The evolution of mammalian brain size.

Relative brain size has long been considered a reflection of cognitive capacities and has played a fundamental role in developing core theories in the life sciences. Yet, the notion that relative brain size validly represents selection on brain size relies on the untested assumptions that brain-body allometry is restrained to a stable scaling relationship across species and that any deviation from this slope is due to selection on brain size. Using the largest fossil and extant dataset yet assembled, we find that shifts in allometric slope underpin major transitions in mammalian evolution and are often primarily characterized by marked changes in body size. Our results reveal that the largest-brained mammals achieved large relative brain sizes by highly divergent paths. These findings prompt a reevaluation of the traditional paradigm of relative brain size and open new opportunities to improve our understanding of the genetic and developmental mechanisms that influence brain size.

The anatomy of Dolichocebus gaimanensis, a stem platyrrhine monkey from Argentina.

Dolichocebus is known from the type skull encased in a concretion, numerous isolated teeth, parts of two mandibles, and a talus. The specimens come from the Trelew Member (early Miocene, Colhuehuapian South American Land Mammal Age) of the Sarmiento Formation near the village of Gaiman, Chubut Province, Argentina, dated to about 20Ma. We describe all Dolichocebus fossil material using conventional surface anatomy and micro-CT data from the cranium. The new material and newly imaged internal anatomy of the skull demonstrate that anatomical characters hitherto supposed to support a phyletic link between Dolichocebus and either callitrichines (marmosets, tamarins, and Callimico) or Saimiri (squirrel monkeys) are either indeterminate or absent. To more fully explore the phyletic position of Dolichocebus, we undertook a comprehensive phylogenetic analysis. We examined 268 characters of the cranium and dentition of 16 living platyrrhine genera, some late Oligocene and early Miocene platyrrhines, Tarsius, some Eocene and Oligocene stem anthropoids, and several extant catarrhines. These analyses consistently indicate that Dolichocebus is a stem platyrrhine, as are late Oligocene Branisella and early Miocene Tremacebus, Soriacebus, and Carlocebus. Platyrrhine evolution often is conceived of as a single ancient adaptive radiation. Review of all available phyolgenetic data suggests a more layered evolutionary pattern, with several independent extinct clades filling modern platyrrhine niche space, and modern platyrrhine families and subfamilies appearing over a nine-million-year interval in the Miocene. The outcome of these analyses highlights the pervasiveness of homoplasy in dental and cranial characters. Homoplasy is a real evolutionary phenomenon that is present at all levels of biological analysis, from amino-acid sequences to aspects of adult bony morphology, behavior, and adaptation.

Anthropoid humeri from the late Eocene of Egypt.

A number of recent studies have, by necessity, placed a great deal of emphasis on the dental evidence for Paleogene anthropoid interrelationships, but cladistic analyses of these data have led to the erection of phylogenetic hypotheses that appear to be at odds with biogeographic and stratigraphic considerations. Additional morphological data from the cranium and postcranium of certain poorly understood Paleogene primates are clearly needed to help test whether such hypotheses are tenable. Here we describe humeri attributable to Proteopithecus sylviae and Catopithecus browni, two anthropoids from late Eocene sediments of the Fayum Depression in Egypt. Qualitative and morphometric analyses of these elements indicate that humeri of the oligopithecine Catopithecus are more similar to early Oligocene propliopithecines than they are to any other Paleogene anthropoid taxon, and that Proteopithecus exhibits humeral similarities to parapithecids that may be symplesiomorphies of extant (or "crown") Anthropoidea. The humeral morphology of Catopithecus is consistent with certain narrowly distributed dental apomorphies-such as the loss of the upper and lower second premolar and the development of a honing blade for the upper canine on the lower third premolar-which suggest that oligopithecines constitute the sister group of a clade containing propliopithecines and Miocene-Recent catarrhines and are not most closely related to Proteopithecus as has recently been proposed.

The recognition and evaluation of homoplasy in primate and human evolution.

