The cranium of Proviverra typica (Mammalia,Hyaenodonta) and its impact on hyaenodont phylogeny and endocranial evolution

We describe the first endocast reconstruction of a hyaenodont mammal based on X‐ray microtomography. The endocast belongs to the type material of the European hyaenodont Proviverra typica. We performed phylogenetic analysis to contextualize the evolution of endocranial size and complexity in Hyaenodonta. We added several European hyaenodonts and modified several codings of the most recent character–taxon matrix established to question the relationships within Hyaenodonta. Including these new species in a phylogenetic analysis reveals a new clade: Hyaenodontoidea. Comparisons with several previously described endocasts show that there was an increase in complexity in the convolutions of the encephalon within Hyaenodontidae history. Moreover, the analysis of the encephalization quotient reveals that the endocranium of the Hyaenodonta is not smaller than those of fossil Carnivora or some extant Carnivora. Therefore, the extinction of Hyaenodonta may not be linked to the relative size of hyaenodont brains.     

Virtual brain endocast of Antifer (Mammalia: Cervidae), an extinct large cervid from South America

A diverse fossil record of Cervidae (Mammalia) has been documented in the South American Pleistocene, when these animals arrived during the Great American Biotic Interchange. Using computed tomography-scanning techniques, it is possible to access the endocranial morphology of extinct species. Here, we studied the brain endocast of the extinct late Pleistocene cervid Antifer ensenadensis from southern Brazil, one of the largest forms that lived on this continent, using comparative morphology, geometric morphometrics, and encephalization quotients. The analyzed endocasts demonstrate that A. ensenadensis had a gyrencephalic brain, showing a prominent longitudinal sinus (=sagittal superior sinus), which is also observed in the large South American cervid Blastocerus dichotomus. The encephalization quotient is within the variation of extant cervids, suggesting maintenance of the pattern of encephalization from at least the late Pleistocene. Geometric morphometric analysis suggested a clear and linear allometric trend between brain endocast size and shape, and highlights A. ensenadensis as an extreme form within the analyzed cervids regarding brain morphology.     

Ancestral state reconstruction of body size in the Caniformia (Carnivora, Mammalia): the effects of incorporating data from the fossil record

A recent molecular phylogeny of the mammalian order Carnivora implied large body size as the ancestral condition for the caniform subclade Arctoidea using the distribution of species mean body sizes among living taxa. "Extant taxa-only" approaches such as these discount character state observations for fossil members of living clades and completely ignore data from extinct lineages. To more rigorously reconstruct body sizes of ancestral forms within the Caniformia, body size and first appearance data were collected for 149 extant and 367 extinct taxa. Body sizes were reconstructed for four ancestral nodes using weighted squared-change parsimony on log-transformed body mass data. Reconstructions based on extant taxa alone favored large body sizes (on the order of 10 to 50 kg) for the last common ancestors of both the Caniformia and Arctoidea. In contrast, reconstructions incorporating fossil data support small body sizes (< 5 kg) for the ancestors of those clades. When the temporal information associated with fossil data was discarded, body size reconstructions became ambiguous, demonstrating that incorporating both character state and temporal information from fossil taxa unambiguously supports a small ancestral body size, thereby falsifying hypotheses derived from extant taxa alone. Body size reconstructions for Caniformia, Arctoidea, and Musteloidea were not sensitive to potential errors introduced by uncertainty in the position of extinct lineages relative to the molecular topology, or to missing body size data for extinct members of an entire major clade (the aquatic Pinnipedia). Incorporating character state observations and temporal information from the fossil record into hypothesis testing has a significant impact on the ability to reconstruct ancestral characters and constrains the range of potential hypotheses of character evolution. Fossil data here provide the evidence to reliably document trends of both increasing and decreasing body size in several caniform clades. More generally, including fossils in such analyses incorporates evidence of directional trends, thereby yielding more reliable ancestral character state reconstructions.     

