Eric G. Ekdale

Late Cretaceous relatives of rabbits, rodents, and other extant eutherian mammals

Extant eutherian mammals and their most recent common ancestor constitute the crown group Placentalia. This taxon, plus all extinct taxa that share a more recent common ancestor with placentals than they do with Metatheria (including marsupials), constitute Eutheria. The oldest well documented eutherian-dominated fauna in the world is Dzharakuduk, Uzbekistan. Among eutherians that it yields is Kulbeckia, an 85–90-Myr-old member of Zalambdalestidae (a family of Late Cretaceous Asian eutherians). This extends Zalambdalestidae back by some 10 million years from sites in the Gobi Desert, Mongolia. A phylogenetic analysis of well described Late Cretaceous eutherians strongly supports Zalambdalestidae, less strongly supports ‘Zhelestidae’ (a Late Cretaceous clade related to Tertiary ungulates), but does not support Asioryctitheria (a group of Late Cretaceous Asian eutherians). A second analysis incorporating placentals from clades that include rodents (Tribosphenomys), lagomorphs (Mimotona) and archaic ungulates (Protungulatum and Oxyprimus) strongly supports Zalambdalestidae in a clade with Glires (rabbits, rodents and extinct relatives) and less strongly ‘Zhelestidae’ within a clade that includes archaic ungulates (‘condylarths’). This argues that some Late Cretaceous eutherians belong within the crown group Placentalia. The ages of these taxa are in line with molecularly based estimates of 64–104 Myr ago (median 84 Myr ago) for the superordinal diversification of some placentals, but provide no support for a Late Cretaceous diversification of extant placental orders.

Comparative Anatomy of the Bony Labyrinth (Inner Ear) of Placental Mammals

Background Variation is a naturally occurring phenomenon that is observable at all levels of morphology, from anatomical variations of DNA molecules to gross variations between whole organisms. The structure of the otic region is no exception. The present paper documents the broad morphological diversity exhibited by the inner ear region of placental mammals using digital endocasts constructed from high-resolution X-ray computed tomography (CT). Descriptions cover the major placental clades, and linear, angular, and volumetric dimensions are reported. Principal Findings The size of the labyrinth is correlated to the overall body mass of individuals, such that large bodied mammals have absolutely larger labyrinths. The ratio between the average arc radius of curvature of the three semicircular canals and body mass of aquatic species is substantially lower than the ratios of related terrestrial taxa, and the volume percentage of the vestibular apparatus of aquatic mammals tends to be less than that calculated for terrestrial species. Aspects of the bony labyrinth are phylogenetically informative, including vestibular reduction in Cetacea, a tall cochlear spiral in caviomorph rodents, a low position of the plane of the lateral semicircular canal compared to the posterior canal in Cetacea and Carnivora, and a low cochlear aspect ratio in Primatomorpha. Significance The morphological descriptions that are presented add a broad baseline of anatomy of the inner ear across many placental mammal clades, for many of which the structure of the bony labyrinth is largely unknown. The data included here complement the growing body of literature on the physiological and phylogenetic significance of bony labyrinth structures in mammals, and they serve as a source of data for future studies on the evolution and function of the vertebrate ear.

Anatomical evidence for low frequency sensitivity in an archaeocete whale: comparison of the inner ear of Zygorhiza kochii with that of crown Mysticeti

The evolution of hearing in cetaceans is a matter of current interest given that odontocetes (toothed whales) are sensitive to high frequency sounds and mysticetes (baleen whales) are sensitive to low and potentially infrasonic noises. Earlier diverging stem cetaceans (archaeocetes) were hypothesized to have had either low or high frequency sensitivity. Through CT scanning, the morphology of the bony labyrinth of the basilosaurid archaeocete Zygorhiza kochii is described and compared to novel information from the inner ears of mysticetes, which are less known than the inner ears of odontocetes. Further comparisons are made with published information for other cetaceans. The anatomy of the cochlea of Zygorhiza is in line with mysticetes and supports the hypothesis that Zygorhiza was sensitive to low frequency noises. Morphological features that support the low frequency hypothesis and are shared by Zygorhiza and mysticetes include a long cochlear canal with a high number of turns, steeply graded curvature of the cochlear spiral in which the apical turn is coiled tighter than the basal turn, thin walls separating successive turns that overlap in vestibular view, and reduction of the secondary bony lamina. Additional morphology of the vestibular system indicates that Zygorhiza was more sensitive to head rotations than extant mysticetes are, which likely indicates higher agility in the ancestral taxon.

