Convergent evolution of anthropoid-like adaptations in Eocene adapiform primates.

Adapiform or 'adapoid' primates first appear in the fossil record in the earliest Eocene epoch ( approximately 55 million years (Myr) ago), and were common components of Palaeogene primate communities in Europe, Asia and North America. Adapiforms are commonly referred to as the 'lemur-like' primates of the Eocene epoch, and recent phylogenetic analyses have placed adapiforms as stem members of Strepsirrhini, a primate suborder whose crown clade includes lemurs, lorises and galagos. An alternative view is that adapiforms are stem anthropoids. This debate has recently been rekindled by the description of a largely complete skeleton of the adapiform Darwinius, from the middle Eocene of Europe, which has been widely publicised as an important 'link' in the early evolution of Anthropoidea. Here we describe the complete dentition and jaw of a large-bodied adapiform (Afradapis gen. nov.) from the earliest late Eocene of Egypt ( approximately 37 Myr ago) that exhibits a striking series of derived dental and gnathic features that also occur in younger anthropoid primates-notably the earliest catarrhine ancestors of Old World monkeys and apes. Phylogenetic analysis of 360 morphological features scored across 117 living and extinct primates (including all candidate stem anthropoids) does not place adapiforms as haplorhines (that is, members of a Tarsius-Anthropoidea clade) or as stem anthropoids, but rather as sister taxa of crown Strepsirrhini; Afradapis and Darwinius are placed in a geographically widespread clade of caenopithecine adapiforms that left no known descendants. The specialized morphological features that these adapiforms share with anthropoids are therefore most parsimoniously interpreted as evolutionary convergences. As the largest non-anthropoid primate ever documented in Afro-Arabia, Afradapis nevertheless provides surprising new evidence for prosimian diversity in the Eocene of Africa, and raises the possibility that ecological competition between adapiforms and higher primates might have played an important role during the early evolution of stem and crown Anthropoidea in Afro-Arabia.

Last of the oligopithecids? A dwarf species from the youngest primate-bearing level of the Jebel Qatrani Formation, northern Egypt.

Oligopithecids are basal stem catarrhines that make their first definitive appearance in the fossil record in the latest Eocene of Egypt. Previously, the group was assumed to have gone locally extinct in northern Africa shortly after the Eocene-Oligocene boundary, with a last record at the ∼31.5 Ma Taqah locality in Oman. Here we describe a tiny oligopithecid from the youngest (∼29.5-30 Ma) primate-bearing horizon in the Jebel Qatrani Formation, based on a partial hemimandible with a largely complete first molar. This is the first record of an oligopithecid in the upper sequence of that Formation, occurring ∼160 m above the next-youngest oligopithecid-bearing locality (Quarry E), and provides a new last appearance datum for Oligopithecidae. The species is markedly smaller than its older oligopithecid relatives Catopithecus and Oligopithecus, and indeed is one of the smallest anthropoids known, suggesting that it represents a member of a dwarfed lineage. This material adds to the evidence provided by the co-occurring species Afrotarsius chatrathi and Qatrania fleaglei for a fairly diverse, but exceedingly rare, small primate fauna at a horizon that is otherwise dominated by much larger and more derived propliopithecids and parapithecids.

A calcaneus attributable to the primitive late Eocene anthropoid Proteopithecus sylviae: phenetic affinities and phylogenetic implications.

A well-preserved calcaneus referrable to Proteopithecus sylviae from the late Eocene Quarry L-41 in the Fayum Depression, Egypt, provides new evidence relevant to this taxon's uncertain phylogenetic position. We assess morphological affinities of the new specimen using three-dimensional geometric morphometric analyses with a comparative sample of primate calcanei representing major extinct and extant radiations (n = 58 genera, 106 specimens). Our analyses reveal that the calcaneal morphology of Proteopithecus is most similar to that of the younger Fayum parapithecid Apidium. Principal components analysis places Apidium and Proteopithecus in an intermediate position between primitive euprimates and crown anthropoids, based primarily on landmark configurations corresponding to moderate distal elongation, a more distal position of the peroneal tubercle, and a relatively "unflexed" calcaneal body. Proteopithecus and Apidium are similar to cercopithecoids and some omomyiforms in having an ectal facet that is more tightly curved, along with a larger degree of proximal calcaneal elongation, whereas other Fayum anthropoids, platyrrhines and adapiforms have a more open facet with less proximal elongation. The similarity to cercopithecoids is most plausibly interpreted as convergence given the less tightly curved ectal facets of stem catarrhines. The primary similarities between Proteopithecus and platyrrhines are mainly in the moderate distal elongation and the more distal position of the peroneal tubercle, both of which are not unique to these groups. Proteopithecus and Apidium exhibit derived anthropoid features, but also a suite of primitive retentions. The calcaneal morphology of Proteopithecus is consistent with our cladistic analysis, which places proteopithecids as a sister group of Parapithecoidea.