Anatomy of the Cranial Endocast of the Bottlenose Dolphin, Tursiops truncatus, Based on HRXCT

Endocranial surfaces, volumes, and interconnectivities of extant and fossil odontocetes potentially offer information on the general architecture of the brain and on the structure of the specialized cetacean circulatory system. Although conventional methods for acquiring such data have generally involved invasive preparation of the specimen, particularly in the case of fossils, new tomographic technologies afford nondestructive access to these internal morphologies. In this study we used high-resolution X-ray computed tomography (HRXCT) to scan a skull of the extant Tursiops truncatus (Cetacea: Odontoceti). We processed the data to reveal the cranial endocast and details of internal skeletal architecture (data at www.digimorph.org). Major features that can be discerned include aspects of the specimen's hypertrophied retia mirabilia, the major canals and openings of the cranial cavity, and the relationship of the brain and endocranial circulatory structures to the surrounding skeleton. CT data also provide information on the shape of the brain that may be lost in conventional anatomical preparations, and readily provide volumetric and linear measurements of the endocast and its individual segments. These results demonstrate the utility of HRXCT for interpreting the internal cranial anatomy of both extant and fossil cetaceans.     

A Total Evidence Phylogeny of the Arctoidea (Carnivora: Mammalia): Relationships Among Basal Taxa

A total evidence phylogenetic analysis was performed for 14 extant and 18 fossil caniform genera using a data matrix of 5.6 kbp of concatenated sequence data from six independent loci and 80 morphological characters from the cranium and dentition. Maximum parsimony analysis recovered a single most parsimonious cladogram (MPC). The topology of the extant taxa in the MPC agreed with previous molecular phylogenies. Phylogenetic positions for fossil taxa indicate that several taxa previously described as early members of extant families (e.g., Bathygale and Plesictis) are likely stem taxa at the base of the Arctoidea. Taxa in the “Paleomustelidae” were found to be paraphyletic, but a monophyletic Oligobuninae was recovered within this set of taxa. This clade was closely related to the extant genera Gulo and Martes, therefore, nested within the extant radiation of the family Mustelidae. This analysis provides a resolution to several discrepancies between phylogenies considering either fossil taxa or extant taxa separately, and provides a framework for incorporating fossil and extant taxa into comprehensive combined evidence analyses.     

Does encephalization correlate with life history or metabolic rate in Carnivora?

A recent analysis of brain size evolution reconstructed the plesiomorphic brain–body size allometry for the mammalian order Carnivora, providing an important reference frame for comparative analyses of encephalization (brain volume scaled to body mass). I performed phylogenetically corrected regressions to remove the effects of body mass, calculating correlations between residual values of encephalization with basal metabolic rate (BMR) and six life-history variables (gestation time, neonatal mass, weaning time, weaning mass, litter size, litters per year). No significant correlations were recovered between encephalization and any life-history variable or BMR, arguing against hypotheses relating encephalization to maternal energetic investment. However, after correcting for clade-specific adaptations, I recovered significant correlations for several variables, and further analysis revealed a conserved carnivoran reproductive strategy, linking degree of encephalization to the well-documented mammalian life-history trade-off between neonatal mass and litter size. This strategy of fewer, larger offspring correlating with increased encephalization remains intact even after independent changes in encephalization allometries in the evolutionary history of this clade.     

Endocranial capacity of the bodo cranium determined from three-dimensional computed tomography

The 600,000-year-old cranium from Bodo, Ethiopia, is the oldest and most complete early Middle Pleistocene hominid skull from Africa. "Virtual endocast" models created by three-dimensional computed tomography (CT) techniques indicate an endocranial capacity of about 1,250 cc for this cranium (with a reasonable range between approximately 1,200-1,325 cc, depending on how missing portions of the basicranial region are reconstructed). From these determinations, several important implications emerge concerning current interpretations of "tempo and mode" in early hominid brain evolution: 1) already by the early Middle Pleistocene, at least one African hominid species, Homo heidelbergensis, had reached an endocranial capacity within the normal range of modern humans; 2) in spite of its large endocranial capacity, estimates of Bodo's encephalization quotient fall below those found in a large sample of Homo sapiens (both fossil and recent) and Neandertals; and 3) the greatest burst of brain expansion in the Homo lineage may not have been in the last several hundred thousand years, but rather much earlier in the Lower to early Middle Pleistocene.     

