Unexpected evolutionary patterns of dental ontogenetic traits in cetartiodactyl mammals.

Studying ontogeny in both extant and extinct species can unravel the mechanisms underlying mammal diversification and specialization. Among mammalian clades, Cetartiodactyla encompass species with a wide range of adaptations, and ontogenetic evidence could clarify longstanding debates on the origins of modern specialized families. Here, we study the evolution of dental eruption patterns in early diverging cetartiodactyls to assess the ecological and biological significance of this character and shed new light on phylogenetic issues. After investigation of the ontogenetic dental series of 63 extinct genera, our parsimony reconstructions of eruption state evolution suggest that the eruption of molars before permanent premolars represents a plesiomorphic condition within Cetartiodactyla. This result substantially differs from a previous study based on modern species only. As a result, the presence of this pattern in most ruminants might represent an ancestral condition contributing to their specialized herbivory, rather than an original adaptation. In contrast, the late eruption of molars in hippopotamoids is more likely related to biological aspects, such as increases in body mass and slower pace of life. Our study mainly shows that eruption sequences reliably characterize higher level cetartiodactyl taxa and could represent a new source of phylogenetic characters, especially to disentangle the origin of hippopotamoids and cetaceans.

Relationships Between Enamel Prism Decussation and Organization of the Ameloblast Layer in Rodent Incisors.

Rodent enamel microstructure has been extensively investigated, primarily on the basis of 2D electronic microscopy data. The nature and dynamics of the ameloblasts (the enamel-secreting cells) have also been well studied. However, critical issues still remain surrounding exactly how the ameloblasts produce the astonishing microstructural complexity of enamel, and how this subtle architecture evolved through time. In this article, we used a new methodology based on confocal laser microscopy to reconstruct the enamel microstructure of rodent incisors in three dimensions (3D) with the ameloblasts in situ. We proposed interpretations regarding the possible relationships between the workings of the ameloblasts and the resulting enamel prisms, especially how the phenomenon of decussation is generated. Finally, we were able to represent the two main types of modern rodent incisor microstructures (uniserial and multiserial decussations), as a set of parameters that have been entered into the 3D enamel simulation software Simulenam to generate 3D models that can be digitally manipulated. Associating 2D data of incisor enamel microstructure of fossil rodents and Simulenam, it was then possible to better understand how the various decussation parameters evolved through time and gave rise to the two modern microstructure types from the same ancestral type (pauciserial). This study also confirmed that rodent and artiodactyl enamel do not share the same mechanism of decussation formation. Anat Rec, 302:1195-1209, 2019. © 2018 Wiley Periodicals, Inc.

The petrosal and bony labyrinth of Diplobune minor, an enigmatic Artiodactyla from the Oligocene of Western Europe.

Anoplotheriinae are Paleogene European artiodactyls that present a unique postcranial morphology with a tridactyl autopodium and uncommon limb orientation. This peculiar morphology led to various hypotheses regarding anoplotheriine locomotion from semiaquatic to partly arboreal or partly bipedal. The petrosal bone, housing the organs of balance, and hearing, offers complementary information to postcranial morphology on the ecology of this uncommon artiodactyl. Here, we investigate the middle ear and bony labyrinth of the small anoplotheriine Diplobune minor based on four specimens from the Early Oligocene locality of Itardies (Quercy, France). A macroscopic study coupled with a µCT scan investigation of the petrosal anatomy provides novel information on the bony labyrinth, stapes, and innervation and vasculature of the inner ear of this enigmatic taxon. The petrosal of D. minor exhibits a mosaic of plesiomorphic characters and peculiar features that shed new light into the anatomy of this poorly studied taxon of an obscure taxonomic clade. We can confidently reject that D. minor was a semiaquatic species based on the petrosal morphology: presence of a large mastoid process and nonpachyostotic tegmen tympani do not support underwater hearing. On the other hand, the average semicircular canal radius points to a slow or medium slow agility for D. minor, and fully rejects it was a fast moving animal, which is congruent with its postcranial anatomy.

Hippos stem from the longest sequence of terrestrial cetartiodactyl evolution in Africa.

According to molecular data, hippopotamuses and cetaceans form a clade excluding other extant cetartiodactyls. Despite a wealth of spectacular specimens documenting cetacean evolution, this relationship remains poorly substantiated by the fossil record. Indeed, the evolutionary path leading from the hippo-cetacean ancestor to Hippopotamidae is plagued by missing fossil data and phylogenetic uncertainties. Only an origination within the extinct anthracotheres is compatible with molecular results, substantial filling of phyletic gaps and recent discoveries of early Miocene hippopotamids. Yet, the anthracothere stock that gave rise to Hippopotamidae has not been identified. Consequently, recent phylogenetic accounts do not properly integrate the anthracotheriid hypothesis, and relate Hippopotamidae to a stretched ghost lineage and/or close to Suina. Here we describe a new anthracothere from Lokone (Kenya) that unambiguously roots the Hippopotamidae into a well-identified group of bothriodontines, the first large mammals to invade Africa. The hippos are deeply anchored into the African Paleogene.

