Paranasal pneumatization in extant and fossil Cercopithecoidea

Unlike most primates, extant cercopithecoids lack maxillary sinuses, which are pneumatic spaces in the facial skeleton lateral of the nasal cavity proper. Character state analysis of living cercopithecoids across well-supported topologies suggests that the sinus was lost at the origin of the superfamily, only to have evolved again convergently in extant macaques. Recent work has shown that a) the 'early loss' hypothesis is supported by the lack of any pneumatization in Victoriapithecus, a stem cercopithecoid, b) like extant macaques, the fossil cercopithecine Paradolichopithecus shows evidence of presence of the maxillary sinus (MS), and c) unlike extant colobines, the fossil colobine Libypithecus also possesses a maxillary sinus. To more fully assess the pattern of cercopithecoid sinus evolution, fossil taxa from both subfamilies (Colobinae, Cercopithecinae) were examined both visually and by computed tomography (CT). The observations were evaluated according to standard anatomical criteria for defining sinus spaces, and compared with data from all extant Old World monkey genera. Most taxa examined conformed to the pattern already discerned from extant cercopithecoids. Maxillary sinus absence in Theropithecus oswaldi, Mesopithecus, and Rhinocolobus is typical for all extant cercopithecids except Macaca. The fossil macaque Macaca majori possesses a well-developed maxillary sinus, as do all living species of the genus. Cercopithecoides, on the other hand, differs from all extant colobines in possessing a maxillary sinus. Thus, paranasal pneumatization has reemerged a minimum of two and possibly three times in cercopithecoids. The results suggest that maxillary sinus absence in cercopithecoids is due to suppression, rather than complete loss.     

The term "lateral recess" and craniofacial pneumatization in old world monkeys (Mammalia, Primates, Cercopithecoidea)

The primate superfamily Cercopithecoidea (or Old World monkeys) is characterized by a widespread lack of the maxillary sinus, a paranasal pneumatic space found in most other eutherian mammals. Previous discussions of the distribution of pneumatization in the group, however, have been ambiguous and contradictory, and have been further complicated by discussion of a poorly defined structure named the "lateral recess," linked implicitly to the maxillary sinus. Computed tomography (CT) was applied to dry crania of all cercopithecoid genera to evaluate the morphological relevance of the term "lateral recess." Results suggest that the "lateral recess" is a structural consequence of changes in skull form unrelated to pneumatization. Thus, the term should be abandoned. All Old World monkeys (except the genus Macaca) are found to lack the maxillary sinus, but a previously undescribed bulla, only separated from the nasal cavity anteriorly, was discovered in the Chinese golden monkey Rhinopithecus. If this bulla is related to the paranasal sinuses, it suggests that the initial change in cercopithecoid cranial evolution was a suppression of pneumatic development, which may have been subsequently reversed twice in the history of the group, in Macaca and Rhinopithecus.     

Extensive enlargement of the maxillary sinus in Alouatta caraya (mammalia, primates, cebidae): an allometric approach to skull pneumatization in Atelinae

In contrast to the paranasal sinuses of Old World monkeys and hominoids, little information is available about the paranasal sinuses of New World monkeys. Because this information is crucial in order to draw further conclusions about the evolution and biological role of skull pneumatization, this study investigates the morphology of the paranasal sinuses in adult black-and-gold howler monkeys (Alouatta caraya). Volumes of the paranasal sinuses were calculated using computer software (SURFdriver or Allegro) from serial coronal CT scans of 20 skulls of both sexes. Skull pneumatization in A. caraya is more complex than in other higher primates. In both sexes, the maxillary sinus (MS) is the only pneumatic cavity and enlarges regularly into neighboring bones such as the frontal bone and the basisphenoid. The resulting pansinus is often partitioned by several vertical septa. As in most external cranial dimensions, mean MS volume of A. caraya (male 4.08 cm(3); female 2.00 cm(3)) shows significant sexual dimorphism. Reduced major axis regression analysis between MS volume and different cranial dimensions for A. caraya (and for available data from other platyrrhines) suggests a distinct association for this group, with Alouatta having one of the largest pneumatic cavities. The combination of this unusual expansion of the MS of Alouatta and the occurrence of distinct septa within the sinus may be a consequence of the distinct skull architecture of Alouatta.     

