Oldest evidence of abundant C4 grasses and habitat heterogeneity in eastern Africa.

The assembly of Africa's iconic C4 grassland ecosystems is central to evolutionary interpretations of many mammal lineages, including hominins. C4 grasses are thought to have become ecologically dominant in Africa only after 10 million years ago (Ma). However, paleobotanical records older than 10 Ma are sparse, limiting assessment of the timing and nature of C4 biomass expansion. This study uses a multiproxy design to document vegetation structure from nine Early Miocene mammal site complexes across eastern Africa. Results demonstrate that between ~21 and 16 Ma, C4 grasses were locally abundant, contributing to heterogeneous habitats ranging from forests to wooded grasslands. These data push back the oldest evidence of C4 grass-dominated habitats in Africa-and globally-by more than 10 million years, calling for revised paleoecological interpretations of mammalian evolution.

The evolution of hominoid locomotor versatility: Evidence from Moroto, a 21 Ma site in Uganda.

Living hominoids are distinguished by upright torsos and versatile locomotion. It is hypothesized that these features evolved for feeding on fruit from terminal branches in forests. To investigate the evolutionary context of hominoid adaptive origins, we analyzed multiple paleoenvironmental proxies in conjunction with hominoid fossils from the Moroto II site in Uganda. The data indicate seasonally dry woodlands with the earliest evidence of abundant C4 grasses in Africa based on a confirmed age of 21 million years ago (Ma). We demonstrate that the leaf-eating hominoid Morotopithecus consumed water-stressed vegetation, and postcrania from the site indicate ape-like locomotor adaptations. These findings suggest that the origin of hominoid locomotor versatility is associated with foraging on leaves in heterogeneous, open woodlands rather than forests.

Additional hominoid fossils from the early Miocene of the Lothidok Formation, Kenya.

OBJECTIVES: Hominoid fossils are abundant at early Miocene fossil sites in the Lothidok Range, located directly west of Lake Turkana in northern Kenya. The West Turkana Miocene Project (WTMP) has worked in the Lothidok Range since 2008 with the goal of further elucidating the paleobiology of the hominoids through the recovery of new specimens and detailed documentation of their paleoecological context. To date our research has focused largely on the Kalodirr and Moruorot Site Complexes, both radiometrically dated to ~17.5-16.8 Ma. MATERIALS AND METHODS: Our ongoing fieldwork at the Kalodirr Site Complex resulted in the discovery of new dentognathic specimens of the three previously identified species of fossil hominoids-Turkanapithecus kalakolensis, Simiolus enjiessi, and Afropithecus turkanensis. RESULTS: A new mandible and an isolated M3 of T. kalakolensis from Kalodirr further clarify the lower molar morphology of the species and permit identification of KNM-MO 1 as a mandible of T. kalakolensis. A new mandible of S. enjiessi provides evidence of the relative proportions of the first and second lower molars. A new male specimen of A. turkanensis shows unusual P4 morphology that may be a developmental anomaly or a previously unknown morphological variant. DISCUSSION: An improved understanding of the lower molar morphology of T. kalakolensis further strengthens its identification as a nyanzapithecine. Our new specimens and subsequent re-identification of existing collections makes it clear that all three Lothidok hominoids are known from both the Moruorot and Kalodirr Site Complexes. The Lothidok Range holds great promise for further documenting hominoid evolution.

Skeleton of a Cretaceous mammal from Madagascar reflects long-term insularity.

The fossil record of mammaliaforms (mammals and their closest relatives) of the Mesozoic era from the southern supercontinent Gondwana is far less extensive than that from its northern counterpart, Laurasia1,2. Among Mesozoic mammaliaforms, Gondwanatheria is one of the most poorly known clades, previously represented by only a single cranium and isolated jaws and teeth1-5. As a result, the anatomy, palaeobiology and phylogenetic relationships of gondwanatherians remain unclear. Here we report the discovery of an articulated and very well-preserved skeleton of a gondwanatherian of the latest age (72.1-66 million years ago) of the Cretaceous period from Madagascar that we assign to a new genus and species, Adalatherium hui. To our knowledge, the specimen is the most complete skeleton of a Gondwanan Mesozoic mammaliaform that has been found, and includes the only postcranial material and ascending ramus of the dentary known for any gondwanatherian. A phylogenetic analysis including the new taxon recovers Gondwanatheria as the sister group to Multituberculata. The skeleton, which represents one of the largest of the Gondwanan Mesozoic mammaliaforms, is particularly notable for exhibiting many unique features in combination with features that are convergent on those of therian mammals. This uniqueness is consistent with a lineage history for A. hui of isolation on Madagascar for more than 20 million years.