Form and function of the mammalian inner ear

The inner ear of mammals consists of the cochlea, which is involved with the sense of hearing, and the vestibule and three semicircular canals, which are involved with the sense of balance. Although different regions of the inner ear contribute to different functions, the bony chambers and membranous ducts are morphologically continuous. The gross anatomy of the cochlea that has been related to auditory physiologies includes overall size of the structure, including volume and total spiral length, development of internal cochlear structures, including the primary and secondary bony laminae, morphology of the spiral nerve ganglion, and the nature of cochlear coiling, including total number of turns completed by the cochlear canal and the relative diameters of the basal and apical turns. The overall sizes, shapes, and orientations of the semicircular canals are related to sensitivity to head rotations and possibly locomotor behaviors. Intraspecific variation, primarily in the shape and orientation of the semicircular canals, may provide additional clues to help us better understand form and function of the inner ear.

Review of the Cetacean Nose: Form, Function, and Evolution

The cetacean nose presents a unique suite of anatomical modifications. Key among these is posterior movement of the external nares from the tip of the rostrum to the top of the head. Concomitant with these anatomical changes are functional changes including the evolution of echolocation in odontocetes, and reduction of olfaction in Neoceti (crown odontocetes and mysticetes). Anatomical and embryological development of the nose in crown cetaceans is reviewed as well as their functional implications. A sequence of evolutionary transformations of the nose is proposed in the transition from a terrestrial to an aquatic lifestyle made by whales. Basilosaurids and all later whales reduce the nasal turbinates. The next stage characterizes Neoceti which exhibit reduction of the major olfactory structures, i.e. the ethmoturbinates, cribriform plate and maxilloturbinates with further reduction and subsequent loss in odontocetes. These anatomical modifications reflect underlying genetic changes such as the reduction of olfactory receptor genes, although mysticetes retain some olfactory abilities. Modifications of the facial and nasal region of odontocetes reflect specialization for biosonar sound production. Anat Rec, 297:2205–2215, 2014.

Vascularization of the Gray Whale Palate (Cetacea, Mysticeti, Eschrichtius robustus): Soft Tissue Evidence for an Alveolar Source of Blood to Baleen

The origin of baleen in mysticetes heralded a major transition during cetacean evolution. Extant mysticetes are edentulous in adulthood, but rudimentary teeth develop in utero within open maxillary and mandibular alveolar grooves. The teeth are resorbed prenatally and the alveolar grooves close as baleen germ develops. Arteries supplying blood to highly vascularized epithelial tissue from which baleen develops pass through lateral nutrient foramina in the area of the embryonic alveolar grooves and rudimentary teeth. Those vessels are hypothesized to be branches of the superior alveolar artery, but branches of the greater palatine arteries may play a role in the baleen vascularization. Through a combination of latex injection, CT, and traditional dissection of the palate of a neonatal gray whale (Eschrichtius robustus), we confirm that the baleen receives blood from vessels within the superior alveolar canal via the lateral foramina. The greater palatine artery is restricted to its own passage with no connections to the baleen. This study has implications for the presence of baleen in extinct taxa by identifying the vessels and bony canals that supply blood to the epithelium from which baleen develops. The results indicate that the lateral foramina in edentulous mysticete fossils are bony correlates for the presence of baleen, and the results can be used to help identify bony canals and foramina that have been used to reconstruct baleen in extinct mysticetes that retained teeth in adulthood. Further comparisons are made with mammals that also possess oral keratin structures, including ruminants, ornithorhynchid monotremes, and sirenians. Anat Rec, 298:691–702, 2015.