The maxillary sinus of Paradolichopithecus sushkini (late Pliocene, southern Tajikistan) and its phyletic implications

Paradolichopithecus sushkini is a large fossil cercopithecine from the late Pliocene discovered at Kuruk-Say, southern Tajikistan. Despite its rather long face and large size, many authorities regard Paradolichopithecus not as a baboon, but as a large macaque, mainly based on the cranial morphology of European specimens. Among Old World monkeys, macaques are the only species that possess a maxillary sinus. Thus, we evaluated the presence/absence and morphology of this feature in P. sushkini using computed tomography (CT) scans of two Kuruk-Say cranial specimens in order to assess this species' taxonomic affinities. One of the specimens shows a thin bony wall separating a small area from the nasal cavity. Posterior to this structure is a pair of bony ridges: one protrudes from the alveolar process and the other descends from the superior portion of the nasal wall. A similar configuration was detected in the other specimen. These features strongly suggest the presence of a maxillary sinus in this species. This interpretation is supported by the fact that the superior portion of the alveolar process is excavated in the adult specimen. Thus, both specimens exhibit a maxillary sinus expanding laterally to share the external thin wall of the muzzle, and such a configuration may depend on the reduction of the maxillary bone, i.e., the presence of a maxillary fossa. The Kuruk-Say specimens probably retained a small maxillary sinus, despite the reduced size of the maxillary body. Thus, based on this evidence, P. sushkini probably belongs to the macaque lineage rather than that of baboons, although structural influences of the maxillary fossa leading to formation of the maxillary sinus have yet to be evaluated in extant macaques and baboons.     

Victoriapithecus: The key to Old World monkey and catarrhine origins

The past ten years have witnessed major changes in reconstructions of the history of Old World monkeys, most of them driven by new material of the Miocene monkey Victoriapithecus from Maboko Island, Kenya. Before the mid-1980s, predictions about the morphological and ecological adaptations of the earliest cercopithecoids relied heavily on evidence from extant colobine and cercopithecine monkeys. It was argued that the earliest cercopithecoids were largely or at least partly folivorous, had short colobine-like faces, and were arboreal. The only studies suggesting that some of these arguments were not true were based on limited knowledge of the anatomy of Victoriapithecus. The presence of semi-terrestrial adaptations in middle Miocene monkeys hinted to some that early monkeys may not have been arboreal. Others attempted to cope with the discrepancy between neontological predictions and the fossil evidence by proposing that limb bones with stronger terrestrial adaptations within the Maboko sample were derived cercopithecine remains, while those with more arboreal features belonged in the subfamily Colobinae and should be regarded as primitive.     

Isometric scaling of maxillary sinus volume in hominoids

Previous hypotheses of maxillary sinus size evolution have proposed one or more changes in the volume of the structure across hominoid phylogeny. These hypotheses have been used subsequently to support the phylogenetic placement of fossil taxa relative to the living Hominoidea. The null hypothesis, that no change in sinus volume independent of size has occurred in ape evolution, is evaluated here by scaling analysis. Mixed sex samples of adult dry crania for the extant ape genera were examined by computer tomography imaging and the volume of the maxillary sinus was obtained. Sinus volume was then regressed, using both least squares and reduced major axis models, against cranial size variables.The results clearly demonstrate that the null hypothesis of no change in relative sinus volume cannot be rejected; thus, there is no support for hypotheses that maxillary sinus volume, independent of cranial size, has changed in the course of hominoid evolution. This result, in turn, has implications for the phylogenetic placement of fossil taxa and highlights the need for the careful delineation of character states in studies of hominoid systematics.     

Origins of New World monkeys

Fossil ceboid evidence is reviewed with reference to the origins and affinities of the New World monkeys. This evidence indicates that the ceboids evolved from a North American primate of omomyid-like form. The events of continental drift apparently had little to do with the origin and dispersion of the New World monkeys and direct relationships to the Old World monkeys are not indicated. Three of the five extant New World monkey subfamilies are represented in late Miocene deposits of South America and it appears that evolutionary events leading to extant Ceboidea occurred within the South American continent.     