First record of a parapithecid primate from the Oligocene of Kenya.

Recent excavations in northwestern Kenya have recovered a vertebrate fauna of late early or early late Oligocene age. Among the mammal remains, a fragmentary lower jaw and an isolated upper molar have been attributed to a small primate, Lokonepithecus manai gen. et sp. nov. Lokonepithecus is a primitive member of the Parapithecidae and possibly most closely related to Apidium from the Fayum. The new primate from Kenya is the youngest parapithecid known and its occurrence in the Oligocene of Kenya suggests that sub-Saharan Africa probably played a major role in the evolutionary history of several groups of mammals.

Evolving between land and water: key questions on the emergence and history of the Hippopotamidae (Hippopotamoidea, Cetancodonta, Cetartiodactyla).

The fossil record of the Hippopotamidae can shed light on three major issues in mammalian evolution. First, as the Hippopotamidae are the extant sister group of Cetacea, gaining a better understanding of the origin of the Hippopotamidae and of their Paleogene ancestors will be instrumental in clarifying phylogenetic relationships within Cetartiodactyla. Unfortunately, the data relevant to hippopotamid origins have generally been ignored in phylogenetic analyses of cetartiodactyls. In order to obtain better resolution, future analyses should consider hypotheses of hippopotamid Paleogene relationships. Notably, an emergence of the Hippopotamidae from within anthracotheriids has received growing support, leading to reconciliation between genetic and morphological evidence for the clade Cetancodonta (Hippopotamidae + Cetacea). Secondly, full account needs to be taken of the Hippopotamidae when studying the impact of environmental change on faunal evolution. This group of semi-aquatic large herbivores has a clear and distinct ecological role and a diverse and abundant fossil record, particularly in the African Neogene. We examine three major phases of hippopotamid evolution, namely the sudden appearance of hippopotamines in the late Miocene (the "Hippopotamine Event"), the subsequent rampant endemism in African basins, and the Pleistocene expansion of Hippopotamus. Each may have been influenced by multiple factors, including: late Miocene grass expansion, African hydrographical network disruption, and a unique set of adaptations that allowed Hippopotamus to respond efficiently to early Pleistocene environmental change. Thirdly, the fossil record of the Hippopotamidae documents the independent emergence of adaptive character complexes in relation to semiaquatic habits and in response to insular isolation. The semiaquatic specializations of fossil hippopotamids are particularly useful in interpreting the functional morphology and ecology of other, extinct groups of large semiaquatic herbivores. Hippopotamids can also serve as models to elucidate the evolutionary dynamics of island mammals.

Early Miocene hippopotamids (Cetartiodactyla) constrain the phylogenetic and spatiotemporal settings of hippopotamid origin.

The affinities of the Hippopotamidae are at the core of the phylogeny of Cetartiodactyla (even-toed mammals: cetaceans, ruminants, camels, suoids, and hippos). Molecular phylogenies support Cetacea as sister group of the Hippopotamidae, implying a long ghost lineage between the earliest cetaceans (approximately 53 Ma) and the earliest hippopotamids (approximately 16 Ma). Morphological studies have proposed two different sister taxa for hippopotamids: suoids (notably palaeochoerids) or anthracotheriids. Evaluating these phylogenetic hypotheses requires substantiating the poorly known early history of the Hippopotamidae. Here, we undertake an original morphological phylogenetic analysis including several "suiform" families and previously unexamined early Miocene taxa to test previous conflicting hypotheses. According to our results, Morotochoerus ugandensis and Kulutherium rusingensis, until now regarded as the sole African palaeochoerid and the sole African bunodont anthracotheriid, respectively, are unambiguously included within the Hippopotamidae. They are the earliest known hippopotamids and set the family fossil record back to the early Miocene (approximately 21 Ma). The analysis reveals that hippopotamids displayed an unsuspected taxonomic and body size diversity and remained restricted to Africa during most of their history, until the latest Miocene. Our results also confirm the deep nesting of Hippopotamidae within the paraphyletic Anthracotheriidae; this finding allows us to reconstruct the sequence of dental innovations that links advanced selenodont anthracotheriids to hippopotamids, previously a source of major disagreements on hippopotamid origins. The analysis demonstrates a close relationship between Eocene choeropotamids and anthracotheriids, a relationship that potentially fills the evolutionary gap between earliest hippopotamids and cetaceans implied by molecular analyses.

Cosmogenic nuclide dating of Sahelanthropus tchadensis and Australopithecus bahrelghazali: Mio-Pliocene hominids from Chad.