Homoplasy has been a prominent issue in primate systematics and phylogeny for as long as people have been studying human evolution. In the past, homoplasy, in the form of parallel evolution, was often considered the dominant theme in primate evolution. Today, it receives blame for difficulties in phylogenetic analysis, but is essential in the study of adaptation. This paper reviews the history of study of homoplasy, methods of defining homoplasy, and methodological and biological factors that generate homoplasy. A post hoc definition of homology and homoplasy, based on patterns of character distributions and their congruence or incongruence on a cladogram, is the most consistent method of recognizing these phenomena. Defined this way, homology and homoplasy are mutually exclusive. However, when different levels of analysis are examined, it is seen that homoplasy at one level, such as adult phenotype, often exists simultaneously with homology at a different level, such as developmental process. Thus, in some cases, patterns of homoplasy may point to underlying similarities that reflect the shared heritage of a particular clade. This is an old concept that is being renewed on the strength of recent trends in developmental biology. Factors that influence homoplasy include character definition and a host of biological factors, such as developmental constraints, allometry, and adaptation. These interact with one another to provide explanations of homoplastic patterns. Because of the repetition of events, explanations of homoplastic features are often more reliable than those for homologous features, and serve as effective tests for hypotheses of evolutionary process. In some cases, particular explanations of homoplasy lead to generalizations about the likelihood of homoplasy in a type of structure. The structure may be adaptive or highly epigenetic, or it may belong to an anatomical system considered to be more prone to homoplasy than others. However, our review shows that these generalizations are usually based on theory, and contradictory expectations can be developed under different theoretical models. More rigorous empirical studies are necessary to discover what, if any, generalizations can be made about the likelihood of homoplasy in different types of characters.

Takeoff and landing forces of leaping strepsirhine primates.

Knowledge of the forces animals generate and are exposed to during locomotion is an important prerequisite for understanding the musculoskeletal correlates of locomotor modes. We recorded takeoff and landing forces for 14 animals representing seven species of strepsirhine primates with a compliant force pole. Our sample included both specialized vertical clingers and leapers and more generalized species. Takeoff forces are higher than landing forces. Peak forces during acceleration for takeoff ranged from 6 to 12 times body weight, and the peak impact forces at landing are between 5 and 9 times body weight. There is a size-related trend in peak force magnitudes. Both takeoff and landing forces decrease with increasing body size in our sample of animals from 1 kg to over 5 kg. Peak forces increase with distance leapt. The distance effect is less clear, probably due to the narrow range of distances represented in our sample. A comparison of subadult and adult animals of two species of sifakas reveals a tendency for the young animals to exert relatively higher peak forces in comparison to their adult conspecifics. Finally, Lemur catta and Eulemur rubriventer, the "generalists" in our sample, tend to generate higher forces for equal tasks than the specialized vertical clingers and leapers (i.e., the indriids and Hapalemur).A broad-scale comparison of peak leaping forces and peak forces for quadrupedal and bipedal walking and running shows that leaping at small body size is associated with exceptionally high forces. Whereas relative forces (i.e., forces divided by body weight) decrease with increasing body mass for leaping, forces for walking and running do not change much with size. Leaping forces in our sample scale to (mass)(-1/3), which is consistent with expectations derived from geometric similarity models. Forces associated with other locomotor activities do not appear to follow this pattern. The very high forces found in strepsirhine leapers do not seem to be matched by bone robusticity beyond that documented for quadrupedal species.

Canine sexual dimorphism in Egyptian Eocene anthropoid primates: Catopithecus and Proteopithecus.

Two very small late Eocene anthropoid primates, Catopithecus browni and Proteopithecus sylviae, from Fayum, Egypt show evidence of substantial sexual dimorphism in canine teeth. The degree of dimorphism suggests that these early anthropoids lived in social groups with a polygynous mating system and intense male-male competition. Catopithecus and Proteopithecus are smaller in estimated body size than any living primates showing canine dimorphism. The origin of canine dimorphism and polygyny in anthropoids was not associated with the evolution of large body size.

Skeletal and dental morphology supports diphyletic origin of baboons and mandrills.

Numerous biomolecular studies from the past 20 years have indicated that the large African monkeys Papio, Theropithecus, and Mandrillus have a diphyletic relationship with different species groups of mangabeys. According to the results of these studies, mandrills and drills (Mandrillus) are most closely related to the torquatus-galeritus group of mangabeys placed in the genus Cercocebus, whereas baboons (Papio) and geladas (Theropithecus) are most closely related to the albigena-aterrimus mangabeys, now commonly placed in the genus Lophocebus. However, there has been very little morphological evidence linking mandrills on the one hand and baboons and geladas on the other with different groups of mangabeys. In a study of mangabey locomotion and skeletal anatomy, we have identified features of the postcranial skeleton and the dentition that support the molecular phylogeny and clearly link mandrills with Cercocebus and Papio with Lophocebus. Moreover, the features linking Cercocebus and Mandrillus accord with ecological studies of these species indicating that these two genera are a cryptic clade characterized by unique adaptations for gleaning insects, hard nuts, and seeds from the forest floor.