On the loss of uricolytic activity during primate evolution--I. Silencing of urate oxidase in a hominoid ancestor

Urate oxidase activity is not detectable in liver homogenates from the gibbon, orangutan, chimpanzee, gorilla and human. Liver homogenates from five genera of Old World and two genera of New World monkeys have easily detectable levels of urate oxidase activity. There is no evidence for extant detectable intermediate steps in the loss of urate oxidase activity in the hominoids. Urate oxidase activity from Old World and New World monkeys is stable, a simple observation which debunks a long-standing myth. Urate oxidase activity was silenced in an ancestor to the five living genera of hominoids after divergence from the Old World monkeys.     

Comparative assessment of the ischial morphology of Victoriapithecus macinnesi

An almost complete primate ischium was recovered from middle Miocene (ca. 15 ma) deposits of Maboko Island (Kenya) in 1987. The specimen shows numerous similarities to the ischial morphology of extant cercopithecids and is attributed to Victoriapithecus macinnesi (Von Koenigswald, 1969), the early Old World monkey best known from Maboko Island. The Victoriapithecus ischium provides the first evidence of early Old World monkey pelvic girdle anatomy. The ischium is characterized by an obliquely oriented and broadly flaring tuberosity, a relatively small acetabulum with little ventrally directed curvature of its caudal portion, a long ischial body and a flange-like ischial spine positioned caudal to the rim of the acetabulum. In these features, Victoriapithecus most closely resembles the vervet monkey, Cercopithecus aethiops. The fossil specimen indicates that Victoriapithecus possessed ischial callosities, a mobile tail and adaptations for (possibly cursorial) quadrupedalism with an adducted posture of the thigh. The occurrence of ischial callosities in Victoriapithecus extends the documented antiquity of this feature in catarrhines by more than 12 million years and shows that the distinctive “sitting-sleeping” adaptations of Old World monkeys (Washburn, 1957) originated prior to the divergence of Colobinae and Cercopithecinae. Differences of developmental sequence and tissue composition indicate that the ischial pads of cercopithecids, hylobatids, and pongids may have arisen independently, through parallel evolution. Contrary to Strasser and Delson (1987), discontinuity of ischial callosities was probably the primitive condition for male cercopithecids.     

Patterns of cranial shape diversification during the phylogenetic branching process of New World monkeys (Primates: Platyrrhini)

One of the central topics in evolutionary biology is understanding the processes responsible for phenotypic diversification related to ecological factors. New World monkeys are an excellent reference system to investigate processes of diversification at macroevolutionary scales. Here, we investigate the cranial shape diversification related to body size and ecology during the phylogenetic branching process of platyrrhines. To investigate this diversification, we used geometric morphometric techniques, a molecular phylogenetic tree, ecological data and phylogenetic comparative methods. Our statistical analyses demonstrated that the phylogenetic branching process is the most important dimension to understand cranial shape variation among extant platyrrhines and suggested that the main shape divergence among the four principal platyrrhine clades probably occurred during the initial branching process. The phylogenetic conservatism, which is the retention of ancestral traits over time within the four principal platyrrhine clades, could be the most important characteristic of platyrrhine cranial shape diversification. Different factors might have driven early shape divergence and posterior relative conservatism, including genetic drift, stabilizing selection, genetic constraints owing to pleiotropy, developmental or functional constraint, lack of genetic variation, among others. Understanding the processes driving the diversification among platyrrhines will probably require further palaeontological, phylogenetic and comparative studies.     