A fossil primate of uncertain affinities from the earliest late Eocene of Egypt.

Paleontological work carried out over the last 3 decades has established that three major primate groups were present in the Eocene of Africa-anthropoids, adapiforms, and advanced strepsirrhines. Here we describe isolated teeth of a previously undocumented primate from the earliest late Eocene ( approximately 37 Ma) of northern Egypt, Nosmips aenigmaticus, whose phylogenetic placement within Primates is unclear. Nosmips is smaller than the sympatric adapiform Afradapis but is considerably larger than other primate taxa known from the same paleocommunity. The species bears an odd mosaic of dental features, combining enlarged, elongate, and molariform premolars with simple upper molars that lack hypocones. Phylogenetic analysis across a series of different assumption sets variously places Nosmips as a stem anthropoid, a nonadapiform stem strepsirrhine, or even among adapiforms. This phylogenetic instability suggests to us that Nosmips likely represents a highly specialized member of a previously undocumented, and presumably quite ancient, endemic African primate lineage, the subordinal affinities of which have been obscured by its striking dental autapomorphies. Discriminant functions based on measurements of lower molar size and topography reliably classify extant prosimian primates into their correct dietary groups and identify Nosmips and Afradapis as omnivores and folivores, respectively. Although Nosmips currently defies classification, this strange and unexpected fossil primate nevertheless provides additional evidence for high primate diversity in northern Africa approximately 37 million years ago and further underscores the fact that our understanding of early primate evolution on that continent remains highly incomplete.

Evolution of locomotion in Anthropoidea: the semicircular canal evidence.

Our understanding of locomotor evolution in anthropoid primates has been limited to those taxa for which good postcranial fossil material and appropriate modern analogues are available. We report the results of an analysis of semicircular canal size variation in 16 fossil anthropoid species dating from the Late Eocene to the Late Miocene, and use these data to reconstruct evolutionary changes in locomotor adaptations in anthropoid primates over the last 35 Ma. Phylogenetically informed regression analyses of semicircular canal size reveal three important aspects of anthropoid locomotor evolution: (i) the earliest anthropoid primates engaged in relatively slow locomotor behaviours, suggesting that this was the basal anthropoid pattern; (ii) platyrrhines from the Miocene of South America were relatively agile compared with earlier anthropoids; and (iii) while the last common ancestor of cercopithecoids and hominoids likely was relatively slow like earlier stem catarrhines, the results suggest that the basal crown catarrhine may have been a relatively agile animal. The latter scenario would indicate that hominoids of the later Miocene secondarily derived their relatively slow locomotor repertoires.

New primate first metatarsals from the Paleogene of Egypt and the origin of the anthropoid big toe.

The specialized grasping feet of primates, and in particular the nature of the hallucal grasping capabilities of living strepsirrhines and tarsiers (i.e., 'prosimians'), have played central roles in the study of primate origins. Prior comparative studies of first metatarsal (Mt1) morphology have documented specialized characters in living prosimians that are indicative of a more abducted hallux, which in turn is often inferred to be related to an increased ability for powerful grasping. These include a well-developed peroneal process and a greater angle of the proximal articular surface relative to the long axis of the diaphysis. Although known Mt1s of fossil prosimians share these characters with living non-anthropoid primates, Mt1 morphology in the earliest crown group anthropoids is not well known. Here we describe two Mt1s from the Fayum Depression of Egypt - one from the latest Eocene (from the ∼34 Ma Quarry L-41), and one from the later early Oligocene (from the ∼29-30 Ma Quarry M) - and compare them with a sample of extant and fossil primate Mt1s. Multivariate analyses of Mt1 shape variables indicate that the Fayum specimens are most similar to those of crown group anthropoids, and likely belong to the stem catarrhines Catopithecus and Aegyptopithecus specifically, based on analyses of size. Also, phylogenetic analyses with 16 newly defined Mt1 characters support the hypotheses that "prosimian"-like Mt1 features evolved along the primate stem lineage, while crown anthropoid Mt1 morphology and function is derived among primates, and likely differed from that of basal stem anthropoids. The derived loss of powerful hallucal grasping as reflected in the Mt1 morphology of crown anthropoids may reflect long-term selection for improved navigation of large-diameter, more horizontal branches at the expense of movement in smaller, more variably inclined branches in the arboreal environment.

