How smart was T. rex? Testing claims of exceptional cognition in dinosaurs and the application of neuron count estimates in palaeontological research.

Recent years have seen increasing scientific interest in whether neuron counts can act as correlates of diverse biological phenomena. Lately, Herculano-Houzel (2023) argued that fossil endocasts and comparative neurological data from extant sauropsids allow to reconstruct telencephalic neuron counts in Mesozoic dinosaurs and pterosaurs, which might act as proxies for behaviors and life history traits in these animals. According to this analysis, large theropods such as Tyrannosaurus rex were long-lived, exceptionally intelligent animals equipped with "macaque- or baboon-like cognition", whereas sauropods and most ornithischian dinosaurs would have displayed significantly smaller brains and an ectothermic physiology. Besides challenging established views on Mesozoic dinosaur biology, these claims raise questions on whether neuron count estimates could benefit research on fossil animals in general. Here, we address these findings by revisiting Herculano-Houzel's (2023) work, identifying several crucial shortcomings regarding analysis and interpretation. We present revised estimates of encephalization and telencephalic neuron counts in dinosaurs, which we derive from phylogenetically informed modeling and an amended dataset of endocranial measurements. For large-bodied theropods in particular, we recover significantly lower neuron counts than previously proposed. Furthermore, we review the suitability of neurological variables such as neuron numbers and relative brain size to predict cognitive complexity, metabolic rate and life history traits in dinosaurs, coming to the conclusion that they are flawed proxies for these biological phenomena. Instead of relying on such neurological estimates when reconstructing Mesozoic dinosaur biology, we argue that integrative studies are needed to approach this complex subject.

The virtual brain endocast of Trogosus (Mammalia, Tillodontia) and its relevance in understanding the extinction of archaic placental mammals.

After successfully diversifying during the Paleocene, the descendants of the first wave of mammals that survived the end-Cretaceous mass extinction waned throughout the Eocene. Competition with modern crown clades and intense climate fluctuations may have been part of the factors leading to the extinction of these archaic groups. Why these taxa went extinct has rarely been studied from the perspective of the nervous system. Here, we describe the first virtual endocasts for the archaic order Tillodontia. Three species from the middle Eocene of North America were analyzed: Trogosus hillsii, Trogosus grangeri, and Trogosus castoridens. We made morphological comparisons with the plaster endocast of another tillodont, Tillodon fodiens, as well as groups potentially related to Tillodontia: Pantodonta, Arctocyonidae, and Cimolesta. Trogosus shows very little inter-specific variation with the only potential difference being related to the fusion of the optic canal and sphenorbital fissure. Many ancestral features are displayed by Trogosus, including an exposed midbrain, small neocortex, orbitotemporal canal ventral to rhinal fissure, and a broad circular fissure. Potential characteristics that could unite Tillodontia with Pantodonta, and Arctocyonidae are the posterior position of cranial nerve V3 exit in relation to the cerebrum and the low degree of development of the subarcuate fossa. The presence of large olfactory bulbs and a relatively small neocortex are consistent with a terrestrial lifestyle. A relatively small neocortex may have put Trogosus at risk when competing with artiodactyls for potentially similar resources and avoiding predation from archaic carnivorans, both of which are known to have had larger relative brain and neocortex sizes in the Eocene. These factors may have possibly exacerbated the extinction of Tillodontia, which showed highly specialized morphologies despite the increase in climate fluctuations throughout the Eocene, before disappearing during the middle Eocene.

Evolution of cortical geometry and its link to function, behaviour and ecology.

Studies in comparative neuroanatomy and of the fossil record demonstrate the influence of socio-ecological niches on the morphology of the cerebral cortex, but have led to oftentimes conflicting theories about its evolution. Here, we study the relationship between the shape of the cerebral cortex and the topography of its function. We establish a joint geometric representation of the cerebral cortices of ninety species of extant Euarchontoglires, including commonly used experimental model organisms. We show that variability in surface geometry relates to species' ecology and behaviour, independent of overall brain size. Notably, ancestral shape reconstruction of the cortical surface and its change during evolution enables us to trace the evolutionary history of localised cortical expansions, modal segregation of brain function, and their association to behaviour and cognition. We find that individual cortical regions follow different sequences of area increase during evolutionary adaptations to dynamic socio-ecological niches. Anatomical correlates of this sequence of events are still observable in extant species, and relate to their current behaviour and ecology. We decompose the deep evolutionary history of the shape of the human cortical surface into spatially and temporally conscribed components with highly interpretable functional associations, highlighting the importance of considering the evolutionary history of cortical regions when studying their anatomy and function.

