Thomas E. Macrini

Fossil Evidence on Origin of the Mammalian Brain

Evidence from two early fossils suggests that brain enlargement and specialization proceeded in three pulses. Many hypotheses have been postulated regarding the early evolution of the mammalian brain. Here, x-ray tomography of the Early Jurassic mammaliaforms Morganucodon and Hadrocodium sheds light on this history. We found that relative brain size expanded to mammalian levels, with enlarged olfactory bulbs, neocortex, olfactory (pyriform) cortex, and cerebellum, in two evolutionary pulses. The initial pulse was probably driven by increased resolution in olfaction and improvements in tactile sensitivity (from body hair) and neuromuscular coordination. A second pulse of olfactory enhancement then enlarged the brain to mammalian levels. The origin of crown Mammalia saw a third pulse of olfactory enhancement, with ossified ethmoid turbinals supporting an expansive olfactory epithelium in the nasal cavity, allowing full expression of a huge odorant receptor genome.

Inner ear of a notoungulate placental mammal: anatomical description and examination of potentially phylogenetically informative characters

We provide the first detailed description of the inner ear of a notoungulate, an extinct group of endemic South American placental mammals, based on a three‐dimensional reconstruction extracted from CT imagery of a skull of Notostylops murinus. This description provides new anatomical data that should prove to be phylogenetically informative, an especially significant aspect of this research given that both the interrelationships of notoungulates and the position of Notoungulata within Placentalia are still unresolved. We also assess the locomotor agility of Notostylops based on measurements of the semicircular canals. This is the best available data on the locomotion of a notostylopid because significant postcranial remains for this group have not been described. The cochlea of Notostylops has 2.25 turns, and the stapedial ratio is 1.6. The stapedial ratio is one of the lowest recorded for a eutherian, which typically have ratios greater than 1.8. The fenestra cochleae is located posterior to the fenestra vestibuli, a condition previously only reported for some stem primates. The separation of the saccule and utricule of the vestibule is visible on the digital endocast of the bony labyrinth. The posterior arm of the LSC and the inferior arm of the PSC are confluent, but these do not form a secondary crus commune, and the phylogenetic or functional significance of this confluence is unclear at this time. Locomotor agility scores for Notostylops suggest a medium or ‘average’ degree of agility of motion compared to extant mammals. In terms of its locomotion, we tentatively predict that Notostylops was a generalized terrestrial mammal, with cursorial tendencies, based on its agility scores and the range of locomotor patterns inferred from postcranial analyses of other notoungulates.

Comparative study of notoungulate (Placentalia, Mammalia) bony labyrinths and new phylogenetically informative inner ear characters

The phylogenetic relationships of notoungulates, an extinct group of predominantly South American herbivores, remain poorly resolved with respect to both other placental mammals and among one another. Most previous phylogenetic analyses of notoungulates have not included characters of the internal cranium, not least because few such features, including the bony labyrinth, have been described for members of the group. Here we describe the inner ears of the notoungulates Altitypotherium chucalensis (Mesotheriidae), Pachyrukhos moyani (Hegetotheriidae) and Cochilius sp. (Interatheriidae) based on reconstructions of bony labyrinths obtained from computed tomography imagery. Comparisons of the bony labyrinths of these taxa with the basally diverging notoungulate Notostylops murinus (Notostylopidae), an isolated petrosal from Itaboraí, Brazil, referred to Notoungulata, and six therian outgroups, yielded an inner ear character matrix of 25 potentially phylogenetically informative characters, 14 of them novel to this study. Two equivocally optimized character states potentially support a pairing of Mesotheriidae and Hegetotheriidae, whereas four others may be diagnostic of Notoungulata. Three additional characters are potentially informative for diagnosing more inclusive clades: one for crown Placentalia; another for a clade containing Kulbeckia, Zalambdalestes, and Placentalia; and a third for Eutheria (crown Placentalia plus stem taxa). Several other characters are apomorphic for at least one notoungulate in our study and are of potential interest for broader taxonomic sampling within Notoungulata to clarify currently enigmatic interrelationships. Measures of the semicircular canals were used to infer agility (e.g. capable of quick movements vs. lethargic movements) of these taxa. Agility scores calculated from these data generally corroborate interpretations based on postcranial remains of these or closely related species. We provide estimates of the low‐frequency hearing limits in notoungulates based on the ratio of radii of the apical and basal turns of the cochlea. These limits range from 15 Hz in Notostylops to 149 Hz in Pachyrukhos, values comparable to the Asian elephant (Elephas maximus) and the California sea lion (Zalophus californianus) when hearing in air, respectively.