Primitive Old World monkey from the earliest Miocene of Kenya and the evolution of cercopithecoid bilophodonty.

Old World monkeys (Cercopithecoidea) are a highly successful primate radiation, with more than 130 living species and the broadest geographic range of any extant group except humans. Although cercopithecoids are highly variable in habitat use, social behavior, and diet, a signature dental feature unites all of its extant members: bilophodonty (bi: two, loph: crest, dont: tooth), or the presence of two cross-lophs on the molars. This feature offers an adaptable Bauplan that, with small changes to its individual components, permits its members to process vastly different kinds of food. Old World monkeys diverged from apes perhaps 30 million years ago (Ma) according to molecular estimates, and the molar lophs are sometimes incompletely developed in fossil species, suggesting a mosaic origin for this key adaptation. However, critical aspects of the group's earliest evolution remain unknown because the cercopithecoid fossil record before ∼18 Ma consists of only two isolated teeth, one from Uganda and one from Tanzania. Here we describe a primitive Old World monkey from Nakwai, Kenya, dated at ∼22 Ma, that offers direct evidence for the initial key steps in the evolution of the cercopithecoid dentition. The simple dentition and absence of bilophodonty in the Nakwai monkey indicate that the initial radiation of Old World monkeys was first characterized by a reorganization of basic molar morphology, and a reliance on cusps rather than lophs suggests frugivorous diets and perhaps hard object feeding. Bilophodonty evolved later, likely in response to the inclusion of leaves in the diet.

A new species of Simiolus from the middle Miocene of the Tugen Hills, Kenya.

A new species of the "small-bodied ape" Simiolus is described here that extends the temporal range of the genus to the end of the Middle Miocene. As such, it is one of the few species of fossil primates known from East Africa during a time of significant change in which Old World monkeys and crown hominoids replaced the primitive ape-like primates that had dominated the early Miocene. The dynamics of this important event in our evolutionary history are obscured by the small number of fossil primates known from Africa between 14 and 6 million years ago, as well as persistent ambiguity regarding the phylogenetic status of the ape-like Miocene primates. The new species described here helps to fill this temporal gap, and our analysis of its phylogenetic position suggests that Simiolus and many other Miocene primates were not only ape-like, they were, indeed, stem hominoids. Judging from the available material, the new species may be the smallest known ape.

Nasolacrimal anatomy and haplorhine origins.

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

Ontogeny and Microanatomy of the Nasal Turbinals in Lemuriformes.

The nasal cavity of strepsirrhine primates (lemurs and lorises) has the most primitive arrangement of extant primates. In nocturnal species, the numerous turbinals of the ethmoid bear a large surface area of olfactory mucosa (OM). In this study, we examine turbinal development in four genera of diurnal or cathemeral lemuriformes. In addition, we examined an age series of each genus to detect whether structures bearing OM as opposed to respiratory mucosa (RM) develop differently, as has been observed in nocturnal strepsirrhines. In adults, the maxilloturbinal is covered by highly vascular respiratory mucosa throughout its entire length, with large sinusoidal vessels in the lamina propria; any parts of other turbinals that closely borders the maxilloturbinal has a similar mucosa. Posteriorly, the most vascular RM is restricted in the nasopharyngeal duct, which becomes partitioned from the dorsal olfactory region. A comparison of newborns to adults reveals that the first ethmoturbinal increases more in length in the parts that are covered with RM than OM, which supports the idea that ethmoturbinals can specialize in more than one function. Finally, we observe that the regions of turbinals that are ultimately covered with RM develop more accessory lamellae or additional surface area of existing scrolls compared to the regions covered with OM. Because such outgrowths of bone develop postnatally and without cartilaginous precursors, we hypothesize that the complexity of olfactory lamellae within the ethmoturbinal complex is primarily established at birth, while respiratory lamellae become elaborated due to the epigenetic influence of respiratory physiology. Anat Rec, 299:1492-1510, 2016. © 2016 Wiley Periodicals, Inc.

First cranial remains of a gondwanatherian mammal reveal remarkable mosaicism.

