Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy.

Endothermy underpins the ecological dominance of mammals and birds in diverse environmental settings1,2. However, it is unclear when this crucial feature emerged during mammalian evolutionary history, as most of the fossil evidence is ambiguous3-17. Here we show that this key evolutionary transition can be investigated using the morphology of the endolymph-filled semicircular ducts of the inner ear, which monitor head rotations and are essential for motor coordination, navigation and spatial awareness18-22. Increased body temperatures during the ectotherm-endotherm transition of mammal ancestors would decrease endolymph viscosity, negatively affecting semicircular duct biomechanics23,24, while simultaneously increasing behavioural activity25,26 probably required improved performance27. Morphological changes to the membranous ducts and enclosing bony canals would have been necessary to maintain optimal functionality during this transition. To track these morphofunctional changes in 56 extinct synapsid species, we developed the thermo-motility index, a proxy based on bony canal morphology. The results suggest that endothermy evolved abruptly during the Late Triassic period in Mammaliamorpha, correlated with a sharp increase in body temperature (5-9 °C) and an expansion of aerobic and anaerobic capacities. Contrary to previous suggestions3-14, all stem mammaliamorphs were most probably ectotherms. Endothermy, as a crucial physiological characteristic, joins other distinctive mammalian features that arose during this period of climatic instability28.

The maxillary canal of the titanosuchid Jonkeria (Synapsida, Dinocephalia).

The maxillary canal of the titanosuchid dinocephalian Jonkeria is described based on digitised serial sections. We highlight that its morphology is more like that of the tapinocephalid Moschognathus than that of Anteosaurus. This is unexpected given the similarities between the dentition of Jonkeria and Anteosaurus (i.e., presence of a canine) and the fact that the branching pattern of the maxillary canal in synapsids usually co-varies with dentition. Hypotheses to account for similarities between Jonkeria and Moschognathus (common ancestry, function in social signalling or underwater sensing) are discussed. It is likely that the maxillary canal carries a strong phylogenetic signal, here supporting the clade Tapinocephalia.

Attentional bias and response inhibition in severe obesity with food disinhibition: a study of P300 and N200 event-related potential.

BACKGROUND/OBJECTIVE: In obesity there is growing evidence for common mechanism between food intake regulation and substance use disorders, especially more attentional bias and less cognitive control. In the present study we investigated whether severely obese subjects with or without disordered eating exhibit electroencephalographic (EEG) event-related potential (ERP) modifications as observed in substance abusers. SUBJECTS/METHODS: A total of 90 women were included; 30 in the normal-weight (NW) group (18.5 < BMI < 24.5 kg/m2; no food disinhibition or restriction on the Three-Factor Eating Questionnaire) and 60 participants with BMI ≥ 35 kg/m2 were separated into two groups (n = 30): without food disinhibition (disinhibition score ≤8; ObFD- group) and with food disinhibition (score >8; ObFD+). Clinical and metabolic parameters as well as compartmental aspects (Eating Disorders Inventory-2, EDI-2) were assessed. Participants underwent an ERP recording with an auditory oddball paradigm. RESULTS: The mean ± SD P300 amplitudes in Pz were significantly (p < 0.05) lower in ObFD- (12.4 ± 4.6) and ObFD+ (12.5 ± 4.4) groups than in the NW group (15.8 ± 5.9). The mean ± SD N200 amplitude in Cz was significantly lower in the ObFD- group (-2.0 ± 5.4) than in the NW group (-5.2 ± 4.2 vs; p = 0.035). N200 Cz amplitude was correlated with EDI-2 Binge eating risk score (ρ = 0.331; p = 0.01), EDI-2 Body Dissatisfaction score (ρ = 0.351; p = 0.007), and Drive for Thinness score (ρ = 0.26; p = 0.05). CONCLUSIONS: The present study provides evidence for reduction of P300 and N200 amplitude in obese women and that N200 amplitude may be related to more disordered eating and eating disorder risk. This leads to consider attentional bias and response inhibition as core mechanisms in obesity and as possible targets for new therapeutic strategy.