Variation in maxillary sinus anatomy among platyrrhine monkeys

Variations in the maxillary sinus anatomy of extant and fossil catarrhine primates have been extensively examined using computed tomography (CT), and have potential utility for phylogenetic analyses. This approach has also been used to demonstrate its anatomical variation in eight of the 16 extant genera of platyrrhines and the absence of the sinus in Saimiri and Cacajao. We used this approach to evaluate the three-dimensional anatomy of the maxillary sinus in all extant platyrrhine genera, and here argue the phylogenic implications of this variation. This study confirms, for the most part, previous CT studies and augments them with the six genera not studied previously: Ateles, Lagothrix, Callithrix, Cebuella, Pithecia and Chiropotes. The entire maxilla is pneumatized by the sinus in the atelines, Cebus, and Callicebus, whereas the sinus pneumatizes only the medial part of the maxilla in the callitrichines and Aotus. Pithecia has a unique conformation in which the maxillary sinus and the expanded inferior meatus pneumatize the posteromedial and anterolateral parts of the entire maxilla, respectively. Chiropotes has no sinus, and the inferior meatus possibly expands into the area between the middle meatus and medial surface of the maxilla to disturb sinus formation, as in the case of its close relative Cacajao. Finally, we argue that the sinus that pneumatizes the entire maxilla is a primitive feature in extant platyrrhines and was probably shared by the last common ancestor of the anthropoids.     

The phylogeny of Old World monkeys

The living Old World monkeys, family Cercopithecidae, are the most successful group of nonhuman primates alive today. Overall, they account for over one quarter of the extant genera of primates and approximately 40% of the species. They have an extensive fossil record extending back to the early and middle Miocene of Africa.^1,2 Despite this specific diversity and a long evolutionary history, it is commonly argued that the group is relatively uniform in both its skeletal³ and dental⁴ anatomy, suggesting that much of the current taxonomic diversity is a relatively recent phenomenon. In such a species group, it is perhaps not surprising that the taxonomy of Old World monkeys is subject to many differing classifications. Thus, in recent years, authors have recognized as few as 10 and as many as 22 different genera within the family. Although some of this greater-than-two-fold difference in the number of genera can be attributed to the “splitting” versus “lumping” philosophies of different researchers, much of it is based on major disagreements over phylogenetic relationships. Recent studies of the genetics and chromosomes of this group have illuminated Old World monkey phylogeny in many ways. Some of these studies have resolved longstanding debates based on morphological data; others have revealed phylogenetic relationships that morphologists had never suspected.     

Pattern in craniofacial biology: Evidence from the old world monkeys (Cercopithecidae)

An understanding of craniofacial growth, both evolutionarily and clinically, requires an investigation of pattern —geometric relations that remain relatively constant among growing structures or components of the skull. Several craniofacial biologists have suggested that specific morphological relations remain invariant during growth and in interspecific comparisons of adults of varying size. We tested the hypothesized invariance of a series of craniofacial angles in a sample of adult Old World monkeys. Fifteen angles were determined from lateral cranial radiographs. Criteria for examining angular invariance included tests for significant correlations and regression slopes with palatal length (overall skull size), tests for significant mean differences (ANOVAs) in angular values between the two subfamilies of Cercopithecidae — Cercopithecinae and Colobinae — and the computation and ranking of standard deviations (SDs) and coefficients of variation (CVs). Results indicate that most of the cranial angles purported to be invariant do not in fact meet the criteria for acceptance. One of the few cranial angles that evinces a somewhat constant value is that between the posterior maxillary plane and the neutral axis of the orbits, providing very limited support for Enlow’s (1982) claim that this region represents a fundamental anatomical interface (at least within Old World monkeys). Our analysis suggests that while there may be several relatively invariant structural relations within the skull, most of those previously discussed as representing evidence of pattern in primate-wide or mammal-wide comparisons are incorrect.     

The geologic history of the Lythraceae

The known fossil record of the Lythraceae has been amplified by recent studies in northern Latin America. A total of 18 genera is recognized in geologic strata ranging in age from lower Eocene to Recent, and among the 22 or 23 modern genera, seven have a documented geologic history. The oldest remains are from an Indo-Malayan Old World warm-temperate to subtropical vegetation preserved in the lower Eocene London Clay flora. The most ancient of extant genera isLagerstroemia and the most recent (among those with an adequate fossil record) isCuphea (middle Miocene to Recent). These represent, respectively, primitive and advanced members of the family, and the paleobotanical record supports current concepts concerning phylogenetic relationships among genera of the Lythraceae. The family apparently had an Old World origin and became differentiated into a distinct modern taxon during Paleocene and early Eocene time.     