Previously known only from isolated teeth and lower jaw fragments recovered from the Cretaceous and Palaeogene of the Southern Hemisphere, the Gondwanatheria constitute the most poorly known of all major mammaliaform radiations. Here we report the discovery of the first skull material of a gondwanatherian, a complete and well-preserved cranium from Upper Cretaceous strata in Madagascar that we assign to a new genus and species. Phylogenetic analysis strongly supports its placement within Gondwanatheria, which are recognized as monophyletic and closely related to multituberculates, an evolutionarily successful clade of Mesozoic mammals known almost exclusively from the Northern Hemisphere. The new taxon is the largest known mammaliaform from the Mesozoic of Gondwana. Its craniofacial anatomy reveals that it was herbivorous, large-eyed and agile, with well-developed high-frequency hearing and a keen sense of smell. The cranium exhibits a mosaic of primitive and derived features, the disparity of which is extreme and probably reflective of a long evolutionary history in geographic isolation.

A Rangwapithecus gordoni mandible from the early Miocene site of Songhor, Kenya.

A mandible of Rangwapithecus gordoni from the early Miocene site of Songhor, Kenya, provides additional information about this relatively poorly known taxon. The R. gordoni sample is small, being composed of dental and a few gnathic parts. The fossil described here provides examples of previously unknown dental and mandibular anatomy, and confirms former reassignments of isolated anterior teeth based on less certain evidence. The phylogenetic status of Rangwapithecus, its distribution, and paleobiology are briefly reviewed. Rangwapithecus shows a suite of dental and gnathic features that warrants its generic distinction from Proconsul. Derived features shared with Nyanzapithecus and Turkanapithecus indicate that it is an early member of the subfamily Nyanzapithecinae. Its molar morphology suggests a considerable component of folivory in its diet. A review of the hypodigm shows Rangwapithecus to be restricted to Songhor. This distribution parallels that of Limnopithecus evansi, and is mirrored by Limnopithecus legetet and Micropithecus clarki suggesting that Songhor may have differed ecologically from other more or less contemporary sites in the region.

Dentognathic remains of an Afropithecus individual from Kalodirr, Kenya.

We describe here the well-preserved dentognathic remains of an Afropithecus individual from the early Miocene site of Kalodirr in northern Kenya. The specimen includes a nearly complete dentition in which most of the crowns are undamaged and unworn. The new information gleaned from this specimen adds to our knowledge of this genus in several ways. Afropithecus exhibits an atypical pattern of canine dimorphism, and is probably more easily sexed by the pattern of variation in its upper premolars. Both phenomena are likely related to the modification of its antemolar dentition for the purpose of sclerocarp harvesting. The new fossils clarify the role in this adaptation of the premolars, which appear specialized for initiating and propagating cracks in large food items bearing protective coats. Comparison with other Miocene apes suggests that the closest known relative of Afropithecus is Nacholapithecus, to which Equatorius is more distantly related. Morotopithecus shares some primitive traits with Afropithecus, but lacks the derived features shared by the latter and Nacholapithecus.

Early cercopithecid monkeys from the Tugen Hills, Kenya.

The modern Old World Monkeys (Superfamily Cercopithecoidea, Family Cercopithecidae) can be traced back into the late Miocene, but their origin and subsequent diversification is obscured by the scarcity of terrestrial fossil sites in Africa between 15 and 6 Ma. Here, we document the presence of cercopithecids at 12.5 Ma in the Tugen Hills of Kenya. These fossils add 3 My to the known antiquity of crown Cercopithecidae. The two specimens represent one or possibly two species of early colobine, and their morphology suggests that they were less folivorous than their modern relatives.

Microanatomical variation of the nasal capsular cartilage in newborn primates.

The breakdown of nasal capsule cartilage precedes secondary pneumatic expansion of the paranasal sinuses. Recent work indicates the nasal capsule of monkeys undergoes different ontogenetic transformations regionally (i.e., ossification, persistence as cartilage, or resorption). This study assesses nasal capsule morphology at the perinatal age in a taxonomically broad sample of non-human primates. Using traditional histochemical methods, osteopontin immunohistochemistry and tartrate-resistant acid phosphatase procedure, the cartilage of the lateral nasal wall (LNC) was studied. At birth, matrix properties differ between portions of the LNC that ultimately form elements of the ethmoid bone and regions of the LNC that have no postnatal (descendant) structure. The extent of cartilage that remains in the paranasal parts of the LNC varies among species. It is fragmented in species with the greatest extent of maxillary and/or frontal pneumatic expansion. Conversely, greater continuity of the LNC is noted in newborns of species that lack maxillary and/or frontal sinuses as adults. Chondroclasts occur adjacent to elements of the ethmoid bone, along the margin of the nasal tectum, and/or along islands of cartilage that bear no signs of ossification. Chondroclasts are prevalent along remnants of the paranasal LNC in tamarin species (Leontopithecus, Saguinus), which have extensive frontal and maxillary bone pneumatization. Taken together, the morphological observations indicate that the localized loss of cartilage might be considered a critical event at the onset of secondary pneumatization, facilitated by rapid recruitment of chondro-/osteoclasts, possibly occurring simultaneously in cartilage and bone.

