunisiensis, new genus and species, currently known by only one isolated upper molar, is among the most ancient anthropoids to be recorded in Africa thus far. Amamria displays a suite of dental features that are primarily observed in Eosimiiformes (stem Anthropoidea). However, it is not allocated to any known family of that group (i.e., Asian Eosimiidae and Afro-Asian Afrotarsiidae) inasmuch as it develops some dental traits that are unknown among eosimiiforms, but can be found in African simiiform anthropoids such as proteopithecids and oligopithecids. With such a mosaic of dental traits, Amamria appears to be a structural intermediate, and as such it could occupy a key position, close to the root of the African simiiforms. Given its antiquity and its apparent pivotal position, the possibility exists that Amamria could have evolved in Africa from Asian eosimiiform or Asian "proto"-simiiform ancestors, which would have entered Africa sometime during the middle Eocene. Amamria could then represent one of the earliest offshoots of the African simiiform radiation. This view would then be rather in favor of the hypothesis of a monophyletic radiation of endemic simiiform anthropoids in Africa. Finally, these new data suggest that there must have been at least two Asian anthropoid colonizers of Africa: the afrotarsiids and the ancestor of Amamria.

Performance of genomic data sets on the estimation of the divergence time of New World and Old World anthropoids.

The origin of New World anthropoids has received renewed attention since the advent of molecular dating methods that relax the assumption of a strict molecular clock. However, the studies conducted to date have estimated the time of the separation of New World and Old World anthropoids at values as different as 70 and 22 Ma. With the aim of investigating the source of the discrepancies in the inferred ages, we have compared the performance of mitochondrial and nuclear markers in two pairs of datasets. We show that in the larger genomic samples, the dates of the separation of New and Old World anthropoids estimated from nuclear and mitochondrial data are significantly different. The precision of the estimates demonstrated that both markers rendered significantly different estimates. However, parametric estimates from the large nuclear dataset were highly cross-correlated. Cross-correlation of absolute divergence times and evolutionary rates was as great as -96%. Consequently, the age estimates from the large nuclear data were not reproducible, because Markov chains were unable to reach the same parametric values independently, even with the adoption of additional information from calibration priors. Thus, because branch length decomposition was not achieved, a comparison of the genomic age estimates from nuclear and mitochondrial datasets was statistically impractical. We demonstrate the importance of examining the output of Markov chain Monte Carlo analyses for correlation between rate and time in studies that use phylogenomic datasets to examine the chronological scales of primate evolution.

Seven novel MHC class I alleles identified in Cercopithecus mitis.

We report here the identification of three Cemi-A and four Cemi-B novel alleles of Cercopithecus mitis.

Evolution of the relaxin/insulin-like gene family in anthropoid primates.

The relaxin/insulin-like gene family includes signaling molecules that perform a variety of physiological roles mostly related to reproduction and neuroendocrine regulation. Several previous studies have focused on the evolutionary history of relaxin genes in anthropoid primates, with particular attention on resolving the duplication history of RLN1 and RLN2 genes, which are found as duplicates only in apes. These studies have revealed that the RLN1 and RLN2 paralogs in apes have a more complex history than their phyletic distribution would suggest. In this regard, alternative scenarios have been proposed to explain the timing of duplication, and the history of gene gain and loss along the organismal tree. In this article, we revisit the question and specifically reconstruct phylogenies based on coding and noncoding sequence in anthropoid primates to readdress the timing of the duplication event giving rise to RLN1 and RLN2 in apes. Results from our phylogenetic analyses based on noncoding sequence revealed that the duplication event that gave rise to the RLN1 and RLN2 occurred in the last common ancestor of catarrhine primates, between ∼ 44.2 and 29.6 Ma, and not in the last common ancestor of apes or anthropoids, as previously suggested. Comparative analyses based on coding and noncoding sequence suggests an event of convergent evolution at the sequence level between co-ortholog genes, the single-copy RLN gene found in New World monkeys and the RLN1 gene of apes, where changes in a fraction of the convergent sites appear to be driven by positive selection.

A new Late Eocene primate from the Krabi Basin (Thailand) and the diversity of Palaeogene anthropoids in southeast Asia.