Fossil and molecular evidence constrain scenarios for the early evolutionary and biogeographic history of hystricognathous rodents.

The early evolutionary and paleobiogeographic history of the diverse rodent clade Hystricognathi, which contains Hystricidae (Old World porcupines), Caviomorpha (the endemic South American rodents), and African Phiomorpha (cane rats, dassie rats, and blesmols) is of great interest to students of mammalian evolution, but remains poorly understood because of a poor early fossil record. Here we describe the oldest well-dated hystricognathous rodents from an earliest late Eocene (approximately 37 Ma) fossil locality in the Fayum Depression of northern Egypt. These taxa exhibit a combination of primitive and derived features, the former shared with Asian "baluchimyine" rodents, and the latter shared with Oligocene phiomorphs and caviomorphs. Phylogenetic analysis incorporating morphological, temporal, geographic, and molecular information places the new taxa as successive sister groups of crown Hystricognathi, and supports an Asian origin for stem Hystricognathi and an Afro-Arabian origin for crown Hystricognathi, stem Hystricidae, and stem Caviomorpha. Molecular dating of early divergences within Hystricognathi, using a Bayesian "relaxed clock" approach and multiple fossil calibrations, suggests that the split between Hystricidae and the phiomorph-caviomorph clade occurred approximately 39 Ma, and that phiomorphs and caviomorphs diverged approximately 36 Ma. These results are remarkably congruent with our phylogenetic results and the fossil record of hystricognathous rodent evolution in Afro-Arabia and South America.

Stable isotope evidence for an amphibious phase in early proboscidean evolution.

The order Proboscidea includes extant elephants and their extinct relatives and is closely related to the aquatic sirenians (manatees and dugongs) and terrestrial hyracoids (hyraxes). Some analyses of embryological, morphological, and paleontological data suggest that proboscideans and sirenians shared an aquatic or semiaquatic common ancestor, but independent tests of this hypothesis have proven elusive. Here we test the hypothesis of an aquatic ancestry for advanced proboscideans by measuring delta(18)O in tooth enamel of two late Eocene proboscidean genera, Barytherium and Moeritherium, which are sister taxa of Oligocene-to-Recent proboscideans. The combination of low delta(18)O values and low delta(18)O standard deviations in Barytherium and Moeritherium matches the isotopic pattern seen in aquatic and semiaquatic mammals, and differs from that of terrestrial mammals. delta(13)C values of these early proboscideans suggest that both genera are likely to have consumed freshwater plants, although a component of C(3) terrestrial vegetation cannot be ruled out. The simplest explanation for the combined evidence from isotopes, dental functional morphology, and depositional environments is that Barytherium and Moeritherium were at least semiaquatic and lived in freshwater swamp or riverine environments, where they grazed on freshwater vegetation. These results lend new support to the hypothesis that Oligocene-to-Recent proboscideans are derived from amphibious ancestors.

Astragalar morphology of Afradapis, a large adapiform primate from the earliest late Eocene of Egypt.