Visual influences on primate encephalization

Primates differ from most other mammals in having relatively large brains. As a result, numerous comparative studies have attempted to identify the selective variables influencing primate encephalization. However, none have examined the effect of the total amount of visual input on relative brain size. According to Jerison's principle of proper mass, functional areas of the brain devoted primarily to processing visual information should exhibit increases in size when the amount of visual input to those areas increases. As a result, the total amount of visual input to the brain could exert a large influence on encephalization because visual areas comprise a large proportion of total brain mass in primates. The goal of this analysis is to test the expectation of a direct relationship between visual input and encephalization using optic foramen size and optic nerve size as proxies for total visual input. Data were collected for a large comparative sample of primates and carnivorans, and three primary analyses were undertaken. First, the relationship between relative proxies for visual input and relative endocranial volume were examined using partial correlations and phylogenetic comparative methods. Second, to examine the generality of the results derived for extant primates, a parallel series of partial correlation and comparative analyses were undertaken using data for carnivorans. Third, data for various Eocene and Oligocene primates were compared with those for living primates in order to determine whether the fossil taxa demonstrate a similar relationship between relative brain size and visual input. All three analyses confirm the expectations of proper mass and favor the conclusion that the amount of visual input has been a major influence on the evolution of relative brain size in both primates and carnivorans. Furthermore, this study suggests that differences in visual input may partly explain (1) the high encephalization of primates relative to the primitive eutherian condition, (2) the high encephalization of extant anthropoids relative to other primates, and (3) the very low encephalization of Eocene adapiforms.     

Assessing endocranial variations in great apes and humans using 3D data from virtual endocasts

Modern humans are characterized by their large, complex, and specialized brain. Human brain evolution can be addressed through direct evidence provided by fossil hominid endocasts (i.e. paleoneurology), or through indirect evidence of extant species comparative neurology. Here we use the second approach, providing an extant comparative framework for hominid paleoneurological studies. We explore endocranial size and shape differences among great apes and humans, as well as between sexes. We virtually extracted 72 endocasts, sampling all extant great ape species and modern humans, and digitized 37 landmarks on each for 3D generalized Procrustes analysis. All species can be differentiated by their endocranial shape. Among great apes, endocranial shapes vary from short (orangutans) to long (gorillas), perhaps in relation to different facial orientations. Endocranial shape differences among African apes are partly allometric. Major endocranial traits distinguishing humans from great apes are endocranial globularity, reflecting neurological reorganization, and features linked to structural responses to posture and bipedal locomotion. Human endocasts are also characterized by posterior location of foramina rotunda relative to optic canals, which could be correlated to lesser subnasal prognathism compared to living great apes. Species with larger brains (gorillas and humans) display greater sexual dimorphism in endocranial size, while sexual dimorphism in endocranial shape is restricted to gorillas, differences between males and females being at least partly due to allometry. Our study of endocranial variations in extant great apes and humans provides a new comparative dataset for studies of fossil hominid endocasts.     

Endocranial Anatomy of the Charadriiformes: Sensory System Variation and the Evolution of Wing-Propelled Diving

Just as skeletal characteristics provide clues regarding behavior of extinct vertebrates, phylogenetically-informed evaluation of endocranial morphology facilitates comparisons among extinct taxa and extant taxa with known behavioral characteristics. Previous research has established that endocranial morphology varies across Aves; however, variation of those systems among closely related species remains largely unexplored. The Charadriiformes (shorebirds and allies) are an ecologically diverse clade with a comparatively rich fossil record, and therefore, are well suited for investigating interspecies variation, and potential links between endocranial morphology, phylogeny, ecology and other life history attributes. Endocranial endocasts were rendered from high resolution X-ray computed tomography data for 17 charadriiforms (15 extant and two flightless extinct species). Evaluation of endocranial character state changes on a phylogeny for Charadriiformes resulted in identification of characters that vary in taxa with distinct feeding and locomotor ecologies. In comparison with all other charadriiforms, stem and crown clade wing-propelled diving Pan-Alcidae displayed compressed semicircular canals, and indistinct occipital sinuses and cerebellar fissures. Flightless wing-propelled divers have relatively smaller brains for their body mass and smaller optic lobes than volant pan-alcids. Observed differences between volant and flightless wing-propelled sister taxa are striking given that flightless pan-alcids continue to rely on the flight stroke for underwater propulsion. Additionally, the brain of the Black Skimmer Rynchops niger, a taxon with a unique feeding ecology that involves continuous forward aerial motion and touch-based prey detection used both at day and night, is discovered to be unlike that of any other sampled charadriiform in having an extremely large wulst as well as a small optic lobe and distinct occipital sinus. Notably, the differences between the Black Skimmer and other charadriiforms are more pronounced than between wing-propelled divers and other charadriiforms. Finally, aspects of endosseous labyrinth morphology are remarkably similar between divers and non-divers, and may deserve further evaluation.     