Comparative Morphology of the Internal Nasal Skeleton of Adult Marsupials Based on X-ray Computed Tomography

Abstract The internal skeleton of the nasal cavity is sporadically and often incompletely described for many marsupial species and mammals in general. Here, I provide an anatomical survey of the ethmoid in the skulls of adult marsupials based on examination of computed tomography (CT) imagery of 29 taxa representing all the major extant groups of marsupials. This survey resulted in a description of the “generalized condition” for the morphology of the marsupial ethmoid bone, ossified nasal septum, and associated structures of the interior of the nasal cavity. I also described how the ethmoid in different clades varies in morphology from the general condition for Marsupialia. Intraspecific variation of the ethmoid was described based on a sample of 18 specimens of Monodelphis domestica, the gray short-tailed opossum, and asymmetries within a single specimen are documented for other taxa. For the most part I follow the nomenclature of previous nasal cavity workers, but I also provide explicit definitions of all the terms used and some of the common synonyms for these in the literature. Endoturbinals and ectoturbinals are numbered sequentially following the work of previous authors, because of the issues with serial homology for these elements. The number of elements of the marsupial ethmoid is fairly conserved with the typical and likely ancestral condition being the presence of an ossified maxilloturbinal, nasoturbinal, two ectoturbinals, and five endoturbinals. However, there is considerable variation in the complexity, spatial placement, and overall morphology of the bony internal skeleton of the nose. Based on this descriptive work, I documented 35 discrete characters from the ethmoid and ossified nasal septum complex in marsupials. These characters were scored for this sample of marsupials and five mammalian outgroups. Examination of these characters on preexisting topologies of marsupial relationships revealed some phylogenetic signal for this sample of marsupial species. Three of the characters are punitively diagnostic for previously recognized clades within Marsupialia. It is possible that when this matrix is combined with morphological data from other anatomical systems and molecular data that previously unrecognized or controversial clades within Marsupialia may be supported. Even so, the relatively little amount of phylogenetic signal from my character matrix prompted me to search for alternative explanations for mechanisms driving the variation in this anatomical system. Consequently, I compared ecological data with the number of ecto- and endoturbinals as a preliminary test to determine whether some of the interspecific variation in the osteology of the ethmoid is a result of ecological factors, but found few correlations to support this idea. Finally, my study highlights some issues with homologies of mammalian nasal cavity elements that need to be resolved and reexamined. These include whether the ossified nasal septum arises from the presphenoid or the mesethmoid, and a test of the current view of serial homology of the endoturbinals and ectoturbinals.

Description of a digital cranial endocast of Bathygenys reevesi (Merycoidodontidae; Oreodontoidea) and implications for apomorphy-based diagnosis of isolated, natural endocasts

ABSTRACT Relatively few studies of cranial endocasts document intraspecific variation. Here, discrete morphological and morphometric variation from a sample of more than 150 natural cranial endocasts from a single Eocene locality, Reeves Bonebed (hereafter ‘RBB’) from West Texas are documented. The first description of a digital endocast of an oreodont, Bathygenys reevesi, is given to provide comparative data for other oreodont endocasts. The RBB endocasts were originally assigned to B. reevesi, but virtually none has diagnostic craniodental material still attached, and isolated endocasts of other cetartiodactyl species are known from this locality. Consequently, an attempt was made to identify apomorphies on the RBB sample to diagnose specimens to the lowest possible taxonomic level. The RBB endocasts were diagnosed as oreodonts based on the presence of large, rounded casts of the tuberculum olfactorium, but no specimen can be diagnosed to a particular species. The range for most linear measurements for the RBB sample overlapped with measures from multiple species of oreodonts from RBB. A coefficient of variation analysis of linear measurements suggests that the RBB sample represents more than one species. Therefore, endocasts from RBB that lack associated craniodental material cannot be definitively assigned to a species, and the original assumption that all are B. reevesi is not supported. This illustrates the necessity of applying apomorphy-based identifications for isolated specimens, including endocasts. In addition, this study reveals some gaps in data from cetartiodactyl brains, which need to be filled for future studies on brain evolution in this clade.