One small step: A review of Plio-Pleistocene hominin foot evolution.

Bipedalism is a hallmark of being human and the human foot is modified to reflect this unique form of locomotion. Leonardo da Vinci is credited with calling the human foot "a masterpiece of engineering and a work of art." However, a scientific approach to human origins has revealed that our feet are products of a long, evolutionary history in which a mobile, grasping organ has been converted into a propulsive structure adapted for the rigors of bipedal locomotion. Reconstructing the evolutionary history of foot anatomy benefits from a fossil record; yet, prior to 1960, the only hominin foot bones recovered were from Neandertals. Even into the 1990s, the human foot fossil record consisted mostly of fragmentary remains. However, in the last two decades, the human foot fossil record has quadrupled, and these new discoveries have fostered fresh new perspectives on how our feet evolved. In this review, we document anatomical differences between extant ape and human foot bones, and comprehensively examine the hominin foot fossil record. Additionally, we take a novel approach and conduct a cladistics analysis on foot fossils (n = 19 taxa; n = 80 characters), and find strong evidence for mosaic evolution of the foot, and a variety of anatomically and functionally distinct foot forms as bipedal locomotion evolved.

The mystery of a missing bone: revealing the orbitosphenoid in basal Epicynodontia (Cynodontia, Therapsida) through computed tomography.

The basal non-mammaliaform cynodonts from the late Permian (Lopingian) and Early Triassic are a major source of information for the understanding of the evolutionary origin of mammals. Detailed knowledge of their anatomy is critical for understanding the phylogenetic transition toward mammalness and the paleobiological reconstruction of mammalian precursors. Using micro-computed tomography (µCT), we describe the internal morphology of the interorbital region that includes the rarely fossilized orbitosphenoid elements in four basal cynodonts. These paired bones, which are positioned relatively dorsally in the skull, contribute to the wall of the anterior part of the braincase and form the floor for the olfactory lobes. Unlike procynosuchids and the more basal therapsids in which the orbitosphenoids are well developed, dense, and bear a ventral keel, the basal epicynodonts Cynosaurus, Galesaurus, and Thrinaxodon display cancellous, reduced, and loosely articulated orbitosphenoids, a condition shared with many eucynodonts. The hemi-cylindrical orbitosphenoid from which the mammalian condition is derived re-evolved convergently in traversodontid and some probainognathian cynodonts.

Endocranial Casts of Pre-Mammalian Therapsids Reveal an Unexpected Neurological Diversity at the Deep Evolutionary Root of Mammals.

The origin and evolution of the mammalian brain has long been the focus of scientific enquiry. Conversely, little research has focused on the palaeoneurology of the stem group of Mammaliaformes, the Permian and Triassic non-mammaliaform Therapsida (NMT). This is because the majority of the NMT have a non-ossified braincase, making the study of their endocranial cast (sometimes called the "fossil brain") problematic. Thus, descriptions of the morphology and size of NMT endocranial casts have been based largely on approximations rather than reliable determination. Accordingly, here we use micro-CT scans of the skulls of 1 Dinocephalia and 3 Biarmosuchia, which are NMT with a fully ossified braincase and thus a complete endocast. For the first time, our work enables the accurate determination of endocranial shape and size in NMT. This study suggests that NMT brain size falls in the upper range of the reptilian and amphibian variation. Brain size in the dicynodont Kawingasaurus is equivalent to that of early Mammaliaformes, whereas the Dinocephalia show evidence of a secondary reduction of brain size. In addition, unlike other NMT in which the endocast has a tubular shape and its parts are arranged in a linear manner, the biarmosuchian endocast is strongly flexed at the level of the midbrain, creating a near right angle between the fore- and hindbrain. These data highlight an unexpected diversity of endocranial size and morphology in NMT, features that are usually considered conservative in this group.

Physiological implications of the abnormal absence of the parietal foramen in a late Permian cynodont (Therapsida).

