Drivers of the artiodactyl turnover in insular western Europe at the Eocene-Oligocene Transition.

Simultaneously investigating the effects of abiotic and biotic factors on diversity dynamics is essential to understand the evolutionary history of clades. The Grande Coupure corresponds to a major faunal turnover at the Eocene-Oligocene transition (EOT) (~34.1 to 33.55 Mya) and is defined in western Europe as an extinction of insular European mammals coupled with the arrival of crown clades from Asia. Here, we focused on the species-rich group of endemic European artiodactyls to determine the drivers of the Grande Coupure during the major environmental disruptions at the EOT. Using Bayesian birth-death models, we analyzed an original high-resolution fossil dataset (90 species, >2,100 occurrences) from southwestern France (Quercy area) and estimated the regional diversification and diversity dynamics of endemic and immigrant artiodactyls. We show that the endemic artiodactyl radiation was mainly related to the Eocene tropical conditions, combined with biotic controls on speciation and clade-related diversity dependence. We further highlight that the major environmental changes at the transition (77% of species became extinct) and the concurrent increase in seasonality in Europe during the Oligocene were likely the main drivers of their decline. Surprisingly, our results do not support the widely-held hypothesis of active competition between endemic and immigrant artiodactyls but rather suggest a passive or opportunistic replacement by immigrants, which is further supported by morphological clustering of specific ecological traits across the Eocene-Oligocene transition. Our analyses provide insights into the evolutionary and ecological processes driving the diversification and decline of mammalian clades during a major biological and climatic crisis.

Endocranial Casts of Camelops hesternus and Palaeolama sp.: New Insights into the Recent History of the Camelid Brain.

Endocranial casts are capable of capturing the general brain form in extinct mammals due to the high fidelity of the endocranial cavity and the brain in this clade. Camelids, the clade including extant camels, llamas, and alpacas, today display high levels of gyrification and brain complexity. The evolutionary history of the camelid brain has been described as involving unique neocortical growth dynamics which may have led to its current state. However, these inferences are based on their fossil endocast record from approximately ∼40 Mya (Eocene) to ∼11 Mya (Miocene), with a gap in this record for the last ∼10 million years. Here, we present the first descriptions of two camelid endocrania that document the recent history of the camelid brain: a new specimen of Palaeolama sp. from ∼1.2 Mya, and the plaster endocast of Camelops hesternus, a giant camelid from ∼44 to 11 Kya which possessed the largest brain (∼990 g) of all known camelids. We find that neocortical complexity evolved significantly between the Miocene and Pleistocene Epochs. Already ∼1.2 Mya the camelid brain presented morphologies previously known only in extant taxa, especially in the frontal and parietal regions, which may also be phylogenetic informative. The new fossil data indicate that during the Pleistocene, camelid brain dynamics experienced neocortical invagination into the sagittal sinus rather than evagination out of it, as observed in Eocene to Miocene taxa.

Early evolution of the ossicular chain in Cetacea: into the middle ear gears of a semi-aquatic protocetid whale.

Modifications of the morphology and acoustic properties of the ossicular chain are among the major changes that accompanied the adaptation of Cetacea to the aquatic environment. Thus, data on the middle ear ossicles of early whales are crucial clues to understand the first steps of the emblematic terrestrial/aquatic transition that occurred in that group. Yet, the delicate nature and very small size of these bones make their preservation in the fossil record extremely rare. Due to the scarcity of available data, major questions remain concerning the sound transmission pathways in early non-fully aquatic whales. Virtual reconstruction of a partially complete ossicular chain of an Eocene protocetid whale documents for the first time the three ossicles of a semi-aquatic archaeocete. Contrary to previous hypotheses, these ossicles present different evolutionary patterns, showing that the ossicular chain does not act as a single morphological module. Functional analyses of the different middle ear units highlight a mosaic pattern of terrestrial and aquatic signatures. This integrative anatomical and functional study brings strong evidence that protocetids were adapted to their dual acoustic environment with efficient hearing in both air and water.

Endocranial morphology of Microchoerus erinaceus (Euprimates, Tarsiiformes) and early evolution of the Euprimates brain.

OBJECTIVES: Innovations in brain structure and increase in brain size relative to body mass are key features of Primates evolutionary history. Surprisingly, the endocranial morphology of early Euprimates is still rather poorly known, and our understanding of early euprimate brain evolution (Eocene epoch) relies on a handful of specimens. MATERIALS AND METHODS: In this article, we describe the endocranial cast of the tarsiiform Microchoerus erinaceus from the late Early Eocene of Perrière (Quercy fissure filling, France) based on a virtual reconstruction extracted from CT scan data of the endocranial cavity of the complete, undeformed specimen UM-PRR1771. RESULTS: The endocast of M. erinaceus shows the derived features observed in other Euprimates (e.g. sylvian fissure and temporal lobe), with limited neocortical folding, and a telencephalic flexure comparable to that of extant primates. DISCUSSION: Comparison with the endocasts of other available late Eocene primates shows that they already exhibited a variety of brain morphologies, highlighting the complex history of the external features of the primate brain, as early as the Eocene. M. erinaceus was a fruit and gum eater considered as nocturnal based on its orbit size. However, its brain showed small olfactory bulbs--smaller than in the coeval diurnal taxa Adapis parisiensis--and a neocorticalization similar to folivorous taxa. These observations contrast with patterns observed in primates today where nocturnal taxa have larger olfactory bulbs than diurnal taxa, and call into question a direct correlation between frugivory and neocorticalization increase in primates.