Cranial anatomy of the Duchesnean primate Rooneyia viejaensis: New insights from high resolution computed tomography

Rooneyia viejaensis is a North American Eocene primate of uncertain phylogenetic affinities. Although the external cranial anatomy of Rooneyia is well studied, various authors have suggested that Rooneyia is a stem haplorhine, stem strepsirrhine, stem tarsiiform, or stem anthropoid. Here we describe the internal cranial anatomy of the Rooneyia holotype based on micro-computed tomography and discuss the phylogenetic implications of this anatomy. Precise measurements of the natural endocast filling the braincase of the Rooneyia holotype reveal that the genus had a relative brain size comparable to some living callitrichines and strepsirrhines. Rooneyia was thus probably more encephalized than any other known omomyiform, adapiform, or plesiadapiform. Relative olfactory bulb size in Rooneyia was most comparable to some living strepsirrhines and the stem anthropoid Parapithecus. The nasal fossa of Rooneyia resembled that of living strepsirrhines in retaining an obliquely oriented nasolacrimal canal, four ethmoturbinals, and an olfactory recess separated from the nasopharyngeal meatus by a transverse lamina. The ear region of Rooneyia is characterized by large and complete canals for both the stapedial and promontory branches of the internal carotid artery. Rooneyia also retains a patent parotic fissure and thus had an extrabullar origin of the stapedius muscle. In most of these respects, Rooneyia exhibits the condition that is presumed to be primitive for crown primates and lacks a number of key crown haplorhine synapomorphies (e.g., a dorso-ventrally oriented nasolacrimal canal, loss of the olfactory recess, loss of ethmoturbinals 3-4, loss or extreme reduction of the stapedial canal due to involution of the stapedial artery). These data are consistent with the hypothesis that Rooneyia is an advanced stem primate or a basal crown primate but are inconsistent with prior suggestions that Rooneyia is a crown haplorhine.

Reproductive status and sex show strong effects on knee OA in a baboon model

OBJECTIVE We aimed to characterize severity and occurrence of knee osteoarthritis (OA), and effects of age, sex, body mass, and reproductive status on population-level normal variation in this condition in the baboon, a natural model of human knee OA. METHODS We visually inspected articular cartilage of distal right femora of 464 baboons (309 females, 155 males) and assigned an OA severity score (comparable to a modified Outerbridge score) from 1 = unaffected to 4 = advanced OA (eburnation). Presence/absence of osteophytes was recorded. We tested for significant effects of age, sex, body mass, and, in females, reproductive status (pre-, peri-, or post-menopausal) on OA. When appropriate, analyses were repeated on an age-matched subset (153 of each sex). RESULTS Knee OA was more frequent and severe in older animals (P < 0.0001), but significant age variation was apparent in each severity grade. Sex differences within the younger and older age groups suggest that males develop knee OA earlier, but females progress more quickly to advanced disease. There is a strong relationship between reproductive status and OA severity grade in females (P = 0.0005) with more severe OA in peri- and post-menopausal female baboons, as in humans. CONCLUSIONS Idiopathic knee OA is common in adult baboons. Occurrence and severity are influenced strongly by reproductive status in females, and by sex with regard to patterns of disease progression - providing an animal model to investigate sex-specific variation in OA susceptibility in which the environmental heterogeneity inherent in human populations is vastly reduced.