The third eye (pineal eye), an organ responsible for regulating exposure to sunlight in extant ectotherms, is located in an opening on the dorsal surface of the skull, the parietal foramen. The parietal foramen is absent in extant mammals but often observed in basal therapsids, the stem-group to true mammals. Here, we report the absence of the parietal foramen in a specimen of Cynosaurus suppostus, a Late Permian cynodont from South Africa (SA). Comparison with Procynosuchus delaharpeae, a contemporaneous non-mammalian cynodont from SA, demonstrates that the absence of this foramen is an abnormal condition for such a basal species. Because seasonality was marked during the Late Permian in SA, it is proposed that the third eye was functionally redundant in Cynosaurus, possibly due to the acquisition of better thermoregulation or the evolution of specialized cells in the lateral eyes to compensate for the role of the third eye.

First CT-assisted study of the palate and postcrania of Diarthrognathus broomi (Cynodontia, Probainognathia).

Diarthrognathus broomi is a transitional taxon between non-mammaliaform cynodonts and Mammaliaformes that occurred during the Late Triassic to Early Jurassic. All known specimens of Diarthrognathus represent juveniles, and the postcrania have not been thoroughly described. The palatal, basicranial and postcranial elements of the referred specimen NMQR 1535 are described here for the first time using 3D reconstructions generated from X-ray micro-computed tomography (µCT) data. The presence of a large interpterygoid vacuity, open medial suture between the vomers and medially unossified secondary palate all support the interpretation that NMQR 1535 is a juvenile. In addition, Diarthrognathus uniquely possesses "suborbital" vacuities, which distinguishes it from every other known cynodont. The presence of an ossified olecranon process, among other features, suggests that Diarthrognathus may have been a scratch-digger. The postcranial skeleton of Diarthrognathus appears to be more plesiomorphic than tritylodontids, Brasilodon and other tritheledontids as, among other traits, it retains amphicoelous vertebrae. However, this taxon also displays synapomorphies with the more derived cynodonts, such as the mammalian pattern of neurocentral ossification and possible absence of an ectepicondylar foramen.

New insights into the ear region anatomy and cranial blood supply of advanced stem Strepsirhini: evidence from three primate petrosals from the Eocene of Chambi, Tunisia.

We report the discovery of three isolated primate petrosal fragments from the fossiliferous locality of Chambi (Tunisia), a primate-bearing locality dating from the late early to the early middle Eocene. These fossils display a suite of anatomical characteristics otherwise found only in strepsirhines, and as such might be attributed either to Djebelemur or/and cf. Algeripithecus, the two diminutive stem strepsirhine primates recorded from this locality. Although damaged, the petrosals provide substantial information regarding the ear anatomy of these advanced stem strepsirhines (or pre-tooth-combed primates), notably the patterns of the pathway of the arterial blood supply. Using µCT-scanning techniques and digital segmentation of the structures, we show that the transpromontorial and stapedial branches of the internal carotid artery (ICA) were present (presence of bony tubes), but seemingly too small to supply enough blood to the cranium alone. This suggests that the ICA was not the main cranial blood supply in stem strepsirhines, but that the pharyngeal or vertebral artery primitively ensured a great part of this role instead, an arterial pattern that is reminiscent of modern cheirogaleid, lepilemurid lemuriforms and lorisiforms. This could explain parallel loss of the ICA functionality among these families. Specific measurements made on the cochlea indicate that the small strepsirhine primate(s) from Chambi was (were) highly sensitive to high frequencies and poorly sensitive to low frequencies. Finally, variance from orthogonality of the plane of the semicircular canals (SCs) calculated on one petrosal (CBI-1-569) suggests that Djebelemur or cf. Algeripithecus likely moved (at least its head) in a way similar to that of modern mouse lemurs.

A memory already like an elephant's? The advanced brain morphology of the last common ancestor of Afrotheria (Mammalia).

