Diurnality, nocturnality, and the evolution of primate visual systems.

Much of the recent research on the evolution of primate visual systems has assumed that a minimum number of shifts have occurred in circadian activity patterns over the course of primate evolution. The evolutionary origins of key higher taxonomic groups have been interpreted by some researchers as a consequence of a rare shift from nocturnality to diurnality (e.g., Anthropoidea) or from diurnality to nocturnality (e.g., Tarsiidae). Interpreting the evolution of primate visual systems with an ecological approach without parsimony constraints suggests that the evolutionary transitions in activity pattern are more common than what would be allowed by parsimony models, and that such transitions are probably less important in the origin of higher level taxa. The analysis of 17 communities of primates distributed widely around the world and through geological time shows that primate communities consistently contain both nocturnal and diurnal forms, regardless of the taxonomic sources of the communities. This suggests that primates in a community will adapt their circadian pattern to fill empty diurnal or nocturnal niches. Several evolutionary transitions from one pattern to the other within narrow taxonomic groups are solidly documented, and these cases probably represent a small fraction of such transitions throughout the Cenozoic. One or more switches have been documented among platyrrhine monkeys, Malagasy prosimians, Eocene omomyids, Eocene adapoids, and early African anthropoids, with inconclusive but suggestive data within tarsiids. The interpretation of living and extinct primates as fitting into one of two diarhythmic categories is itself problematic, because many extant primates show significant behavioral activity both nocturnally and diurnally. Parsimony models routinely interpret ancestral primates to have been nocturnal, but analyses of morphological and genetic data indicate that they may have been diurnal, or that early primate radiations were likely to have generated both nocturnal and diurnal forms, especially given the unusual annual light regimes faced by Early Tertiary primates living outside today's latitudinal tropics. We review the essential morphology and physiology of the primate visual system to look for features that might constrain evolutionary switches, and we find that the pattern of variation within and among primate groups in eye size, corneal size, retinal morphology, and opsin distribution are all consistent with the idea that there is considerable evolutionary flexibility in the visual system. These results suggest that primate lineages may evolve from diurnal to nocturnal, and vice versa, more readily and more rapidly than has been suggested by the use of strict parsimony models. This has implications for interpreting the fossil record and reconstructing key evolutionary events in primate evolution.

Tarsier-like locomotor specializations in the oligocene primate afrotarsius.

Tarsiers and extinct tarsier-like primates have played a central role in views of primate phylogeny and evolution for more than a century. Because of the importance of tarsiers in so many primatological problems, there has been particular interest in questions about the origin of tarsier specializations and the biogeography of early tarsioid radiations. We report on a new fossil of rare Afrotarsius that shows near identity to modern Tarsius in unique specializations of the leg, which provides information about the locomotor behavior and clarifies the phylogenetic position of this previously controversial primate. These specializations constitute evidence that Afrotarsius is a tarsiid, closely related to extant Tarsius; hence, it is now excluded from being a generalized sister taxon to Anthropoidea.

Evolutionary history of lorisiform primates.