The ∼37 million-year-old Birket Qarun Locality 2 (BQ-2), in the Birket Qarun Formation of Egypt's Fayum Depression, yields evidence for a diverse primate fauna, including the earliest known lorisiforms, parapithecoid anthropoids, and Afradapis longicristatus, a large folivorous adapiform. Phylogenetic analysis has placed Afradapis as a stem strepsirrhine within a clade of caenopithecine adapiforms, contradicting the recently popularized alternative hypothesis aligning adapiforms with haplorhines or anthropoids. We describe an astragalus from BQ-2 (DPC 21445C), attributable to Afradapis on the basis of size and relative abundance. The astragalus is remarkably similar to those of extant lorises, having a low body, no posterior shelf, a broad head and neck. It is like extant strepsirrhines more generally, in having a fibular facet that slopes gently away from the lateral tibial facet, and in having a groove for the tendon of flexor fibularis that is lateral to the tibial facet. Comparisons to a sample of euarchontan astragali show the new fossil to be most similar to those of adapines and lorisids. The astragali of other adapiforms are most similar to those of lemurs, but distinctly different from those of all anthropoids. Our measurements show that in extant strepsirrhines and adapiforms the fibular facet slopes away from the lateral tibial facet at a gradual angle (112-126°), in contrast to the anthropoid fibular facet, which forms a sharper angle (87-101°). Phylogenetic analyses incorporating new information from the astragalus continue to support strepsirrhine affinities for adapiforms under varying models of character evolution.

High-resolution computed tomography study of the cranium of a fossil anthropoid primate, Parapithecus grangeri: new insights into the evolutionary history of primate sensory systems.

Extant anthropoids have large brains, small olfactory bulbs, and high-acuity vision compared with other primates. The relative timing of the evolution of these characteristics may have important implications for brain evolution. Here computed tomography is used to examine the cranium of a fossil anthropoid, Parapithecus grangeri. It is found that P. grangeri had a relatively small brain compared with living primates. In addition, it had an olfactory bulb in the middle of the range for living primates. Methods for relating optic foramen area and other cranial measurements to acuity are discussed. Multiple regression is used to estimate retinal ganglion cell number in P. grangeri. Given currently available comparative data, P. grangeri seems to have had retinal ganglion cell counts intermediate for living primates, overlapping with the upper end of the range for strepsirrhines and possibly with the lower end for anthropoids.

Isolation of females prior to parturition reduces neonatal mortality in Galago.

Eighteen years of birth records for three species of Galago at the Duke University Primate Center were examined to determine the effects of isolation of pregnant females on neonatal mortality rates. Isolation significantly decreased neonatal mortality rates in all three species over neonatal mortality rates in infants born to unisolated females. The frequency of cannibalism of infants did not differ between isolated and unisolated females. Secondary sex ratio differed significantly from 1:1 for all three species, but higher mortality in males in the first 10 days of life resulted in sex ratios that did not differ from 1:1 in G. garnettii and G. crassicaudatus.

Tactics of care for young infants by forest-living ruffed lemurs (Varecia variegata variegata): Ground nests, parking, and biparental guarding.

Over a 4 month period, systematic and ad libitum observations were conducted on two adult female black-and-white ruffed lemurs (Varecia variegata variegata) and their infants in a 3.5 ha forest enclosure. The females were mother and daughter, members of a family group that had been semifree-ranging for 2 years and 3 months at the time of the births. One to two weeks before parturition, the females independently constructed nests, in which they kept their infants during the first few weeks following parturition. The older mother, cage-reared herself, prepared at least one nest. Her daughter, who has lived in the forest since late juvenescence, prepared at least four. Two to three weeks after parturition, the mothers moved their infants high into trees. During periods of maternal absence, the infants were often alone, and they rarely or never moved, vocalized, or groomed themselves. The mothers often kept their infants together after nests were no longer used. Each infant nursed freely from both lactating females. The infants were carried orally only by their mothers and were never transported by clinging to the pelage of any group members. Previously, researchers suggested that ruffed lemurs build nests for care of infants high up in trees. The present observations, however, suggest that two major modes of neonate care in Varecia exist: serial use of multiple ground nests and "parking" of infants high in trees. Advance preparation of several nest sites, relative lack of large predators, alternate maternal and paternal guarding of infants, infant immobility during absence of mother, and rapid infant development make this tactic of care for neonates plausible.

Gestation length in Tarsius bancanus.

A gestation length of 178 days was determined for Tarsius bancanus based on a vaginal smear containing whole sperm. This value replaces the only previously reported information on gestation length in tarsiers, a rough estimate of approximately 6 months for T. syrichta.

Description of ultrasonic vocalizations of the mouse lemur (Microcebus murinus) and the fat-tailed dwarf lemur (Cheirogaleus medius).