Locomotor behavior and hearing sensitivity in an early lagomorph reconstructed from the bony labyrinth.

The structure of the bony labyrinth is highly informative with respect to locomotor agility (semicircular canals [SCC]) and hearing sensitivity (cochlear and oval windows). Here, we reconstructed the agility and hearing sensitivity of the stem lagomorph Megalagus turgidus from the early Oligocene of the Brule Formation of Nebraska (USA). Megalagus has proportionally smaller SCCs with respect to its body mass compared with most extant leporids but within the modern range of variability, suggesting that it was less agile than most of its modern relatives. A level of agility for Megalagus within the range of modern rabbits is consistent with the evidence from postcranial elements. The hearing sensitivity for Megalagus is in the range of extant lagomorphs for both low- and high-frequency sounds. Our data show that by the early Oligocene stem lagomorphs had already attained fundamentally rabbit-like hearing sensitivity and locomotor behavior, even though Megalagus was not a particularly agile lagomorph. This is likely because Megalagus was more of a woodland dweller than an open-habitat runner. The study of sensory evolution in Lagomorpha is practically unknown, and these results provide first advances in understanding the primitive stages for the order and how the earliest members of this clade perceived their environment.

Scaling patterns of cerebellar petrosal lobules in Euarchontoglires: Impacts of ecology and phylogeny.

The petrosal lobules (in whole or part homologous with the paraflocculi) of the cerebellum regulate functions associated with vision including smooth pursuit and velocity control of eye movements, suggesting a possible relationship between the petrosal lobules and behavioral adaptation. Previous studies have produced diverging conclusions regarding the lobules' ecological signal. The current study examines lobule scaling within an ecologically diverse but phylogenetically constrained sample of extant mammals to determine whether ecology influences relative petrosal lobule size. Using the endocasts of 140 Euarchontoglires (Primates, Scandentia, Dermoptera, Lagomorpha, Rodentia), petrosal lobule size was evaluated relative to endocranium and body size, accounting for phylogenetic relationships and ecology (locomotor behavior, diet, activity pattern). Results show a strong positive relationship between lobule size and both endocranial volume and body mass. Phylogeny is a major factor in the scaling of the petrosal lobules, with significant differences in relative size identified between orders and suborders. Concerning ecology, fossorial taxa were found to have significantly smaller petrosal lobules relative to body mass compared to other locomotor groups across Euarchontoglires. The small lobules possessed by this group may reflect an adaptation related to reduced visual reliance. In contrast to previous research, no relationship was identified between relative lobule size and any other ecological variables. While variation in relative lobule size may be adaptively significant in some groups (i.e., fossorial species), it is critical to study the evolution of petrosal lobule size within a narrow phylogenetic scope, with inclusion of fossil material to inform our understanding of evolutionary trajectories.

Brawn before brains in placental mammals after the end-Cretaceous extinction.

Mammals are the most encephalized vertebrates, with the largest brains relative to body size. Placental mammals have particularly enlarged brains, with expanded neocortices for sensory integration, the origins of which are unclear. We used computed tomography scans of newly discovered Paleocene fossils to show that contrary to the convention that mammal brains have steadily enlarged over time, early placentals initially decreased their relative brain sizes because body mass increased at a faster rate. Later in the Eocene, multiple crown lineages independently acquired highly encephalized brains through marked growth in sensory regions. We argue that the placental radiation initially emphasized increases in body size as extinction survivors filled vacant niches. Brains eventually became larger as ecosystems saturated and competition intensified.

Petrosal Anatomy of the Paleocene Eutherian Mammal Deltatherium fundaminis (Cope, 1881).