The endocast from Dana Aoule North (DAN5/P1): A 1.5 million year-old human braincase from Gona,Afar, Ethiopia

The nearly complete cranium DAN5/P1 was found at Gona (Afar, Ethiopia), dated to 1.5–1.6 Ma, and assigned to the species Homo erectus. Its size is, nonetheless, particularly small for the known range of variation of this taxon, and the cranial capacity has been estimated as 598 cc. In this study, we analyzed a reconstruction of its endocranial cast, to investigate its paleoneurological features. The main anatomical traits of the endocast were described, and its morphology was compared with other fossil and modern human samples. The endocast shows most of the traits associated with less encephalized human taxa, like narrow frontal lobes and a simple meningeal vascular network with posterior parietal branches. The parietal region is relatively tall and rounded, although not especially large. Based on our set of measures, the general endocranial proportions are within the range of fossils included in the species Homo habilis or in the genus Australopithecus. Similarities with the genus Homo include a more posterior position of the frontal lobe relative to the cranial bones, and the general endocranial length and width when size is taken into account. This new specimen extends the known brain size variability of Homo ergaster/erectus, while suggesting that differences in gross brain proportions among early human species, or even between early humans and australopiths, were absent or subtle.     

Morphology and postnatal ontogeny of the cranial endocast and paranasal sinuses of capybara (Hydrochoerus hydrochaeris), the largest living rodent

Recent studies have analyzed and described the endocranial cavities of caviomorph rodents. However, no study has documented the changes in the morphology and relative size of such cavities during ontogeny. Expecting to contribute to the discussion of the endocranial spaces of extinct caviomorphs, we aimed to characterize the cranial endocast morphology and paranasal sinuses of the largest living rodent, Hydrochoerus hydrochaeris, by focusing on its ontogenetic growth patterns. We analyzed 12 specimens of different ontogenetic stages and provided a comparison with other cavioids. Our study demonstrates that the adult cranial endocast of H. hydrochaeris is characterized by olfactory bulbs with an irregular shape, showing an elongated olfactory tract without a clear circular fissure, a marked temporal region that makes the endocast with rhombus outline, and gyrencephaly. Some of these traits change as the brain grows. The cranial pneumatization is present in the frontal and lacrimal bones. We identified two recesses (frontal and lacrimal) and one sinus (frontal). These pneumatic cavities increase their volume as the cranium grows, covering the cranial region of the cranial endocast. The encephalization quotient was calculated for each specimen, demonstrating that it decreases as the individual grows, being much higher in younger specimens than in adults. Our results show that the ontogenetic stage can be a confounding factor when it comes to the general patterns of encephalization of extinct rodents, reinforcing the need for paleobiologists to take the age of the specimens into account in future studies on this subject to avoid age-related biases.     

INTEGRATING FOSSILS WITH MOLECULAR PHYLOGENIES IMPROVES INFERENCE OF TRAIT EVOLUTION

Comparative biologists often attempt to draw inferences about tempo and mode in evolution by comparing the fit of evolutionary models to phylogenetic comparative data consisting of a molecular phylogeny with branch lengths and trait measurements from extant taxa. These kinds of approaches ignore historical evidence for evolutionary pattern and process contained in the fossil record. In this article, we show through simulation that incorporation of fossil information dramatically improves our ability to distinguish among models of quantitative trait evolution using comparative data. We further suggest a novel Bayesian approach that allows fossil information to be integrated even when explicit phylogenetic hypotheses are lacking for extinct representatives of extant clades. By applying this approach to a comparative dataset comprising body sizes for caniform carnivorans, we show that incorporation of fossil information not only improves ancestral state estimates relative to those derived from extant taxa alone, but also results in preference of a model of evolution with trend toward large body size over alternative models such as Brownian motion or Ornstein–Uhlenbeck processes. Our approach highlights the importance of considering fossil information when making macroevolutionary inference, and provides a way to integrate the kind of sparse fossil information that is available to most evolutionary biologists.     