Endocranial morphology of Palaeocene Plesiadapis tricuspidens and evolution of the early primate brain.

Expansion of the brain is a key feature of primate evolution. The fossil record, although incomplete, allows a partial reconstruction of changes in primate brain size and morphology through time. Palaeogene plesiadapoids, closest relatives of Euprimates (or crown-group primates), are crucial for understanding early evolution of the primate brain. However, brain morphology of this group remains poorly documented, and major questions remain regarding the initial phase of euprimate brain evolution. Micro-CT investigation of the endocranial morphology of Plesiadapis tricuspidens from the Late Palaeocene of Europe--the most complete plesiadapoid cranium known--shows that plesiadapoids retained a very small and simple brain. Plesiadapis has midbrain exposure, and minimal encephalization and neocorticalization, making it comparable with that of stem rodents and lagomorphs. However, Plesiadapis shares a domed neocortex and downwardly shifted olfactory-bulb axis with Euprimates. If accepted phylogenetic relationships are correct, then this implies that the euprimate brain underwent drastic reorganization during the Palaeocene, and some changes in brain structure preceded brain size increase and neocortex expansion during evolution of the primate brain.

A 50-million-year-old, three-dimensionally preserved bat skull supports an early origin for modern echolocation.

Bats are among the most recognizable, numerous, and widespread of all mammals. But much of their fossil record is missing, and bat origins remain poorly understood, as do the relationships of early to modern bats. Here, we describe a new early Eocene bat that helps bridge the gap between archaic stem bats and the hyperdiverse modern bat radiation of more than 1,460 living species. Recovered from ∼50 million-year-old cave sediments in the Quercy Phosphorites of southwestern France, Vielasia sigei's remains include a near-complete, three-dimensionally preserved skull-the oldest uncrushed bat cranium yet found. Phylogenetic analyses of a 2,665 craniodental character matrix, with and without 36.8 kb of DNA sequence data, place Vielasia outside modern bats, with total evidence tip-dating placing it sister to the crown clade. Vielasia retains the archaic dentition and skeletal features typical of early Eocene bats, but its inner ear shows specializations found in modern echolocating bats. These features, which include a petrosal only loosely attached to the basicranium, an expanded cochlea representing ∼25% basicranial width, and a long basilar membrane, collectively suggest that the kind of laryngeal echolocation used by most modern bats predates the crown radiation. At least 23 individuals of V. sigei are preserved together in a limestone cave deposit, indicating that cave roosting behavior had evolved in bats by the end of the early Eocene; this period saw the beginning of significant global climate cooling that may have been an evolutionary driver for bats to first congregate in caves.

Middle Eocene rodents from Peruvian Amazonia reveal the pattern and timing of caviomorph origins and biogeography.

The long-term isolation of South America during most of the Cenozoic produced a highly peculiar terrestrial vertebrate biota, with a wide array of mammal groups, among which caviomorph rodents and platyrrhine primates are Mid-Cenozoic immigrants. In the absence of indisputable pre-Oligocene South American rodents or primates, the mode, timing and biogeography of these extraordinary dispersals remained debated. Here, we describe South America's oldest known rodents, based on a new diverse caviomorph assemblage from the late Middle Eocene (approx. 41 Ma) of Peru, including five small rodents with three stem caviomorphs. Instead of being tied to the Eocene/Oligocene global cooling and drying episode (approx. 34 Ma), as previously considered, the arrival of caviomorphs and their initial radiation in South America probably occurred under much warmer and wetter conditions, around the Mid-Eocene Climatic Optimum. Our phylogenetic results reaffirm the African origin of South American rodents and support a trans-Atlantic dispersal of these mammals during Middle Eocene times. This discovery further extends the gap (approx. 15 Myr) between first appearances of rodents and primates in South America.

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.

Infrasonic and Ultrasonic Hearing Evolved after the Emergence of Modern Whales.