Are we looking for loads in all the right places? New research directions for studying the masticatory apparatus of New World monkeys.

New World monkeys display a wide range of masticatory apparatus morphologies related to their diverse diets and feeding strategies. While primatologists have completed many studies of the platyrrhine masticatory apparatus, particularly morphometric analyses, we collectively acknowledge key shortcomings in our understanding of the function and evolution of the platyrrhine feeding apparatus. Our goal in this contribution is to review several recent, and in most cases ongoing, efforts to address some of the deficits in our knowledge of how the platyrrhine skull is loaded during feeding. We specifically consider three broad research areas: (1) in vivo physiological studies documenting mandibular bone strains during feeding, (2) metric analyses assessing musculoskeletal functional morphology and performance, as well as (3) the initiation of a physiological ecology of feeding that measures in vivo masticatory mechanics in a natural environment. We draw several conclusions from these brief reviews. First, we need better documentation of in vivo strain patterns in the platyrrhine skull during feeding given their empirical role in developing adaptive hypotheses explaining masticatory apparatus form. Second, the greater accuracy of new technologies, such as CT scanning, will allow us to better describe the functional consequences of jaw form. Third, performance studies are generally lacking for platyrrhine jaws, muscles, and teeth and offer exciting avenues for linking form to feeding behavior and diet. Finally, attempts to bridge distinct research agendas, such as collecting in vivo physiological data during feeding in natural environments, present some of the greatest opportunities for novel insights into platyrrhine feeding biology.

Distribution of olfactory and nonolfactory surface area in the nasal fossa of Microcebus murinus: implications for microcomputed tomography and airflow studies.

The nasal fossa of most mammals exemplifies extreme skeletal complexity. Thin scrolls of bone (turbinals) that both elaborate surface area (SA) and subdivide nasal space are used as morphological proxies for olfactory and respiratory physiology. The present study offers additional details on the nasal fossa of the adult mouse lemur (Microcebus murinus), previously described by Smith and Rossie (Smith and Rossie [2008]; Anatomical Record 291:895-915). Additional, intervening histological sections of the specimen were used to map and quantify the distribution of olfactory and nonolfactory mucosa on the smaller turbinal of the frontal recess (FR; frontoturbinal) and those that occur between ethmoturbinals (ETs; interturbinals). A second adult Microcebus specimen, available as a dried skull, was scanned using microcomputed tomography (microCT) and reconstructed to infer the position of these turbinals within the nasal airway. Overall, turbinal bones comprise more than half of internal nasal SA. All ETs combined comprise about 30% of total nasal fossa SA, and contribute nearly half of all olfactory SA. Of these, the nasoturbinal (NT) is most completely covered with olfactory mucosa, whereas ET I is least covered with olfactory mucosa. The FR contributes significantly to total olfactory SA (ca. 20%). This recess and the single frontoturbinal within it lie in a more lateral pathway of airflow compared with interturbinals, which lie in more central zone just anterior to the olfactory recess of Microcebus. Variations in the turbinals and recesses that complicate central and paranasal in primates should be investigated further in light of zone-specific distributions of olfactory receptors (ORs) that differ between these regions in rodents.

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.

The maxillary sinus in three genera of new world monkeys: factors that constrain secondary pneumatization.