We describe the tympanic anatomy of the petrosal of Deltatherium fundaminis, an enigmatic Paleocene mammal based on cranial specimens recovered from New Mexico, U.S.A. Although the ear region of Deltatherium has previously been described, there has not been a comprehensive, well-illustrated contribution using current anatomical terminology. The dental and cranial anatomy of Deltatherium is a chimera, with morphological similarities to both 'condylarth' and 'cimolestan' taxa. As such, the phylogenetic relationships of this taxon have remained elusive since its discovery, and it has variably been associated with Arctocyonidae, Pantodonta and Tillodontia. The petrosal of Deltatherium is anteriorly bordered by an open space comprising a contiguous carotid opening and pyriform fenestra. The promontorium features both a small rostral tympanic process and small epitympanic wing but lacks well-marked sulci. A large ventral facing external aperture of the canaliculus cochleae is present and bordered posteriorly by a well-developed caudal tympanic process. The hiatus Fallopii opens on the ventral surface of the petrosal. The tegmen tympani is mediolaterally broad and anteriorly expanded, and its anterior margin is perforated by a foramen for the ramus superior of the stapedial artery. The tympanohyal is small but approximates the caudal tympanic process to nearly enclose the stylomastoid notch. The mastoid is widely exposed on the basicranium and bears an enlarged mastoid process, separate from the paraoccipital process. These new observations provide novel anatomical data corroborating previous hypotheses regarding the plesiomorphic eutherian condition but also reveal subtle differences among Paleocene eutherians that have the potential to help inform the phylogeny of Deltatherium. Supplementary Information: The online version contains supplementary material available at 10.1007/s10914-021-09568-3.

Divergence-time estimates for hominins provide insight into encephalization and body mass trends in human evolution.

Quantifying speciation times during human evolution is fundamental as it provides a timescale to test for the correlation between key evolutionary transitions and extrinsic factors such as climatic or environmental change. Here, we applied a total evidence dating approach to a hominin phylogeny to estimate divergence times under different topological hypotheses. The time-scaled phylogenies were subsequently used to perform ancestral state reconstructions of body mass and phylogenetic encephalization quotient (PEQ). Our divergence-time estimates are consistent with other recent studies that analysed extant species. We show that the origin of the genus Homo probably occurred between 4.30 and 2.56 million years ago. The ancestral state reconstructions show a general trend towards a smaller body mass before the emergence of Homo, followed by a trend towards a greater body mass. PEQ estimations display a general trend of gradual but accelerating encephalization evolution. The obtained results provide a rigorous temporal framework for human evolution.

The impact of locomotion on the brain evolution of squirrels and close relatives.

How do brain size and proportions relate to ecology and evolutionary history? Here, we use virtual endocasts from 38 extinct and extant rodent species spanning 50+ million years of evolution to assess the impact of locomotion, body mass, and phylogeny on the size of the brain, olfactory bulbs, petrosal lobules, and neocortex. We find that body mass and phylogeny are highly correlated with relative brain and brain component size, and that locomotion strongly influences brain, petrosal lobule, and neocortical sizes. Notably, species living in trees have greater relative overall brain, petrosal lobule, and neocortical sizes compared to other locomotor categories, especially fossorial taxa. Across millions of years of Eocene-Recent environmental change, arboreality played a major role in the early evolution of squirrels and closely related aplodontiids, promoting the expansion of the neocortex and petrosal lobules. Fossoriality in aplodontiids had an opposing effect by reducing the need for large brains.

Evolution of arboreality and fossoriality in squirrels and aplodontid rodents: Insights from the semicircular canals of fossil rodents.