Virtually reconstructed and natural endocranial casts are used in the study of brain evolution through geological time. We here present work investigating the paleoneurological evolution of afrotherian mammals. Using microCT-generated endocasts we show that, with the exception of the subfamilies Macroscelidinae and Tenrecoidea, most Afroinsectiphilia display a more or less gyrencephalic and ventrally expanded neopallium, two derived features that are unexpected for these insectivore-grade afrotherians. This implies that the endocranial cast morphology at the root of the afrotherian clade may have been more advanced than previously thought. The reconstructed endocranial morphology of the Afrotheria's last common ancestor reaches the level of complexity of some early Cenozoic archaic ungulates. Our result gives support to the hypothesis of an ungulate-like ancestral body plan for Afrotheria. It also implies that the a priori 'primitive' suite of traits evident in the brain of Afroinsectivora, especially in the tenrecs, may have been secondarily acquired. Implications on the overestimation of the divergence age of Afrotheria are discussed.

Craniodental anatomy in Permian-Jurassic Cynodontia and Mammaliaformes (Synapsida, Therapsida) as a gateway to defining mammalian soft tissue and behavioural traits.

Mammals are diagnosed by more than 30 osteological characters (e.g. squamosal-dentary jaw joint, three inner ear ossicles, etc.) that are readily preserved in the fossil record. However, it is the suite of physiological, soft tissue and behavioural characters (e.g. endothermy, hair, lactation, isocortex and parental care), the evolutionary origins of which have eluded scholars for decades, that most prominently distinguishes living mammals from other amniotes. Here, we review recent works that illustrate how evolutionary changes concentrated in the cranial and dental morphology of mammalian ancestors, the Permian-Jurassic Cynodontia and Mammaliaformes, can potentially be used to document the origin of some of the most crucial defining features of mammals. We discuss how these soft tissue and behavioural traits are highly integrated, and how their evolution is intermingled with that of craniodental traits, thus enabling the tracing of their previously out-of-reach phylogenetic history. Most of these osteological and dental proxies, such as the maxillary canal, bony labyrinth and dental replacement only recently became more easily accessible-thanks, in large part, to the widespread use of X-ray microtomography scanning in palaeontology-because they are linked to internal cranial characters. This article is part of the theme issue 'The mammalian skull: development, structure and function'.

At the root of the mammalian mind: The sensory organs, brain and behavior of pre-mammalian synapsids.

All modern mammals are descendants of the paraphyletic non-mammaliaform Synapsida, colloquially referred to as the "mammal-like reptiles." It has long been assumed that these mammalian ancestors were essentially reptile-like in their morphology, biology, and behavior, i.e., they had a small brain, displayed simple behavior, and their sensory organs were unrefined compared to those of modern mammals. Recent works have, however, revealed that neurological, sensory, and behavioral traits previously considered typically mammalian, such as whiskers, enhanced olfaction, nocturnality, parental care, and complex social interactions evolved before the origin of Mammaliaformes, among the early-diverging "mammal-like reptiles." In contrast, an enlarged brain did not evolve immediately after the origin of mammaliaforms. As such, in terms of paleoneurology, the last "mammal-like reptiles" were not significantly different from the earliest mammaliaforms. The abundant data and literature published in the last 10 years no longer supports the "three pulses" scenario of synapsid brain evolution proposed by Rowe and colleagues in 2011, but supports the new "outside-in" model of Rodrigues and colleagues proposed in 2018, instead. As Mesozoic reptiles were becoming the dominant taxa within terrestrial ecosystems, synapsids gradually adapted to smaller body sizes and nocturnality. This resulted in a sensory revolution in synapsids as olfaction, audition, and somatosensation compensated for the loss of visual cues. This altered sensory input is aligned with changes in the brain, the most significant of which was an increase in relative brain size.

Evolutionary history of hominin brain size and phylogenetic comparative methods.

An absolutely and relatively large brain has traditionally been viewed as a distinctive characteristic of the Homo genus, with anatomically modern humans presented at the apex of a long line of progressive increases in encephalization. Many studies continue to focus attention on increasing brain size in the Homo genus, while excluding measures of absolute and relative brain size of more geologically recent, smaller brained, hominins such as Homo floresiensis, and Homo naledi and smaller brained Homo erectus specimens. This review discusses the benefits of using phylogenetic comparative methods to trace the diverse changes in hominin brain evolution and the drawbacks of not doing so.