Femoral anatomy of Aegyptopithecus zeuxis, an early oligocene anthropoid.

Three partial femora from Quarries I and M of the early Oligocene Jebel Qatrani Formation in the Fayum of Egypt are attributed to Aegyptopithecus zeuxis on the basis of their appropriate size and anthropoid morphology. Compared with extant catarrhines, Aegyptopithecus is unusual in having a distinct gluteal tuberosity (third trochanter) and a relatively deep distal femoral articulation. In the estimated neck angle, Aegyptopithecus resembles arboreal quadrupeds rather than either leaping or suspensory primates. It seems likely that the femur of this species was relatively robust and short for its body mass. In aspects of its femoral anatomy, Aegyptopithecus is quite different from the parapithecid Apidium and more similar to Catopithecus from late Eocene deposits of the Fayum, and also to small hominoids from the Miocene of East Africa.

Myological correlates of prosimian leaping.

Although the skeletal correlates of vertical clinging and leaping behavior in primates have been studied in great detail, myological information on this locomotor group is not readily available. We here provide relative muscle mass data for the hindlimb of four prosimian leapers, representing indriids as well as the small-bodied tarsiers and galagos. Wet weights of all hindlimb muscles, with the exception of the intrinsic muscles of the foot, were determined. For comparative purposes muscle weights were also gathered for Varecia, an arboreal quadruped, and previously unpublished dry muscle weights of several monkeys are included as well. The specialized leapers are characterized by a predominance of muscles for hindlimb joint extensions. Indriids have larger hip extensors than ankle plantarflexors, whereas the galago and tarsier display the reverse condition. This dichotomy in relative muscle mass corresponds to a dichotomy in leaping kinematics, with indriids going through a greater range of movement at the hip joint and galagos and tarsiers at the ankle joint. However, the most striking result is the overwhelming dominance of the quadriceps femoris muscle in both groups. This suggests that power may be transferred from the knee and thigh to adjacent joints and segments. In contrast, quadrupedal primates have more extensor musculature at the hip, suggesting that the need for a short swing phase pendulum constrains muscle mass distribution within the limb of quadrupeds. Total muscle mass of the hindlimb as well as the mass of the propulsive muscles scale with body mass at exponents below the functional equivalence expectation. Larger-bodied leapers therefore have less muscle force available per unit body weight to be propelled than their smaller-bodied counterparts.

First hominoid from the Miocene of Ethiopia and the evolution of the catarrhine elbow.

The first known fossil ape from the early-middle Miocene of Fejej, Ethiopia, is described here. The specimen, FJ-18SB-68, is a partial ulna from a locality dated by 40Ar/39Ar and paleomagnetic methods to a minimum age of 16.18 MYA. Compared to a variety of extant and fossil ulnae, FJ-18SB-68 is most similar to Turkanapithecus, Proconsul, and Pliopithecus, and appears to have been an arboreal quadruped with substantial forearm rotational mobility. Among the extant ulnae, canonical variates analysis successfully discriminates platyrrhines from catarrhines and within the latter, cercopithecoids from hominoids. Basal catarrhines (e.g., Aegyptopithecus) are platyrrhine-like in their morphology. Two basic trends appear to evolve from this generalized template: one with less mobile and more habitually pronated forearms, as seen in living and fossil cercopithecoids (including Victoriapithecus and Paracolobus), and another with greater forearm rotational mobility in fossil and modern hominoids. Primitive Miocene apes, including Proconsul, Turkanapithecus, and FJ-18SB-68, share with extant hominoids a more laterally positioned and laterally facing radial notch and an incipient trochlear keel. This morphology, along with a large insertion area for m. brachialis, suggests a departure from the more habitually pronated hand posture of monkeys and may indicate greater climbing abilities in these arboreally quadrupedal apes. Later Miocene apes, such as Oreopithecus and Dryopithecus share additional morphological features with hominoids, indicating considerable suspensory and climbing capabilities.

Geographic and climatic control of primate diversity.