We integrate information from the fossil record, morphology, behavior and molecular studies to provide a current overview of lorisoid evolution. Several Eocene prosimians of the northern continents, including both omomyids and adapoids, have been suggested as possible lorisoid ancestors, but these cannot be substantiated as true strepsirhines. A small-bodied primate, Anchomomys, of the middle Eocene of Europe may be the best candidate among putative adapoids for status as a true strepsirhine. Recent finds of Eocene primates in Africa have revealed new prosimian taxa that are also viable contenders for strepsirhine status. Plesiopithecus teras is a Nycticebussized, nocturnal prosimian from the late Eocene, Fayum, Egypt, that shares cranial specializations with lorisoids, but it also retains primitive features (e.g. four premolars) and has unique specializations of the anterior teeth excluding it from direct lorisiform ancestry. Another unnamed Fayum primate resembles modern cheirogaleids in dental structure and body size. Two genera from Oman, Omanodon and Shizarodon, also reveal a mix of similarities to both cheirogaleids and anchomomyin adapoids. Resolving the phylogenetic position of these Africa primates of the early Tertiary will surely require more and better fossils. By the early to middle Miocene, lorisoids were well established in East Africa, and the debate about whether these represent lorisines or galagines is reviewed. Neontological data are used to address the controversial branching sequences among extent lorisid clades. Data from the skin and scent glands, when integrated with other lines of evidence, suggest that Asian and African lorisines share a common lorisine ancestry. The hypothesis of an African clade containing both pottos and galagos to the exclusion of Asian lorisines is less tenable. True galagines are found in the fossil record of Namibia, while true lorisines are known from the Miocene of Asia. The hypothetical branching sequences can be integrated with behavioral and morphological features to develop an adaptive model of lorisoid divergence. By specializing on two different foraging modes early in their radiation, lorisines and galagines subsequently underwent a chain of integrated evolutionary changes eventually having an impact on many components of locomotor behavior, anatomy, physiology, reproduction, life history, and social behavior. Ongoing evolutionary studies of extant galagines are illuminating population phenomena and processes of speciation in an ecological context.

Skull of Catopithecus browni, an early tertiary catarrhine.

Fossil crania from quarry L-41, Fayum, Egypt, representing Catopithecus browni, a primate similar in size to callitrichids but with a catarrhine dental formula, provide the geologically earliest record of an anthropoidean skull. Catopithecus had postorbital closure developed to the stage seen in extant anthropoideans, with direct contact between zygomatic plate and maxillary tuber, isolating an anterior orbital fissure from the inferior orbital fissure. The auditory region also resembles that of later anthropoideans: The posterior carotid foramen is placed adjacent to the jugular fossa; a large promontory canal crosses the promontorium; and the annular ectotympanic is fused ventrally to the bulla. The incisors and canines show an assemblage of features found only among modern anthropoideans and adapoids. The face is characterized by a relatively deep maxilla, broad ascending wing of the premaxilla, and long nasal bones, yielding a moderate muzzle similar to that of Aegyptopithecus. The small braincase bears an anteriorly broad frontal trigon and a posteriorly developed sagittal crest. The mandibular symphysis is unfused even in mature adults. The encephalization quotient (EQ) probably falls within the range of Eocene prosimians, much lower than the EQs of Neogene anthropoideans.

A remarkable cranium of Plesiopithecus teras (Primates, Prosimii) from the Eocene of Egypt.

Between 1991 and 1993 specimens of a highly distinctive primate, named Plesiopithecus teras [Simons, E.L. (1992) Proc. Natl. Acad. Sci. USA 89, 10743-10747], were found at site L-41 in late Eocene deposits of the Fayum Depression, Egypt. The most important of these specimens consists of a nearly complete skull, which facilitates the evaluation of affinities of this primate. Characteristics of the known material now demonstrate that Plesiopithecus is a prosimian, although mandibular molar morphology, in particular, bears similarity to that in molars of archaic members of Anthropoidea. Plesiopithecus has a postorbital bar but lacks postorbital closure, it has upper molars without hypocones, and it may retain four lower premolars. Its familial rank was considered incertae sedis by Simons [Simons, E.L. (1992) Proc. Natl. Acad. Sci. USA 89, 10743-10747]; it can now be demonstrated that Plesiopithecus justifies establishment of a new family and superfamily. The new superfamily apparently lies closer to the toothcomb prosimians (strepsirhines) than to any other known primate group. Under this interpretation the enlarged, procumbent tooth in the jaw of Plesiopithecus is homologous to either the lateral incisor or the canine of the prosimian toothcomb.

Taxeopody in the carpus and tarsus of Oligocene Pliohyracidae (Mammalia: Hyracoidea) and the phyletic position of hyraxes.