Ages were determined at two hominid localities from the Chad Basin in the Djurab Desert (Northern Chad). In the Koro Toro fossiliferous area, KT 12 locality (16 degrees 00'N, 18 degrees 53'E) was the site of discovery of Australopithecus bahrelghazali (Abel) and in the Toros-Menalla fossiliferous area, TM 266 locality (16 degrees 15'N, 17 degrees 29'E) was the site of discovery of Sahelanthropus tchadensis (Toumaï). At both localities, the evolutive degree of the associated fossil mammal assemblages allowed a biochronological estimation of the hominid remains: early Pliocene (3-3.5 Ma) at KT 12 and late Miocene ( approximately 7 Ma) at TM 266. Atmospheric (10)Be, a cosmogenic nuclide, was used to quasicontinuously date these sedimentary units. The authigenic (10)Be/(9)Be dating of a pelite relic within the sedimentary level containing Abel yields an age of 3.58 +/- 0.27 Ma that points to the contemporaneity of Australopithecus bahrelghazali (Abel) with Australopithecus afarensis (Lucy). The 28 (10)Be/(9)Be ages obtained within the anthracotheriid unit containing Toumaï bracket, by absolute dating, the age of Sahelanthropus tchadensis to lie between 6.8 and 7.2 Ma. This chronological constraint is an important cornerstone both for establishing the earliest stages of hominid evolution and for new calibrations of the molecular clock.

Anthracothere dental anatomy reveals a late Miocene Chado-Libyan bioprovince.

Recent discovery of an abundant and diverse late Miocene fauna at Toros-Ménalla (Chad, central Africa) by the Mission Paléoanthropologique Franco-Tchadienne provides a unique opportunity to examine African faunal and hominid evolution relative to the early phases of the Saharan arid belt. This study presents evidence from an African Miocene anthracotheriid Libycosaurus, particularly well documented at Toros-Ménalla. Its remains reveal a large semiaquatic mammal that evolved an autapomorphic upper fifth premolar (extremely rare in Cenozoic mammals). The extra tooth appeared approximately 12 million years ago, probably in a small northern African population isolated by climate-driven fragmentation and alteration of the environments inhabited by these anthracotheriids [Flower, B. P. & Kennett, J. P. (1994) Palaeogeogr. Palaeoclimatol. Palaeoecol. 108, 537-555 and Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. (2001) Science 292, 686-693]. The semiaquatic niche of Libycosaurus, combined with the distribution and relationships of its late Miocene species, indicates that by the end of the Miocene, wet environments connected the Lake Chad Basin to the Libyan Sirt Basin, across what is now the Sahara desert.

The position of Hippopotamidae within Cetartiodactyla.

The origin of late Neogene Hippopotamidae (Artiodactyla) involves one of the most serious conflicts between comparative anatomy and molecular biology: is Artiodactyla paraphyletic? Molecular comparisons indicate that Cetacea should be the modern sister group of hippos. This finding implies the existence of a fossil lineage linking cetaceans (first known in the early Eocene) to hippos (first known in the middle Miocene). The relationships of hippos within Artiodactyla are challenging, and the immediate affinities of Hippopotamidae have been studied by biologists for almost two centuries without resolution. Here, we compare opposing hypotheses implicating several "suiform" families. This morphological analysis of a comprehensive set of taxa and characters offers a robust solution to the origins of Hippopotamidae. This family appears to be deeply nested within the otherwise extinct artiodactyl family Anthracotheriidae, most precisely within the most advanced selenodont forms. The proposed sister group of hippos is the middle to late Miocene African semiaquatic Libycosaurus. Any close relationships of hippos with suoids, particularly with Tayassuidae, are rejected. Furthermore, the clade (Hippopotamidae, Anthracotheriidae) is proposed as the sister group of the Cetacea, offering broad morphological support for a molecular phylogeny, such support being also consistent with the fossil record. Corroboration of this relationship requires an exploration of anthracothere affinities with other Paleogene artiodactyls. Among those, the position of Ruminantia is a central question, still to be solved. Further progress in this debate is likely to come from morphological studies of paleontological data, whether known or still to be discovered.

Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad.

All six known specimens of the early hominid Sahelanthropus tchadensis come from Toros-Menalla site 266 (TM 266), a single locality in the Djurab Desert, northern Chad, central Africa. Here we present a preliminary analysis of the palaeontological and palaeoecological context of these finds. The rich fauna from TM 266 includes a significant aquatic component such as fish, crocodiles and amphibious mammals, alongside animals associated with gallery forest and savannah, such as primates, rodents, elephants, equids and bovids. The fauna suggests a biochronological age between 6 and 7 million years. Taken together with the sedimentological evidence, the fauna suggests that S. tchadensis lived close to a lake, but not far from a sandy desert, perhaps the oldest record of desert conditions in the Neogene of northern central Africa.

A new hominid from the Upper Miocene of Chad, Central Africa.

The search for the earliest fossil evidence of the human lineage has been concentrated in East Africa. Here we report the discovery of six hominid specimens from Chad, central Africa, 2,500 km from the East African Rift Valley. The fossils include a nearly complete cranium and fragmentary lower jaws. The associated fauna suggest the fossils are between 6 and 7 million years old. The fossils display a unique mosaic of primitive and derived characters, and constitute a new genus and species of hominid. The distance from the Rift Valley, and the great antiquity of the fossils, suggest that the earliest members of the hominid clade were more widely distributed than has been thought, and that the divergence between the human and chimpanzee lineages was earlier than indicated by most molecular studies.