Although the comparative ecology of primates has been relatively well studied and there have been a number of outstanding studies of individual primate communities, the factors determining primate species diversity on either a local or regional level are largely unexplored. Understanding the determinants of species abundance is an important aspect of biodiversity and is critical for interpreting the comparative ecology of these different communities and for designing effective strategies of conservation. Comparative analysis of species diversity in more than 70 primate communities from South America, Africa, Madagascar, and Asia shows that on major continental areas and large tropical islands, there is a high positive correlation between the number of primate species and the area of tropical forest. Within major continental areas, the species diversity at individual sites is highly correlated with mean annual rainfall for South America, Africa, and Madagascar, but not Asia.

Limb skeleton and locomotor adaptations of Apidium phiomense, an Oligocene anthropoid from Egypt.

Apidium phiomense is the most common primate from the early Oligocene deposits of Fayum, Egypt. It is known from hundreds of dental remains and dozens of skeletal remains, including numerous representatives of the long bones of the forelimb and hindlimb. Apidium phiomense was a small (1,600 g) arboreal quadruped. The forelimb bones of this species show features characteristic of arboreal quadrupeds and lack characteristic features found in the forelimb bones of vertial clingers, terrestrial quadrupeds, or suspensory species. The pelvis and hindlimb bones show numerous adaptations for leaping from a quadrupedal position. In general, Apidium lacks characteristic features of either cercopithecoid monkeys or hominoid apes. Overall, the skeleton shows greatest similarities to the same elements of small platyrrhines such as Saimiri and is also very similar to the hypothetical morphotype for ancestral platyrrhine. The skeleton of Apidium phiomense is the most primitive anthropoid postcranial skeleton known.

Kinetics of leaping primates: influence of substrate orientation and compliance.

Our current knowledge about the forces leapers generate and absorb is very limited and based exclusively on rigid force platform measurements. In their natural environments, however, leapers take off and land on branches and tree trunks, and these may be compliant. We evaluated the influence of substrate properties on leaping kinetics in prosimian leapers by using a combined field and laboratory approach. Tree sway and the timing of takeoffs relative to the movements of trees were documented for animals under natural conditions in Madagascar. Field data collected on three species (Indri indri, Propithecus diadema, Propithecus verreauxi) indicate that in the majority of takeoffs, the substrate sways and the animals takeoff before the elastic rebound of the substrate. This implies that force is "wasted" to deform supports. Takeoff and landing forces were measured in an experimental setting with a compliant force pole at the Duke University Primate Center. Forces were recorded for 2 Propithecus verreauxi and 3 Hapalemur griseus. Peak takeoff forces were 9.6 (P. verreauxi) and 10.3 (H. griseus) times body weight, whereas peak landing forces were 6.7 (P. verreauxi) and 8.4 (H. griseus) times body weight. As part of the impulse generated does not translate into leaping distance but is used to deform the pole, greater effort is required to reach a given target substrate, and, consequently, takeoff forces are high. The landing forces, on the other hand, are damped by the pole/substrate yield that increases the time available for deceleration. Our results contrast with previous studies of leaping forces recorded with rigid platform measuring systems that usually report higher landing than takeoff forces. We conclude that 1) Leapers generate and are exposed to exceptionally high locomotory forces. The takeoff forces are higher than the landing forces when using compliant supports, indicating that the takeoff rather than the landing may be critical in interpreting leaping behavior and related aspects of musculoskeletal design. 2) Large-bodied vertical clingers and leapers do not usually take advantage of the elastic energy stored in substrates. Rather, force (and energy) is wasted to deform compliant supports. 3) A compliant force pole approximates the conditions faced by large-bodied vertical clingers and leapers in the wild more closely than do rigid force platforms.

Partial humeri of two Miocene Colombian primates.

Distal portions of humeri from two Miocene Colombian primates were recovered during field work in 1986. The larger IGM 183420 is very similar in size and morphology to the humerus included in the type specimen of Cebupithecia sarmientoi, recovered from La Venta in 1945 (Stirton and Savage: Serv. Geol. Nac. Bogata 7:345-356, 1951) and is assigned to this taxon. IGM 183420 presents a number of features of the humerus associated with clinging postural behaviors in living platyrrhines, including a medial epicondyle with very little dorsal angulation, a cylindrical trochlea, and a contact facet for the coronoid process of the ulna. In these and other features Cebupithecia most closely resembles the extant genus Pithecia. IGM 183512 is approximately the size of Saimiri sciureus and is very similar in morphology to the humerus of this small arboreal quadruped. The medial epicondyle is more dorsally angled, the medial lip of the trochlea is more pronounced and the capitulum is less spherical as compared to Cebupithecia. This fossil is assigned to the taxon Neosaimiri fieldsi.