THE PHYLOGENETIC RELATIONSHIPS AND BIOGEOGRAPHY OF TRUE PORPOISES (MAMMALIA: PHOCOENIDAE) BASED ON MORPHOLOGICAL DATA

Prior studies of phylogenetic relationships among phocoenids based on morphology and molecular sequence data conflict and yield unresolved relationships among species. This study evaluates a comprehensive set of cranial, postcranial, and soft anatomical characters to infer interrelationships among extant species and several well-known fossil phocoenids, using two different methods to analyze polymorphic data: polymorphic coding and frequency step matrix. Our phylogenetic results confirmed phocoenid monophyly. The division of Phocoenidae into two subfamilies previously proposed was rejected, as well as the alliance of the two extinct genera Salumiphocaena and Piscolithax with Phocoena dioptrica and Phocoenoides dalli . Extinct phocoenids are basal to all extant species. We also examined the origin and distribution of porpoises within the context of this phylogenetic framework. Phocoenid phylogeny together with available geologic evidence suggests that the early history of phocoenids was centered in the North Pacific during the middle Miocene, with subsequent dispersal into the southern hemisphere in the middle Pliocene. A cooling period in the Pleistocene allowed dispersal of the southern ancestor of Phocoena sinus into the North Pacific (Gulf of California).     

Pattern in craniofacial biology: Evidence from the old world monkeys (Cercopithecidae)

An understanding of craniofacial growth, both evolutionarily and clinically, requires an investigation of pattern —geometric relations that remain relatively constant among growing structures or components of the skull. Several craniofacial biologists have suggested that specific morphological relations remain invariant during growth and in interspecific comparisons of adults of varying size. We tested the hypothesized invariance of a series of craniofacial angles in a sample of adult Old World monkeys. Fifteen angles were determined from lateral cranial radiographs. Criteria for examining angular invariance included tests for significant correlations and regression slopes with palatal length (overall skull size), tests for significant mean differences (ANOVAs) in angular values between the two subfamilies of Cercopithecidae — Cercopithecinae and Colobinae — and the computation and ranking of standard deviations (SDs) and coefficients of variation (CVs). Results indicate that most of the cranial angles purported to be invariant do not in fact meet the criteria for acceptance. One of the few cranial angles that evinces a somewhat constant value is that between the posterior maxillary plane and the neutral axis of the orbits, providing very limited support for Enlow’s (1982) claim that this region represents a fundamental anatomical interface (at least within Old World monkeys). Our analysis suggests that while there may be several relatively invariant structural relations within the skull, most of those previously discussed as representing evidence of pattern in primate-wide or mammal-wide comparisons are incorrect.     

A nesting of vipers: Phylogeny and historical biogeography of the Viperidae (Squamata: Serpentes)

Despite their medical interest, the phylogeny of the snake family Viperidae remains inadequately understood. Previous studies have generally focused either on the pitvipers (Crotalinae) or on the Old World vipers (Viperinae), but there has been no comprehensive molecular study of the Viperidae as a whole, leaving the affinities of key taxa unresolved. Here, we infer the phylogenetic relationships among the extant genera of the Viperidae from the sequences of four mitochondrial genes (cytochrome b, NADH subunit 4, 16S and 12S rRNA). The results confirm Azemiops as the sister group of the Crotalinae, whereas Causus is nested within the Viperinae, and thus not a basal viperid or viperine. Relationships among the major clades of Viperinae remain poorly resolved despite increased sequence information compared to previous studies. Bayesian molecular dating in conjunction with dispersal-vicariance analysis suggests an early Tertiary origin in Asia for the crown group Viperidae, and rejects suggestions of a relatively recent, early to mid-Tertiary origin of the Caenophidia.     