According to the most recent discoveries from the Middle Eocene of Myanmar and China, anthropoid primates originated in Asia rather than in Africa, as was previously considered. But the Asian Palaeogene anthropoid community remains poorly known and inadequately sampled, being represented only from China, Myanmar, Pakistan and Thailand. Asian Eocene anthropoids can be divided into two distinct groups, the stem group eosimiiforms and the possible crown group amphipithecids, but the phylogenetic relationships between these two groups are not well understood. Therefore, it is critical to understand their evolutionary history and relationships by finding additional fossil taxa. Here, we describe a new small-sized fossil anthropoid primate from the Late Eocene Krabi locality in Thailand, Krabia minuta, which shares several derived characters with the amphipithecids. It displays several unique dental characters, such as extreme bunodonty and reduced trigon surface area, that have never been observed in other Eocene Asian anthropoids. These features indicate that morphological adaptations were more diversified among amphipithecids than was previously expected, and raises the problem of the phylogenetic relations between the crown anthropoids and their stem group eosimiiforms, on one side, and the modern anthropoids, on the other side.

Uniquely derived upper molar morphology of Eocene Amphipithecidae (Primates: Anthropoidea): homology and phylogeny.

The extinct Southeast Asian primate family Amphipithecidae is regularly cited in discussions of anthropoid origins, but its phylogenetic position remains controversial. In part, the lack of consensus regarding amphipithecid relationships can be attributed to uncertainty regarding the homology of upper molar structures in this group. Here, we describe a virtually pristine upper molar of Pondaungia cotteri from the late middle Eocene Pondaung Formation of Myanmar, which is the first example of a relatively unworn and well-preserved amphipithecid upper molar ever recovered. The distolingual upper molar cusp in this new specimen of Pondaungia appears to be a lingually displaced and enlarged metaconule, rather than a hypocone or pseudohypocone as previous workers have thought. Reassessment of the upper molar morphology of other amphipithecids and putative amphipithecids reveals a very similar pattern in Siamopithecus, Myanmarpithecus and Ganlea, all of which are interpreted as having upper molars showing many of the same derived features apparent in Pondaungia. In contrast, the upper molar morphology of Bugtipithecus diverges radically from that of undoubted amphipithecids, and the latter taxon is excluded from Amphipithecidae on this basis. Phylogenetic analyses of several character-taxon matrices culled from the recent literature and updated to reflect the new information on amphipithecid upper molar morphology yield similar results. Consensus tree topologies derived from these analyses support amphipithecid monophyly and stable relationships within Amphipithecidae. Amphipithecids appear to be stem members of the anthropoid clade.

Identification of bacterial infection in neotropical primates.

Emerging infectious diseases usually arise from wild animal populations. In the present work, we performed a screening for bacterial infection in natural populations of New World primates. The blood cell bulk DNAs from 181 individuals of four Platyrrhini genera were PCR screened for eubacterial 16S rRNA genes. Bacteria were detected and identified in 13 distinct individuals of Alouatta belzebul, Alouatta caraya, and Cebus apella monkeys from geographically distant regions in the states of Mato Grosso and Pará, Brazil. Sequence analyses showed that these Platyrrhini bacteria are closely related not only to human pathogens Pseudomonas spp. but also to Pseudomonas simiae and sheep-Acari infecting Pseudomonas spp. The identified Pseudomonas possibly represents a group of bacteria circulating in natural monkey populations.

Laterality and the evolution of the prefronto-cerebellar system in anthropoids.

There is extensive evidence for an early vertebrate origin of lateralized motor behavior and of related asymmetries in underlying brain systems. We investigate human lateralized motor functioning in a broad comparative context of evolutionary neural reorganization. We quantify evolutionary trends in the fronto-cerebellar system (involved in motor learning) across 46 million years of divergent primate evolution by comparing rates of evolution of prefrontal cortex, frontal motor cortex, and posterior cerebellar hemispheres along individual branches of the primate tree of life. We provide a detailed evolutionary model of the neuroanatomical changes leading to modern human lateralized motor functioning, demonstrating an increased role for the fronto-cerebellar system in the apes dating to their evolutionary divergence from the monkeys (∼30 million years ago (Mya)), and a subsequent shift toward an increased role for prefrontal cortex over frontal motor cortex in the fronto-cerebellar system in the Homo-Pan ancestral lineage (∼10 Mya) and in the human ancestral lineage (∼6 Mya). We discuss these results in the context of cortico-cerebellar functions and their likely role in the evolution of human tool use and speech.