Ultrasonic (>20 kHz) vocalizations were recorded from two species of prosimian primates, Microcebus murinus and Cheirogaleus medius. Three types of ultrasonic calls were emitted by isolated or paired M. murinus: 1) "chirps," short-duration (30 msec) calls with a sharp onset at 40 kHz followed by rapid and steep declines in frequency and intensity; 2) "twitters," characterized by a brief pulse at 25 kHz prior to the onset of repeating, frequency-modulated units; and 3) "long whistles," monotone signals with a frequency of 20 kHz. Partially ultrasonic "whines" were recorded from C. medius during interactions between mothers and infants. These calls began with a short, high-intensity component at 25 kHz and then dropped gradually in frequency before leveling off at 15 kHz. Study of the acoustic behavior and the structure of vocalizations in these species may lead to a better understanding of animal communication at high frequencies.

Reproductive cycles in Tarsius bancanus.

The reproductive condition of three pairs of Bornean tarsiers (Tarsius bancanus) was documented for 16 months. Each pair was housed separately under a constant photoperiod (L:D = 11.5:12.5) similar to that in their native habitat. Reproductive cycles of females were monitored visually for 6 months and were then monitored with vaginal smears and measurements of external genitalia for an additional 10 months. Progressive proliferation and cornification of vaginal epithelial cells during proestrus and estrus was accompanied by an enlargement of the external genitalia. Cycle lengths averaged 24.0 ± 3.2 days. The external genitalia were swollen each cycle for a period of 6-9 days. Copulations occurred on the 1st day of estrus, which lasted 1-3 days. No menstruation was observed. There was no evidence of seasonality of estrous cycles with this photoperiod. Testicular measurements of males showed no overt seasonal changes. There was variation in testicular size, and one male copulated at a range of testicular sizes. The data indicate that T. bancanus has estrous cycles similar to those of prosimian primates and some New World monkeys and that these cycles occur throughout the year under constant photoperiodic conditions.

Craniodental morphology and systematics of a new family of hystricognathous rodents (Gaudeamuridae) from the late eocene and early oligocene of Egypt.

BACKGROUND: Gaudeamus is an enigmatic hystricognathous rodent that was, until recently, known solely from fragmentary material from early Oligocene sites in Egypt, Oman, and Libya. Gaudeamus' molars are similar to those of the extant cane rat Thryonomys, and multiple authorities have aligned Gaudeamus with Thryonomys to the exclusion of other living and extinct African hystricognaths; recent phylogenetic analyses have, however, also suggested affinities with South American caviomorphs or Old World porcupines (Hystricidae). METHODOLOGY/PRINCIPAL FINDINGS: Here we describe the oldest known remains of Gaudeamus, including largely complete but crushed crania and complete upper and lower dentitions. Unlike younger Gaudeamus species, the primitive species described here have relatively complex occlusal patterns, and retain a number of plesiomorphic features. Unconstrained parsimony analysis nests Gaudeamus and Hystrix within the South American caviomorph radiation, implying what we consider to be an implausible back-dispersal across the Atlantic Ocean to account for Gaudeamus' presence in the late Eocene of Africa. An analysis that was constrained to recover the biogeographically more plausible hypothesis of caviomorph monophyly does not place Gaudeamus as a stem caviomorph, but rather as a sister taxon of hystricids. CONCLUSIONS/SIGNIFICANCE: We place Gaudeamus species in a new family, Gaudeamuridae, and consider it likely that the group originated, diversified, and then went extinct over a geologically brief period of time during the latest Eocene and early Oligocene in Afro-Arabia. Gaudeamurids are the only known crown hystricognaths from Afro-Arabia that are likely to be aligned with non-phiomorph members of that clade, and as such provide additional support for an Afro-Arabian origin of advanced stem and basal crown members of Hystricognathi.

Ecogeographic size variation in small-bodied subfossil primates from Ankilitelo, southwestern Madagascar.