From fossils to mind.

Fossil endocasts record features of brains from the past: size, shape, vasculature, and gyrification. These data, alongside experimental and comparative evidence, are needed to resolve questions about brain energetics, cognitive specializations, and developmental plasticity. Through the application of interdisciplinary techniques to the fossil record, paleoneurology has been leading major innovations. Neuroimaging is shedding light on fossil brain organization and behaviors. Inferences about the development and physiology of the brains of extinct species can be experimentally investigated through brain organoids and transgenic models based on ancient DNA. Phylogenetic comparative methods integrate data across species and associate genotypes to phenotypes, and brains to behaviors. Meanwhile, fossil and archeological discoveries continuously contribute new knowledge. Through cooperation, the scientific community can accelerate knowledge acquisition. Sharing digitized museum collections improves the availability of rare fossils and artifacts. Comparative neuroanatomical data are available through online databases, along with tools for their measurement and analysis. In the context of these advances, the paleoneurological record provides ample opportunity for future research. Biomedical and ecological sciences can benefit from paleoneurology's approach to understanding the mind as well as its novel research pipelines that establish connections between neuroanatomy, genes and behavior.

Computed Tomography elucidates ontogeny within the basal therapsid clade Biarmosuchia.

Biarmosuchia is a clade of basal therapsids that includes forms possessing plesiomorphic 'pelycosaurian' cranial characters as well as the highly derived Burnetiamorpha which are characterised by cranial pachyostosis and a variety of cranial bosses. Potential ontogenetic variation in these structures has been suggested based on growth series of other therapsids with pachyostosed crania, which complicates burnetiamorph taxonomic distinction and thus it is essential to better understand cranial ontogeny of the Burnetiamorpha. Here, three new juvenile biarmosuchian skulls from the late Permian of South Africa are described using X-ray micro computed tomography (CT). We found that juvenile biarmosuchians are distinguished from adults by their relatively large orbits, open cranial sutures, and incomplete ossification of the braincase and bony labyrinth. Also, they manifest multiple centres of ossification within the parietal and preparietal bones. CT examination reveals that the holotype of Lemurosaurus pricei (BP/1/816), previously alleged to be a juvenile, shows no evidence of juvenility and is thus probably an adult. This suggests that the larger skull NMQR 1702, previously considered to be an adult L. pricei, may represent a new taxon. This study provides, for the first time, a list of characters by which to recognise juvenile biarmosuchians.

Histology and µCT reveal the unique evolution and development of multiple tooth rows in the synapsid Endothiodon.

Several amniote lineages independently evolved multiple rows of marginal teeth in response to the challenge of processing high fiber plant matter. Multiple tooth rows develop via alterations to tooth replacement in captorhinid reptiles and ornithischian dinosaurs, but the specific changes that produce this morphology differ, reflecting differences in their modes of tooth attachment. To further understand the mechanisms by which multiple tooth rows can develop, we examined this feature in Endothiodon bathystoma, a member of the only synapsid clade (Anomodontia) to evolve a multi-rowed marginal dentition. We histologically sampled Endothiodon mandibles with and without multiple tooth rows as well as single-rowed maxillae. We also segmented functional and replacement teeth in µ-CT scanned mandibles and maxillae of Endothiodon and several other anomodonts with 'postcanine' teeth to characterize tooth replacement in the clade. All anomodonts in our sample displayed a space around the tooth roots for a soft tissue attachment between tooth and jaw in life. Trails of alveolar bone indicate varying degrees of labial migration of teeth through ontogeny, often altering the spatial relationships of functional and replacement teeth in the upper and lower jaws. We present a model of multiple tooth row development in E. bathystoma in which labial migration of functional teeth was extensive enough to prevent resorption and replacement by newer generations of teeth. This model represents another mechanism by which multiple tooth rows evolved in amniotes. The multiple tooth rows of E. bathystoma may have provided more extensive contact between the teeth and a triturating surface on the palatine during chewing.