Recent hyracoids and elephants share a taxeopode arrangement of tarsal and carpal bones, a condition in which bones are aligned with minimal interlocking between adjacent elements. Taxeopody has often been interpreted as a synapomorphy reflecting a close phyletic link between Hyracoidea and Proboscidea, but recently it has been suggested [Fischer, M. S. (1986) Cour. Forschungsinst. Senckenberg 84, 1-132] that hyracoid taxeopody is an independent acquisition resulting from selection favoring increased midcarpal and midtarsal rotation and that Hyracoidea is actually allied with Perissodactyla. As a test of this hypothesis, isolated carpal and tarsal bones of primitive Oligocene hyracoids from the Fayum, Egypt, have been examined to determine whether these indicate a taxeopode or diplarthral carpus and tarsus. Four complete astragali from the Fayum, representing at least three taxa, show a single, slightly convex articular surface on the head for articulation with the navicular and lack a facet for the cuboid. Two complete magna representing two species have a single proximal facet for articulation with the lunar, and they lack a facet for the scaphoid. Thus, both the carpus and tarsus of Fayum hyracoids are taxeopode. Taxeopody in hyracoids cannot be attributed to selection for carpal and tarsal rotation in climbers because the Oligocene, Miocene, and Recent species show great diversity in body size and probably locomotor specializations, despite relative uniformity of structure in the carpus and tarsus. The shared taxeopody of hyracoids and proboscideans, along with other osteological characters and similarities in hemoglobin, eye lens proteins, and other molecules, all suggest that Hyracoidea belongs within Paenungulata.

Cranial morphology of Aegyptopithecus and Tarsius and the question of the tarsier-anthropoidean clade.

New crania of the Oligocene anthropoidean Aegyptopithecus provide a test of the hypothesized tarsier-anthropoidean clade. Three cranial characters shared by Tarsius and some modern anthropoideans (apical interorbital septum, postorbital septum, "perbullar" carotid pathway) were examined. 1) An apical interorbital septum is absent in Aegyptopithecus. A septum does occur in Galago senegalensis (Lorisidae) and Microcebus murinus (Cheirogaleidae), so the presence of a septum is not strong evidence favoring a tarsiiform-anthropoidean clade. 2) In Aegyptopithecus and other anthropoideans, the postorbital septum is formed mainly by a periorbital flange of the zygomatic that extends medially from the lateral orbital margin onto or near the braincase. The postorbital plate of Tarsius is formed by frontal and alisphenoid flanges that extend laterally from the braincase to the zygomatic's frontal process, which is not broader than the postorbital bars of other prosimians. Periorbital flanges evolved in Tarsius for support or protection of the enormous eyes, as suggested by the occurrence of maxillary and frontal flanges that cup portions of the eye but do not separate it from temporal muscles. 3) The internal carotid artery of Aegyptopithecus enters the bulla posteriorly and crosses the anteroventral part of the promontorium. The tympanic cavity was probably separated from the anteromedial cavity by a septum stretching from the carotid channel to the ventrolateral bullar wall. In Tarsius, the carotid pathway is prepromontorial, and a septum stretches from the carotid channel to the posteromedial bullar wall. Quantitative analyses indicate that anterior carotid position has evolved because of erect head posture. The cranium of Oligocene anthropoideans thus provides no support for the hypothesized tarsier-anthropoidean clade.

Scaling of growth and life history traits relative to body size, brain size, and metabolic rate in lorises and galagos (Lorisidae, primates).

A broad range of variation in body size, brain size, and metabolic rate occurs within the primate family Lorisidae, thus providing an opportunity to examine the relationship of these three parameters to variation in growth and life history traits. Data on adult body weight, gestation length, lactation length, age at first estrus, litter size, and growth parameters were collected from a captive colony of four lorisid species, Loris tardigradus, Nycticebus coucang, Galago crassicaudatus, and G. senegalensis. The data presented here constitute the most complete life history information available for these poorly understood prosimian species. Correlation and allometric analyses were performed to determine the relationships between variables. Among the lorisids studied, adult body weight, adult cranial capacity, and relative cranial capacity did not predict variation in life history traits. Adult basal metabolic rate predicted most of the variability in gestation length, lactation length, and growth parameters. Lorisines differ from similarly sized galagines in having lower basal metabolic rates, slower growth rates, slower developmental rates, and smaller litter sizes, resulting in reduced reproductive potential. This may be a consequence of lorisine adaptation to a diet of toxic insects. Metabolic rate and diet may be among the most important parameters to examine in any study of life history evolution.