Development of the ethmoid in Caluromys philander (Didelphidae, Marsupialia) with a discussion on the homology of the turbinal elements in marsupials.

Homology of turbinals, or scroll bones, of the mammalian ethmoid bone is poorly known and complicated by a varied terminology. Positionally, there are two main types of ossified adult turbinals known as endoturbinals and ectoturbinals, and their cartilaginous precursors are called ethmoturbinals and frontoturbinals, respectively. Endoturbinals are considered to be serially homologous due to similarity in their developmental patterns. Consequently, endoturbinals from mammals with differing numbers of elements cannot be individually homogenized. In this study, the development of the ethmoid of Caluromys philander, the bare‐tailed woolly opossum, is described based on serial sections of six pouchlings ranging in age from 20 to 84 days postnatal (PND‐84), and computed tomography images of an adult skull. I found that four ethmoturbinals initially develop as seen in PND‐20 and PND‐30 individuals but by PND‐64 an interturbinal (corresponding to endoturbinal III in adults) is present between ethmoturbinals II and III. This developmental pattern is identical to that of Monodelphis domestica, the gray short‐tailed opossum, and is probably also present in the marsupials Didelphis marsupialis, and Thylacinus cynocephalus based on work of previous authors. These data suggest that endoturbinal III has a developmental pattern that differs from other endoturbinals, and the name interturbinal should be retained for the adult structure in recognition of this difference. These results may prove useful for homologizing this individual turbinal element across marsupials, the majority of which have five endoturbinals as adults. This might also explain the presumed placental ancestral condition of four endoturbinals if the marsupial interturbinal is lost. Anat Rec, 297:2007–2017, 2014.

The Internal Nasal Skeleton of the Bat Pteropus lylei K. Andersen, 1908 (Chiroptera: Pteropodidae)

ABSTRACT The cranial osteology of the megachiropteran Pteropus Brisson, 1762, was the subject of recent study that covered all of the skull bones in significant detail, except for the anatomy of the nasal capsule. Here, we describe and illustrate the internal nasal skeleton of Pteropus lylei K. Andersen, 1908, using histological sections of a fetus and high resolution X-ray computed tomographic (HRXCT) imagery of an adult specimen. The internal nasal skeleton of Pteropus lacks a rostral nasoturbinal and includes a caudal nasoturbinal that corresponds to the ossified crista semicircularis of the fetus; three endoturbinals; one ectoturbinal; the maxilloturbinal; and a low basal crest that may represent a rudimentary element. We describe in detail the structure and connections of these elements in Pteropus. The maxilloturbinal is the largest element. In cross section, the caudal nasoturbinal is unilaminar, the maxilloturbinal is double bilaminar (i.e., each of the basal twin laminae splits further into two secondary laminae), and the other elements range from incipient to asymmetrically double bilaminar (i.e., one branch simple, the other split). All turbinais of the ethmoidal labyrinth contribute to the cribriform plate, creating a specific pattern of cribriform foramina. The elements found in Pteropus are compared with those of other well-known mammals with relatively few turbinai elements, including other bats, primates, canids, and marsupials. We show that, despite terminological discrepancies across studies, homologies are straightforward to establish among these taxa and so comparative or phylogenetic studies may benefit from inclusion of turbinai characters.

Osteological associations with unique tooth development in manatees (Trichechidae, Sirenia): a detailed look at modern Trichechus and a review of the fossil record.

Modern manatees have a unique type of tooth development, continually forming identical new molars in the posterior end of each quadrant of their mouths, and then progressively moving teeth anteriorly, only to reabsorb roots and spit out worn crowns. This process is not only developmentally complex, but requires space in the oral cavity that imposes its own limitations on other uses of that space. To gain a clearer understanding of the anatomical constraints on the evolution of this unique developmental process, we identified the specialized craniodental features in modern Trichechus that permit this specialization using visual observation and CT. Furthermore, to better understand the evolution of these traits, we review the fossil record of trichechids for these traits, including CT analysis of the skull of Miosiren kocki, a possible early member of the family from the Early Miocene of Belgium. Anat Rec, 2012.