Mysticeti (baleen whales) and Odontoceti (toothed whales) today greatly differ in their hearing abilities: Mysticeti are presumed to be sensitive to infrasonic noises [1-3], whereas Odontoceti are sensitive to ultrasonic sounds [4-6]. Two competing hypotheses exist regarding the attainment of hearing abilities in modern whales: ancestral low-frequency sensitivity [7-13] or ancestral high-frequency sensitivity [14, 15]. The significance of these evolutionary scenarios is limited by the undersampling of both early-diverging cetaceans (archaeocetes) and terrestrial hoofed relatives of cetaceans (non-cetacean artiodactyls). Here, we document for the first time the bony labyrinth, the hollow cavity housing the hearing organ, of two species of protocetid whales from Lutetian deposits (ca. 46-43 Ma) of Kpogamé, Togo. These archaeocete cetaceans, which are transitional between terrestrial and aquatic forms, prove to be a key for determining the hearing abilities of early whales. We propose a new evolutionary picture for the early stages of this history, based on qualitative and quantitative studies of the cochlear morphology of an unparalleled sample of extant and extinct land artiodactyls and cetaceans. Contrary to the hypothesis that archaeocetes have been more sensitive to high-frequency sounds than their terrestrial ancestors [15], we demonstrate that early cetaceans presented a cochlear functional pattern close to that of their terrestrial relatives, and that specialization for infrasonic or ultrasonic hearing in Mysticeti or Odontoceti, respectively, instead only occurred in fully aquatic whales, after the emergence of Neoceti (Mysticeti+Odontoceti).

Digital cranial endocast of Hyopsodus (Mammalia, "Condylarthra"): a case of paleogene terrestrial echolocation?

We here describe the endocranial cast of the Eocene archaic ungulate Hyopsodus lepidus AMNH 143783 (Bridgerian, North America) reconstructed from X-ray computed microtomography data. This represents the first complete cranial endocast known for Hyopsodontinae. The Hyopsodus endocast is compared to other known "condylarthran" endocasts, i. e. those of Pleuraspidotherium (Pleuraspidotheriidae), Arctocyon (Arctocyonidae), Meniscotherium (Meniscotheriidae), Phenacodus (Phenacodontidae), as well as to basal perissodactyls (Hyracotherium) and artiodactyls (Cebochoerus, Homacodon). Hyopsodus presents one of the highest encephalization quotients of archaic ungulates and shows an "advanced version" of the basal ungulate brain pattern, with a mosaic of archaic characters such as large olfactory bulbs, weak ventral expansion of the neopallium, and absence of neopallium fissuration, as well as more specialized ones such as the relative reduction of the cerebellum compared to cerebrum or the enlargement of the inferior colliculus. As in other archaic ungulates, Hyopsodus midbrain exposure is important, but it exhibits a dorsally protruding largely developed inferior colliculus, a feature unique among "Condylarthra". A potential correlation between the development of the inferior colliculus in Hyopsodus and the use of terrestrial echolocation as observed in extant tenrecs and shrews is discussed. The detailed analysis of the overall morphology of the postcranial skeleton of Hyopsodus indicates a nimble, fast moving animal that likely lived in burrows. This would be compatible with terrestrial echolocation used by the animal to investigate subterranean habitat and/or to minimize predation during nocturnal exploration of the environment.

A rhinocerotid skull cooked-to-death in a 9.2 Ma-old ignimbrite flow of Turkey.

BACKGROUND: Preservation of fossil vertebrates in volcanic rocks is extremely rare. An articulated skull (cranium and mandible) of a rhinoceros was found in a 9.2±0.1 Ma-old ignimbrite of Cappadocia, Central Turkey. The unusual aspect of the preserved hard tissues of the skull (rough bone surface and brittle dentine) allows suspecting a peri-mortem exposure to a heating source. METHODOLOGY/PRINCIPAL FINDINGS: Here we describe and identify the skull as belonging to the large two-horned rhinocerotine Ceratotherium neumayri, well-known in the late Miocene of the Eastern Mediterranean Province. Gross structural features and microscopic changes of hard tissues (bones and teeth) are then monitored and compared to the results of forensic and archaeological studies and experiments focusing on heating effects, in order to reconstruct the hypothetical peri-mortem conditions. Macroscopic and microscopic structural changes on compact bones (canaliculi and lamellae vanished), as well as partial dentine/cementum disintegration, drastic enamel-dentine disjunctions or microscopic cracks affecting all hard dental tissues (enamel, cementum, and dentine) point to continued exposures to temperatures around 400-450°C. Comparison to other cases of preservation of fossil vertebrates within volcanic rocks points unambiguously to some similarity with the 79 AD Plinian eruption of the Vesuvius, in Italy. CONCLUSIONS/SIGNIFICANCE: A 9.2±0.1 Ma-old pyroclastic density current, sourced from the Çardak caldera, likely provoked the instant death of the Karacasar rhino, before the body of the latter experienced severe dehydration (leading to the wide and sustainable opening of the mouth), was then dismembered within the pyroclastic flow of subaerial origin, the skull being separated from the remnant body and baked under a temperature approximating 400°C, then transported northward, rolled, and trapped in disarray into that pyroclastic flow forming the pinkish Kavak-4 ignimbrite ∼30 km North from the upper Miocene vent.