The air filled cavities of paranasal sinuses are thought by some to appear opportunistically in spatial "gaps" within the craniofacial complex. Anthropoid primates provide excellent natural experiments for testing this model, since not all species possess a full complement of paranasal sinuses. In this study, two genera of monkeys (Saguinus and Cebuella) which form maxillary sinuses (MS) as adults were compared to squirrel monkeys (Saimiri spp.), in which a MS does not form. Using microCT and histomorphometric methods, the spatial position of paranasal spaces was assessed and size of the adjacent dental sacs was measured. In Saguinus, secondary pneumatization is underway perinatally, and the sinus extends alongside deciduous premolars (dp). The MS overlaps all permanent molars in the adult. In Saimiri, the homologous space (maxillary recess) extends no farther posterior than the first deciduous premolar at birth and extends no farther than the last premolar in the adult. Differences in dental size and position may account for this finding. For example, Saimiri has significantly larger relative dp volumes, and enlarged orbits, which encroach on the internasal space to a greater degree when compared to Saguinus. These factors limit space for posterior expansion of the maxillary recess. These findings support the hypothesis that secondary pneumatization is a novel, opportunistic growth mechanism that removes "unneeded" bone. Moreover, paranasal spaces occur in association with semiautonomous skeletal elements that border more than one functional matrix, and the spatial dynamics of these units can act as a constraint on pneumatic expansion of paranasal spaces.

Terrestrial adaptations in the hands of Equatorius africanus revisited.

Interpretations of the postcranial anatomy of East African early and middle Miocene large-bodied hominoids (e.g., Proconsul, Afropithecus, Turkanapithecus, Nacholapithecus) have suggested that these diverse primates utilized positional behaviors dominated by arboreal quadrupedalism. Preliminary descriptions of the Equatorius africanus partial skeleton (KNM-TH 28860) and other forelimb specimens, however, have argued that this animal relied more on terrestrial locomotion compared to its contemporaries, possibly similar to extant large papionin monkeys. In this paper, we reevaluate this interpretation by examining intrinsic hand proportions based on the lengths of the third proximal phalanx and fifth metacarpal in Equatorius in reference to a large sample of extant catarrhine primate taxa. We focused on the lengths of these hand bones because the ratio between phalanx and metacarpal lengths has been previously documented to discriminate terrestrial from arboreal mammalian taxa, including primates. The Equatorius hand displays semi-terrestrial hand proportions with a relatively shorter proximal phalanx compared to most arboreal monkeys. Its proximal phalanx, however, is relatively longer than those of habitually terrestrial monkeys (e.g., Theropithecus, Papio). Accordingly, although Equatorius retains some arboreal quadrupedal characteristics, these results corroborate the previous inference that it engaged in more terrestrial locomotion than earlier Miocene apes such as Proconsul. We suggest that the postcranial skeleton of Equatorius evinces the earliest signs of semi-terrestriality in the hominoid fossil record. It is likely that the terrestrial specialization utilized by living hominoids, e.g., knuckle-walking, evolved separately.

Fate of the nasal capsular cartilages in prenatal and perinatal tamarins (Saguinus geoffroyi) and extent of secondary pneumatization of maxillary and frontal sinuses.

Development of the nasal capsule cartilages was studied in seven Geoffroy's tamarins (Saguinus geoffroyi), including one fetus, five neonates and one infant. Four additional postnatal specimens of the genus were studied (one 5-month-old and three adults) to determine the magnitude of postnatal expansion of the paranasal sinuses. Alcian blue histochemistry and osteopontin immunohistochemistry were employed in selected subadult specimens to characterize cartilage matrix. The fetal S. geoffroyi possesses a continuous nasal capsule, including a zona anularis; the primordial maxillary sinuses are surrounded by cartilage. Secondary pneumatization is in progress in all older specimens, which have sinuses that are more than twofold larger compared to that of the fetus. Results indicate that extensive ossification of the middle part of the nasal capsule (pars intermedia) is occurring in the perinatal timeframe, forming portions of the ethmoid bone. Anteriorly, the nasal capsule comprises isolated fragments in perinatal specimens, which are fewer and smaller in the infant and in a 5-month-old S. midas, and nearby multinucleate cells suggest that osteoclasts break apart these initially continuous elements. Fragments of the pars intermedia and the tectum nasi are found transiently between mucosa and the sites of secondary pneumatization. The maxillary sinus mucosa is highly vascular in most perinatal specimens. Histochemical and immunohistochemical findings show that cartilage of endochondral bones and non-ossifying parts are distinct in the perinatal time period. These results indicate that breakdown of the capsular cartilage precedes secondary pneumatization as previously suggested. There are portions of the cartilage of the recessus maxillaris and tectum nasi that transiently block mucosa from interfacing directly with bone. Vascularization may play a role in the breakdown of cartilages as well as the onset of secondary pneumatization. Since cartilage has the capacity to produce substances that trigger angiogenesis and bone resorption, further detailed characterization of the cartilage bordering sites of secondary pneumatization is merited.