Reconstructing locomotor behaviour for fossil animals is typically done with postcranial elements. However, for species only known from cranial material, locomotor behaviour is difficult to reconstruct. The semicircular canals (SCCs) in the inner ear provide insight into an animal's locomotor agility. A relationship exists between the size of the SCCs relative to body mass and the jerkiness of an animal's locomotion. Additionally, studies have also demonstrated a relationship between SCC orthogonality and angular head velocity. Here, we employ two metrics for reconstructing locomotor agility, radius of curvature dimensions and SCC orthogonality, in a sample of twelve fossil rodents from the families Ischyromyidae, Sciuridae and Aplodontidae. The method utilizing radius of curvature dimensions provided a reconstruction of fossil rodent locomotor behaviour that is more consistent with previous studies assessing fossil rodent locomotor behaviour compared to the method based on SCC orthogonality. Previous work on ischyromyids suggests that this group displayed a variety of locomotor modes. Members of Paramyinae and Ischyromyinae have relatively smaller SCCs and are reconstructed to be relatively slower compared to members of Reithroparamyinae. Early members of the Sciuroidea clade including the sciurid Cedromus wilsoni and the aplodontid Prosciurus relictus are reconstructed to be more agile than ischyromyids, in the range of extant arboreal squirrels. This reconstruction supports previous inferences that arboreality was likely an ancestral trait for this group. Derived members of Sciuridae and Aplodontidae vary in agility scores. The fossil squirrel Protosciurus cf. rachelae is inferred from postcranial material as arboreal, which is in agreement with its high agility, in the range of extant arboreal squirrels. In contrast, the fossil aplodontid Mesogaulus paniensis has a relatively low agility score, similar to the fossorial Aplodontia rufa, the only living aplodontid rodent. This result is in agreement with its postcranial reconstruction as fossorial and with previous indications that early aplodontids were more arboreal than their burrowing descendants.

Cranial endocast of the stem lagomorph Megalagus and brain structure of basal Euarchontoglires.

Early lagomorphs are central to our understanding of how the brain evolved in Glires (rodents, lagomorphs and their kin) from basal members of Euarchontoglires (Glires + Euarchonta, the latter grouping primates, treeshrews, and colugos). Here, we report the first virtual endocast of the fossil lagomorph Megalagus turgidus, from the Orella Member of the Brule Formation, early Oligocene, Nebraska, USA. The specimen represents one of the oldest nearly complete lagomorph skulls known. Primitive aspects of the endocranial morphology in Megalagus include large olfactory bulbs, exposure of the midbrain, a small neocortex and a relatively low encephalization quotient. Overall, this suggests a brain morphology closer to that of other basal members of Euarchontoglires (e.g. plesiadapiforms and ischyromyid rodents) than to that of living lagomorphs. However, the well-developed petrosal lobules in Megalagus, comparable to the condition in modern lagomorphs, suggest early specialization in that order for the stabilization of eye movements necessary for accurate visual tracking. Our study sheds new light on the reconstructed morphology of the ancestral brain in Euarchontoglires and fills a critical gap in the understanding of palaeoneuroanatomy of this major group of placental mammals.

Virtual endocranial and inner ear endocasts of the Paleocene 'condylarth' Chriacus: new insight into the neurosensory system and evolution of early placental mammals.

The end-Cretaceous mass extinction allowed placental mammals to diversify ecologically and taxonomically as they filled ecological niches once occupied by non-avian dinosaurs and more basal mammals. Little is known, however, about how the neurosensory systems of mammals changed after the extinction, and what role these systems played in mammalian diversification. We here use high-resolution computed tomography (CT) scanning to describe the endocranial and inner ear endocasts of two species, Chriacus pelvidens and Chriacus baldwini, which belong to a cluster of 'archaic' placental mammals called 'arctocyonid condylarths' that thrived during the ca. 10 million years after the extinction (the Paleocene Epoch), but whose relationships to extant placentals are poorly understood. The endocasts provide new insight into the paleobiology of the long-mysterious 'arctocyonids', and suggest that Chriacus was an animal with an encephalization quotient (EQ) range of 0.12-0.41, which probably relied more on its sense of smell than vision, because the olfactory bulbs are proportionally large but the neocortex and petrosal lobules are less developed. Agility scores, estimated from the dimensions of the semicircular canals of the inner ear, indicate that Chriacus was slow to moderately agile, and its hearing capabilities, estimated from cochlear dimensions, suggest similarities with the extant aardvark. Chriacus shares many brain features with other Paleocene mammals, such as a small lissencephalic brain, large olfactory bulbs and small petrosal lobules, which are likely plesiomorphic for Placentalia. The inner ear of Chriacus also shares derived characteristics of the elliptical and spherical recesses with extinct species that belong to Euungulata, the extant placental group that includes artiodactyls and perissodactyls. This lends key evidence to the hypothesized close relationship between Chriacus and the extant ungulate groups, and demonstrates that neurosensory features can provide important insight into both the paleobiology and relationships of early placental mammals.