Molecular phylogeny of Old World monkeys (Cercopithecidae) as inferred from gamma-globin DNA sequences

DNA sequence data of the nuclear-encoded gamma1-gamma2-globin duplication region were used to examine the phylogenetic relationships of 16 cercopithecid (Old World monkey) species representing 12 extant genera. Morphology- and molecular-based hypotheses of Old World monkey branching patterns are generally congruent, except for generic relationships within the subtribe Papionina. The cercopithecids divide into colobines (leaf-eating monkeys) and cercopithecines (cheek-pouched monkeys). The colobines examined by the DNA data divide into an Asian clade (Nasalis, proboscis monkeys; Trachypithecus, langurs) and an African clade (Colobus, colobus monkeys). The cercopithecines divide into tribes Cercopithecini (Erythrocebus, patas monkey; Chlorocebus, green monkeys; Cercopithecus, guenons) and Papionini. Papionins divide into subtribes Macacina (Macaca, macaques) and Papionina (Papio, hamadryas baboons; Mandrillus, drills and mandrills; Theropithecus, gelada baboons; Lophocebus, arboreal mangabeys; Cercocebus, terrestrial mangabeys). In a morphologically based classification, Mandrillus is a subgenus of Papio, whereas Lophocebus is a subgenus of Cercocebus. In contrast, the molecular evidence treats Mandrillus as a subgenus of Cercocebus, and treats both Theropithecus and Lophocebus as subgenera of Papio. Local molecular clock divergence time estimates were used as a yardstick in a "rank equals age" system to propose a reduction in taxonomic rank for most clades within Cercopithecidae.     

A novel family of tRNA-derived SINEs in the colugo and two new retrotransposable markers separating dermopterans from primates

Short interspersed nuclear elements (SINEs) provide a near homoplasy free and copious source of molecular evolutionary markers with precisely defined character polarity. Used as molecular cladistic markers in presence/absence analyses, they represent a powerful complement to phylogenetic reconstructions that are based on sequence comparisons on the level of nucleotide substitutions. Recent sequence comparisons of large data sets incorporating a broad eutherian taxonomic sample have led to considerations of the different primate infraorders to constitute a paraphyletic group. Statistically significant support against the monophyly of primates has been obtained by clustering the flying lemur-also termed colugo-(Cynocephalus, Dermoptera) amidst the primates as the sister group to anthropoid primates (New World monkeys, Old World monkeys, and hominoids). We discovered retrotransposed markers that clearly favor the monophyly of primates, with the markers specific to all extant primates but definitively absent at the orthologous loci in the flying lemur and other non-primates. By screening the colugo genome for phylogenetic informative SINEs, we also recovered a novel family of dermopteran specific SINE elements that we call CYN. This element is probably derived from the isoleucine tRNA and appears in monomeric, dimeric, and trimeric forms. It has no long tRNA unrelated region and no poly(A) linker between the monomeric subunits. The characteristics of the novel CYN-SINE family indicate a relatively recent history. Therefore, this SINE family is not suitable to solve the phylogenetic affiliation between dermopterans and primates. Nevertheless it is a valuable device to reconstruct the evolutionary steps from a functional tRNA to an interspersed SINE element.     

Comparative microcomputed tomography and histological study of maxillary pneumatization in four species of new world monkeys: the perinatal period

In anthropoid primates, it has been hypothesized that the magnitude of maxillary sinus growth is influenced by adjacent dental and soft tissue matrices. Relatively, little comparative evidence exists for the perinatal period when secondary pneumatization is at its earliest stages in some primates. Here, dental and midfacial variables were studied in a perinatal sample of four anthropoid primates, including three callitrichines (Leontopithecus, Saguinus, and Callithrix) and Saimiri boliviensis. In the latter species, the maxillary recess (the ontogenetic precursor to a "true" maxillary sinus) does not undergo secondary pneumatization. Using histological methods and micro-computed tomography, midfacial and dental dimensions and radiographic hydroxyapatite density of tooth cusps were measured. The distribution of osteoclasts and osteoblasts was also documented. Kruskal-Wallis's one-way analysis of variance tests indicates significant (P < 0.05) differences among groups for dental and midfacial measurements. In particular, the posterior maxillary dentition is relatively larger and more mineralized in Saimiri compared to the callitrichines. At posterior dental levels, Saimiri has the lowest palatonasal index [interdental (palatal) width/width of the nasal cavity] and highest bizygomatic-interorbital index. Distribution of osteoclasts indicates that the inferomedial surfaces of the orbits are resorptive in perinatal Saimiri, whereas, in all callitrichines, these surfaces are depository. Taken together, these findings suggest that pneumatization in Saimiri is suppressed by an inward growth trajectory of the orbits, relatively large posterior dentition, and a correspondingly compressed nasal region.