Variation in body size is well documented for both extant and extinct Malagasy primates, and appears to be correlated with geographic patterns of resource seasonality. Less attention has been paid to extant lemurs in subfossil collections, although it has been suggested that subfossil forms of extant species are characterized by greater size than their modern counterpart. This trend of phyletic size change has been related to climate change, habitat fragmentation, or human hunting. However, space- and time-averaging in the subfossil samples of previous studies may have obscured more general ecogeographic patterns underlying these size differences. Our objective is to examine size variation in subfossil still-extant primates within a regional comparative context to determine if subfossil and living forms conform to similar ecogeographic patterns. We report on the subfossil still-extant primate assemblage from Ankilitelo, southwestern Madagascar (approximately 500 yr BP) to test this hypothesis. The Ankilitelo primates were compared with museum specimens of known locality. Extant taxa were assigned to one of five distinct ecogeographic regions, including spiny thicket, dry deciduous forest, succulent woodland, lowland and subhumid rainforest. Comparisons of tooth size in extant lemurs reveal significant geographical patterns of variation within genera. In general, the primates from Ankilitelo are indeed larger than their modern counterpart. However, these differences fit an ecoregional model of size variation, whereby Ankilitelo species are comparable in size to living forms inhabiting ecoregions present near the cave today. This suggests that Malagasy primates have been subjected to similar patterns of resource seasonality for at least 500 years.

A remarkable female cranium of the early Oligocene anthropoid Aegyptopithecus zeuxis (Catarrhini, Propliopithecidae).

The most complete and best-preserved cranium of a Paleogene anthropoid ever found, that of a small female of the early Oligocene ( approximately 29-30 Ma) stem catarrhine species Aegyptopithecus zeuxis, was recovered from the Jebel Qatrani Formation (Fayum Depression, Egypt) in 2004. The specimen is that of a subadult and, in craniodental dimensions, is the smallest Aegyptopithecus individual known. High-resolution computed tomographic (microCT) scanning of the specimen's well preserved cranial vault confirms that Aegyptopithecus had relatively unexpanded frontal lobes and a brain-to-body mass ratio lower than those of living anthropoids. MicroCT scans of a male cranium recovered in 1966 [Egyptian Geological Museum, Cairo (CGM) 40237] reveal that previous estimates of its endocranial volume were too large. Thus, some amount of encephalization evolved independently in platyrrhine and catarrhine anthropoids, and the relative brain size of the last common ancestor of crown Anthropoidea was probably strepsirrhine-like or smaller. A. zeuxis shows extreme sexual dimorphism in craniodental morphology (apparently to a degree otherwise seen only in some highly dimorphic Miocene catarrhines), and the crania of female Aegyptopithecus lack a number of morphological features seen in larger males that have been accorded phylogenetic significance in catarrhine systematics (e.g., a well developed rostrum, elongate sagittal crest, and frontal trigon). Although a unique pattern of craniofacial sexual dimorphism may have characterized advanced stem and basal crown catarrhines, expression of various allegedly "discrete" craniofacial features may have been intraspecifically variable in early catarrhine species due to high levels of dimorphism and so should be treated with caution in phylogenetic analyses.

Additional remains of Wadilemur elegans, a primitive stem galagid from the late Eocene of Egypt.

The late Eocene prosimian Wadilemur elegans from the Jebel Qatrani Formation, northern Egypt, was originally interpreted as an anchomomyin adapiform primate based on limited information from the lower molars and distal premolars. Recently recovered fossils attributable to this species, including a proximal femur, the fourth upper premolar and first and second upper molars, and a mandible preserving the lower second premolar and lower canine and incisor alveoli, reveal a number of derived morphological similarities shared with crown strepsirrhines and, in particular, Miocene-to-Recent stem and crown galagids, to the exclusion of known adapiforms. Phylogenetic analysis of 359 morphological features scored across 95 living and extinct crown primate taxa supports a stem galagid placement for Wadilemur and older Saharagalago, and a close relationship between crown strepsirrhines and the Eocene African taxa "Anchomomys" milleri, Djebelemur, and Plesiopithecus (none of which appear to be closely related to European anchomomyins). This scheme of relationships supports the hypothesis that crown Strepsirrhini is of Afro-Arabian origin and that lemuriforms likely colonized Madagascar by crossing the Mozambique Channel. Wadilemur's known dental and postcranial morphology provides additional support for the hypothesis that galagids and lorisids had diverged by the close of the middle Eocene, and, by bolstering the approximately 37 million-year-old calibration point for crown lorisiform origins provided by Saharagalago, indirect support for the hypothesis of an ancient origin of crown Strepsirrhini and crown Primates.