Virtual endocast of the early Oligocene Cedromus wilsoni (Cedromurinae) and brain evolution in squirrels.

Extant squirrels exhibit extensive variation in brain size and shape, but published endocranial data for living squirrels are limited, and no study has ever examined brain evolution in Sciuridae from the perspective of the fossil record to understand how this diversity emerged. We describe the first virtual endocast for a fossil sciurid, Cedromus wilsoni, which is known from a complete cranium from Wyoming (Orellan, Oligocene), and make comparisons to a diverse sample of virtual endocasts for living sciurids (N = 20). The virtual endocasts were obtained from high-resolution X-ray micro-computed tomography data. Comparisons were also made with endocasts of extinct ischyromyid rodents, the most primitive rodents known from an endocranial record, which provide the opportunity to study the neuroanatomical changes occurring near the base of Sciuridae. The encephalization quotient of C. wilsoni is higher than that of Ischyromys typus from the same epoch, and falls within the range of modern terrestrial squirrel variation, but below the range of extant scansorial, arboreal and gliding sciurids when using cheek-tooth area for the estimation of body mass. In a principal components analysis, the shape of the endocast of C. wilsoni is found to be intermediate between that of primitive fossil taxa and the modern sample. Cedromus wilsoni has a more expanded neocortical surface area, especially the caudal region of the cerebrum, compared with ischyromyid rodents. Furthermore, C. wilsoni had proportionally larger paraflocculi and a more complex cerebellar morphology compared with ischyromyid rodents. These neurological differences may be associated with improvements in vision, although it is worth noting that the size of the parts of the brain most directly involved with vision [the rostral (superior) colliculi and the primary visual cortex] cannot be directly assessed on endocasts. The changes observed could also relate to balance and limb coordination. Ultimately, the available evidence suggests that early squirrels were more agile and visually oriented animals compared with more primitive rodents, which may relate to the process of becoming arboreal. Extant sciurids have an even more expanded neocortical surface area, while exhibiting proportionally smaller paraflocculi, compared with C. wilsoni. This suggests that the neocortex may continue increasing in size in more recent sciurid rodents in relation to other factors than arboreality. Despite the fact that both Primates and Rodentia exhibit neocortical expansion through time, since the adoption of arboreality preceded major increases in the neocortex in Primates, those neurological changes may be related to different ecological factors, underlining the complexity of the inter-relationship between time and ecology in shaping the brain in even closely related clades.

Virtual endocasts of Eocene Paramys (Paramyinae): oldest endocranial record for Rodentia and early brain evolution in Euarchontoglires.

Understanding the pattern of brain evolution in early rodents is central to reconstructing the ancestral condition for Glires, and for other members of Euarchontoglires including Primates. We describe the oldest virtual endocasts known for fossil rodents, which pertain to Paramys copei (Early Eocene) and Paramys delicatus (Middle Eocene). Both specimens of Paramys have larger olfactory bulbs and smaller paraflocculi relative to total endocranial volume than later occurring rodents, which may be primitive traits for Rodentia. The encephalization quotients (EQs) of Pa. copei and Pa. delicatus are higher than that of later occurring (Oligocene) Ischyromys typus, which contradicts the hypothesis that EQ increases through time in all mammalian orders. However, both species of Paramys have a lower relative neocortical surface area than later rodents, suggesting neocorticalization occurred through time in this Order, although to a lesser degree than in Primates. Paramys has a higher EQ but a lower neocortical ratio than any stem primate. This result contrasts with the idea that primates were always exceptional in their degree of overall encephalization and shows that relative brain size and neocortical surface area do not necessarily covary through time. As such, these data contradict assumptions made about the pattern of brain evolution in Euarchontoglires.