Brain evolution in Proboscidea (Mammalia, Afrotheria) across the Cenozoic.

As the largest and among the most behaviourally complex extant terrestrial mammals, proboscideans (elephants and their extinct relatives) are iconic representatives of the modern megafauna. The timing of the evolution of large brain size and above average encephalization quotient remains poorly understood due to the paucity of described endocranial casts. Here we created the most complete dataset on proboscidean endocranial capacity and analysed it using phylogenetic comparative methods and ancestral character states reconstruction using maximum likelihood. Our analyses support that, in general, brain size and body mass co-evolved in proboscideans across the Cenozoic; however, this pattern appears disrupted by two instances of specific increases in relative brain size in the late Oligocene and early Miocene. These increases in encephalization quotients seem to correspond to intervals of important climatic, environmental and faunal changes in Africa that may have positively selected for larger brain size or body mass.

Evolution of facial innervation in anomodont therapsids (Synapsida): Insights from X-ray computerized microtomography.

Anomodontia was the most successful herbivorous clade of the mammalian stem lineage (non-mammalian synapsids) during the late Permian and Early Triassic. Among anomodonts, Dicynodontia stands apart because of the presence of an osseous beak that shows evidence of the insertion of a cornified sheath, the ramphotheca. In this study, fourteen anomodont specimens were microCT-scanned and their trigeminal canals reconstructed digitally to understand the origin and evolution of trigeminal nerve innervation of the ramphotheca. We show that the pattern of innervation of the anomodont "beak" is more similar to that in chelonians (the nasopalatine branch is enlarged and innervates the premaxillary part of the ramphotheca) than in birds (where the nasopalatine and maxillary branches play minor roles). The nasopalatine branch is noticeably enlarged in the beak-less basal anomodont Patranomodon, suggesting that this could be an anomodont or chainosaur synapomorphy. Our analyses suggest that the presence or absence of tusks and postcanine teeth are often accompanied by corresponding variations of the rami innervating the caniniform process and the alveolar region, respectively. The degree of ossification of the canal for the nasal ramus of the ophthalmic branch also appears to correlate with the presence of a nasal boss. The nasopalatine canal is absent from the premaxilla in the Bidentalia as they uniquely show a large plexus formed by the internal nasal branch of the maxillary canal instead. The elongated shape of this plexus in Lystrosaurus supports the hypothesis that the rostrum evolved as an elongation of the subnarial region of the snout. Finally, the atrophied and variable aspect of the trigeminal canals in Myosaurus supports the hypothesis that this genus had a reduced upper ramphotheca.

Synchrotron scanning reveals the palaeoneurology of the head-butting Moschops capensis (Therapsida, Dinocephalia).

Dinocephalian therapsids are renowned for their massive, pachyostotic and ornamented skulls adapted for head-to-head fighting during intraspecific combat. Synchrotron scanning of the tapinocephalid Moschops capensis reveals, for the first time, numerous anatomical adaptations of the central nervous system related to this combative behaviour. Many neural structures (such as the brain, inner ear and ophthalmic branch of the trigeminal nerve) were completely enclosed and protected by bones, which is unusual for non-mammaliaform therapsids. The nearly complete ossification of the braincase enables precise determination of the brain cavity volume and encephalization quotient, which appears greater than expected for such a large and early herbivore. The practice of head butting is often associated with complex social behaviours and gregariousness in extant species, which are known to influence brain size evolution. Additionally, the plane of the lateral (horizontal) semicircular canal of the bony labyrinth is oriented nearly vertically if the skull is held horizontally, which suggests that the natural position of the head was inclined about 60-65°to the horizontal. This is consistent with the fighting position inferred from osteology, as well as ground-level browsing. Finally, the unusually large parietal tube may have been filled with thick conjunctive tissue to protect the delicate pineal eye from injury sustained during head butting.