Virtual reconstruction of cranial endocasts of traversodontid cynodonts (Eucynodontia: Gomphodontia) from the upper Triassic of Southern Brazil

The brain endocasts of the late Triassic (Carnian) traversodontids (Eucynodontia: Gomphodontia) Siriusgnathus niemeyerorum and Exaeretodon riograndensis from southern Brazil are described based on virtual models generated using computed tomography scan data. Their skull anatomy resembles that of other non-mammaliaform cynodonts, showing an endocranial cavity that is not fully ossified. A “V-shaped” orbitosphenoid, neither fully developed nor ossified is present in E. riograndensis. The nasal cavity is confluent with the encephalic cavity. Thus, the anterior limit of the olfactory bulbs is not definite. The brain endocast is elongated, being narrow anteriorly and wide posteriorly, with the maximum width at the parafloccular cast. The olfactory bulbs do not present a clear division between their counterparts, due to the absence of a longitudinal sulcus. A longitudinal sulcus in the forebrain delimiting the cerebral hemispheres, the pineal tube, and the parietal foramen are absent in both taxa. The large and well-developed unossified zone is partially separated from the remaining endocast by a notch formed by the supraoccipital. The encephalization quotients, as well as the endocranial volume/body mass relationships of S. niemeyerorum and E. riograndensis are within the range expected for non-mammaliaform Therapsida.     

Human encephalization and developmental timing

Human evolution is frequently analyzed in the light of changes in developmental timing. Encephalization in particular has been frequently linked to the slow pace of development in Homo sapiens. The "brain allometry extension" theory postulates that the progressive extension of a conserved primate brain allometry into postnatal life was the basis for brain enlargement in the human lineage. This study shows that published primate and human growth data do not corroborate this model. Instead, the unique encephalization of H. sapiens is alternatively described as the result of evolutionary changes in three aspects of developmental timing. The first is a moderate extension in the duration of brain growth relative to our closest extant relatives, contrary to the view that human brain growth is drastically prolonged into postnatal life. Second, humans evolved a derived brain allometry in comparison with chimpanzees and early hominins. Third, humans (and other anthropoid primates to a lesser degree) display a significant retardation in early postnatal body growth in comparison with other mammals, which directly affects adult encephalization in our species. The rejection of the "brain allometry extension" model may require a reevaluation of the adaptive scenarios proposed to explain how human encephalization evolved.     

POTENTIAL PITFALLS OF RECONSTRUCTING DEEP TIME EVOLUTIONARY HISTORY WITH ONLY EXTANT DATA,A CASE STUDY USING THE CANIDAE (MAMMALIA,CARNIVORA)

Reconstructing evolutionary patterns and their underlying processes is a central goal in biology. Yet many analyses of deep evolutionary histories assume that data from the fossil record is too incomplete to include, and rely solely on databases of extant taxa. Excluding fossil taxa assumes that character state distributions across living taxa are faithful representations of a clade's entire evolutionary history. Many factors can make this assumption problematic. Fossil taxa do not simply lead‐up to extant taxa; they represent now‐extinct lineages that can substantially impact interpretations of character evolution for extant groups. Here, we analyze body mass data for extant and fossil canids (dogs, foxes, and relatives) for changes in mean and variance through time. AIC‐based model selection recovered distinct models for each of eight canid subgroups. We compared model fit of parameter estimates for (1) extant data alone and (2) extant and fossil data, demonstrating that the latter performs significantly better. Moreover, extant‐only analyses result in unrealistically low estimates of ancestral mass. Although fossil data are not always available, reconstructions of deep‐time organismal evolution in the absence of deep‐time data can be highly inaccurate, and we argue that every effort should be made to include fossil data in macroevolutionary studies.     