Sexual dimorphism in Laccopithecus robustus, a late miocene hominoid from China.

Laccopithecus robustus is a siamang-sized fossil ape from the Miocene site of Lufeng, China. The species is known from a partial cranium, numerous mandibles, and scores of isolated teeth. This species shows striking dental similarities to Pliopithecus from the Miocene of Europe and a number of cranial similarities to extant gibbons. Laccopithecus differs from extant gibbons and resembles other fossil and extant apes in showing marked sexual dimorphism in the size and shape of the canines and anterior lower premolars. Evidence for sexual differences in either the size or shape of other teeth is less clear. There is some evidence for a sexual size dimorphism based on the variability of molar teeth.

Fossil platyrrhine forelimb bones from the early miocene of Argentina.

Primate scapula and ulna fragments of uncertain taxonomic affinity (MACN-SC 101) have been recovered from the Pinturas deposits at Arroyo Feo, Santa Cruz, Argentina in association with Santacrucian (Early Miocene) land mammals. Least-squares regression of body weight on surface area and on height of the glenoid fossa of the scapula indicates an estimated mean weight of 3.6 kg for this individual. On the basis of qualitative and several metric features, the fossil scapula and ulna most closely resemble living platyrrhine monkeys. In estimated body weight and relative height of the coronoid process, the fossil is similar to arboreal quadrupeds, such as Cebus apella and Chiropotes. However, spinoglenoid, axilloglenoid, and axillospinal angles, length of lever arm, and length and breadth of the sigmoid notch imply behavioral similarity with larger species that also use their forelimbs extensively in climbing, such as Alouatta and Lagothrix. MACN-SC 101 may represent the incipient divergence of a generalized platyrrhine arboreal quadruped toward a more suspensory form.

Age of the earliest african anthropoids.

The earliest fossil record of African anthropoid primates (monkeys and apes) comes from the Jebel Qatrani Formation in the Fayum depression of Egypt. Reevaluation of both geologic and faunal evidence indicates that this formation was deposited in the early part of the Oligocene Epoch, more than 31 million years ago, earlier than previous estimates. The great antiquity of the fossil higher primates from Egypt accords well with their primitive morphology compared with later Old World higher primates. Thus, the anthropoid primates and hystricomorph rodents from Fayum are also considerably older than the earliest higher primates and rodents from South America.

New primate fossils from late Oligocene (Colhuehuapian) localities of Chubut Province, Argentina.

New primate fossils have been recovered from the late Oligocene (Colhuehuapian) localities of Gaiman and Sacanana in Patagonian Argentina. The new fossils are provisionally allocated to Dolichocebus gaimanensis and Tremacebus harringtoni, the only primates previously described from these localities. These new dental remains are more primitive than the teeth of any previously known platyrrhines, living or fossil, and conform extremely well with the hypothetical ancestral morphotype for New World monkeys suggested by several authors. They are also very similar to the teeth of Oligocene catarrhines from Egypt such as Aegyptopithecus zeuxis.

The humerus of Aegyptopithecus zeuxis: a primitive anthropoid.

Two complete humeri of Aegyptopithecus zeuxis have been recovered from Oligocene deposits in the Fayum Province of Egypt. These new specimens support previous interpretations of the locomotor adaptations of this species and indicate that A. zeuxis was a robust, slowly moving arboreal quadruped. While the previously described distal articular region of the humerus is virtually identical with the same region in many extant ceboids and the Miocene hominoid Pliopithecus vindobonensis, the more proximal parts of the humerus show many primitive "prosimianlike" features not found the limbs of extant anthropoids. The primitive features include the absence of a distinct deltoid plane, a broad shallow bicipital groove, a large brachialis flange, and an entepicondylar foramen. In most features, the humerus of Aegyptopithecus zeuxis is more primitive than the hypothetical last common ancestor of extant cercopithecoids and hominoids based on neontological comparisons. This supports other lines of evidence indicating that the hominoids from the Egyptian Oligocene are morphologically ancestral to both Old World monkeys and apes.