New specimens of Oligopithecus savagei, early Oligocene primate from the Fayum, Egypt.

New specimens of the early Oligocene anthropoidean, Oligopithecus savagei, from the Fayum, Egypt, include unworn specimens of lower teeth plus the first known upper molar, premolar, and incisor. These finds confirm the anthropoidean status of Oligopithecus. Comparisons with other Fayum taxa suggest that Oligopithecus is more closely related to Propliopithecidae than to Parapithecidae. Dental similarities between Oligopithecus and early platyrrhines are probably primitive retentions that do not support the hypothesis of an Oligocene trans-Atlantic crossing by primates. Among prosimians, the upper teeth of Oligopithecus very closely resemble those of Protoadapis and allied forms (Europolemur, Mahgarita, Periconodon, Hoanghonius), but differ substantially from other prosimian taxa. Most of the dental and osteological resemblances between Oligopithecus and the Protoadapis group are derived features, thus favoring the hypothesis that Oligopithecus and other Anthropoidea are descended from Adapidae.

A new species of Propliopithecus from the Fayum, Egypt.

Propliopithecus ankeli is described as a new species of hominoid from the early Oligocene of Egypt. The new species occurs at a stratigraphic level 80 m below quarries yielding P. chirobates and Aegyptopithecus zeuxis. P. ankeli differs from other species of the genus in its large size, relatively robust canines, larger and proportionally broader premolars, and M1 that has as great or greater mesiodistal length than M2. Thus, P. ankeli is characterized by increased relative size and robustness of the antemolar dentition, which contrasts with the pattern observed in the Fayum's other large hominoid, A. zeuxis. P. ankeli probably represents a lineage not ancestral to other Fayum hominoids. Discovery of this new species emphasizes the diversity of anthropoid primates that had already evolved by the early Oligocene.

Paleoenvironment of the earliest hominoids: new evidence from the oligocene avifauna of egypt.

Analysis of fossil birds from the Oligocene Jebel Qatrani Formation in the Fayum depression of Egypt, site of the oldest known hominoid primates, allows precise paleoenvironmental reconstruction of the climatic and biotic conditions that influenced some of the earliest stages of hominoid evolution. Unlike the fossil mammals of the Fayum, which belong largely to extinct groups, most of the birds are referable to living families, with some being close to modern genera. The avifauna consists mainly of aquatic species, with such forms as jacanas (Jacanidae) and shoebilled storks (Balaenicipitidae) indicating expanses of freshwater with dense floating vegetation. An avifauna closely analogous to that of the Fayum is found today only in a limited area of Uganda, north and west of Lake Victoria, a region of swampland bordered by forest and grasslands that presents marked faunal similarities to the environment inferred for the Egyptian Oligocene.

Cementum annulus counts provide a means for age determination in Macaca mulatta (primates, anthropoidea).

14 teeth of 8 rhesus macaques (Macaca mulatta) of known age were analyzed to assess the usefulness of cementum annuli counts as a means of estimating chronological age. Methods used were histological examination of stained thin sections by light microscopy, and examination of polished and etched epoxy-embedded sections by scanning electron microscopy. In 11 of 14 cases, the known chronological ages of the individuals fell within the predicted age ranges based on cementum annuli counts; in 2 other cases, it fell within half a year of the ranges. Cementum annulus counts can provide valuable information about the age of primates living in semitropical environments. This is the most accurate method for aging skeletally adult primates that has yet been tested on animals of known age.