Re-evaluation of the endocranial volume of the Guattari 1 Neandertal specimen (Monte Circeo)

The endocranial capacity of Guattari 1 originally was estimated by Sergi as approximately 1.550 cm3. Using three different approaches, a physical endocast, a stereolithographic model, and a virtual endocast, we have estimated the endocranial capacity of Guattari 1 as approximately 1.350 cm3. This paper explains our revision of the estimated endocranial volume of Guattari 1, provides a cautionary case concerning other estimates of endocranial volume, and demonstrates and encourages the use of recent advances in imaging, modeling, and analysis of endocranial volume.     

Cranial endocast of Anagale gobiensis (Anagalidae) and its implications for early brain evolution in Euarchontoglires

Anagalids are an extinct group of primitive mammals from the Asian Palaeogene thought to be possible basal members of Glires. Anagalid material is rare, with only a handful of crania known. Here we describe the first virtual endocast of an anagalid, based on the holotype of Anagale gobiensis (AMNH 26079; late Eocene, China), which allows for comparison with published endocasts from fossil members of modern euarchontogliran lineages (i.e. primates, rodents, lagomorphs). The endocast displays traits often observed in fossorial mammals, such as relatively small petrosal lobules and a low neocortical ratio, which would be consistent with previous inferences about use of subterranean food sources based on heavy dental wear. In fact, Anagale gobiensis has the lowest neocortical ratio yet recorded for a euarchontogliran. This species was olfaction-driven, based on the relatively large olfactory bulbs and laterally expansive palaeocortex. The endocast supports previous inferences that relatively large olfactory bulbs, partial midbrain exposure and low encephalization quotient are ancestral for Euarchontoglires, although the likely fossorial adaptations of Anagale gobiensis may also partly explain these traits. While Anagale gobiensis is a primitive mammal in many aspects, some of its derived endocranial traits point towards a new, different trajectory of brain evolution within Euarchontoglires.     

Dietary quality and encephalization in platyrrhine primates

The high energetic costs of building and maintaining large brains are thought to constrain encephalization. The 'expensive-tissue hypothesis' (ETH) proposes that primates (especially humans) overcame this constraint through reduction of another metabolically expensive tissue, the gastrointestinal tract. Small guts characterize animals specializing on easily digestible diets. Thus, the hypothesis may be tested via the relationship between brain size and diet quality. Platyrrhine primates present an interesting test case, as they are more variably encephalized than other extant primate clades (excluding Hominoidea). We find a high degree of phylogenetic signal in the data for diet quality, endocranial volume and body size. Controlling for phylogenetic effects, we find no significant correlation between relative diet quality and relative endocranial volume. Thus, diet quality fails to account for differences in platyrrhine encephalization. One taxon, in particular, Brachyteles, violates predictions made by ETH in having a large brain and low-quality diet. Dietary reconstructions of stem platyrrhines further indicate that a relatively high-quality diet was probably in place prior to increases in encephalization. Therefore, it is unlikely that a shift in diet quality was a primary constraint release for encephalization in platyrrhines and, by extrapolation, humans.     

Comparative analysis of encephalization in mammals reveals relaxed constraints on anthropoid primate and cetacean brain scaling

There is a well-established allometric relationship between brain and body mass in mammals. Deviation of relatively increased brain size from this pattern appears to coincide with enhanced cognitive abilities. To examine whether there is a phylogenetic structure to such episodes of changes in encephalization across mammals, we used phylogenetic techniques to analyse brain mass, body mass and encephalization quotient (EQ) among 630 extant mammalian species. Among all mammals, anthropoid primates and odontocete cetaceans have significantly greater variance in EQ, suggesting that evolutionary constraints that result in a strict correlation between brain and body mass have independently become relaxed. Moreover, ancestral state reconstructions of absolute brain mass, body mass and EQ revealed patterns of increase and decrease in EQ within anthropoid primates and cetaceans. We propose both neutral drift and selective factors may have played a role in the evolution of brain-body allometry.