Morphometrics and Structure of Complete Baleen Racks in Gray Whales (Eschrichtius robustus) From the Eastern North Pacific Ocean

Mysticetes have evolved a novel filter feeding apparatus—baleen—an epidermal keratinous tissue composed of keratin that grows as a serial arrangement of transverse cornified laminae from the right and left sides of the palate. The structure and function of baleen varies among extant mysticete clades and this variation likely can be viewed as adaptations related to different filter feeding strategies. In one of the first morphometric studies of the full baleen apparatus, we describe the morphology of complete baleen racks in neonate, yearling and adult gray whales (Eschrichtius robustus), and note morphometric variations between age groups as well as within individual racks. Morphometric data and detailed descriptions were collected from the full baleen apparatus of three frozen specimens of E. robustus using previously derived ecologically significant and broad scale measurements of baleen. Additionally, characters of the baleen apparatus were described based on visible patterns of baleen laminae and plates on the dorsal root of the rack. Results indicate that the longest, widest, and thickest plates and laminae are found toward the posterior half of the rack, resulting in the greatest surface area for filtration of prey occurring in this region. Ontogenetic changes were also documented that reveal a progressive increase in the filter surface area of the developing baleen apparatus as baleen laminae and main plates grow in length and width. Also noted was a progressive posterior shift in the position of greatest filtration area. Histological examination of the epithelial base (Zwischensubstanz) and laminae showed basic epidermal layers, as well as gapping between layers and vacuoles. Anat Rec, 298:703–719, 2015.

Morphological variation among the inner ears of extinct and extant baleen whales (Cetacea: Mysticeti)

Living mysticetes (baleen whales) and odontocetes (toothed whales) differ significantly in auditory function in that toothed whales are sensitive to high‐frequency and ultrasonic sound vibrations and mysticetes to low‐frequency and infrasonic noises. Our knowledge of the evolution and phylogeny of cetaceans, and mysticetes in particular, is at a point at which we can explore morphological and physiological changes within the baleen whale inner ear. Traditional comparative anatomy and landmark‐based 3D‐geometric morphometric analyses were performed to investigate the anatomical diversity of the inner ears of extinct and extant mysticetes in comparison with other cetaceans. Principal component analyses (PCAs) show that the cochlear morphospace of odontocetes is tangential to that of mysticetes, but odontocetes are completely separated from mysticetes when semicircular canal landmarks are combined with the cochlear data. The cochlea of the archaeocete Zygorhiza kochii and early diverging extinct mysticetes plot within the morphospace of crown mysticetes, suggesting that mysticetes possess ancestral cochlear morphology and physiology. The PCA results indicate variation among mysticete species, although no major patterns are recovered to suggest separate hearing or locomotor regimes. Phylogenetic signal was detected for several clades, including crown Cetacea and crown Mysticeti, with the most clades expressing phylogenetic signal in the semicircular canal dataset. Brownian motion could not be excluded as an explanation for the signal, except for analyses combining cochlea and semicircular canal datasets for Balaenopteridae. J. Morphol. 277:1599–1615, 2016.

From Teeth to Baleen and Raptorial to Bulk Filter Feeding in Mysticete Cetaceans: The Role of Paleontological, Genetic, and Geochemical Data in Feeding Evolution and Ecology

The origin of baleen and filter feeding in mysticete cetaceans occurred sometime between approximately 34 and 24 million years ago and represents a major macroevolutionary shift in cetacean morphology (teeth to baleen) and ecology (raptorial to filter feeding). We explore this dramatic change in feeding strategy by employing a diversity of tools and approaches: morphology, molecules, development, and stable isotopes from the geological record. Adaptations for raptorial feeding in extinct toothed mysticetes provide the phylogenetic context for evaluating morphological apomorphies preserved in the skeletons of stem and crown edentulous mysticetes. In this light, the presence of novel vascular structures on the palates of certain Oligocene toothed mysticetes is interpreted as the earliest evidence of baleen and points to an intermediate condition between an ancestral condition with teeth only and a derived condition with baleen only. Supporting this step-wise evolutionary hypothesis, evidence from stable isotopes show how changes in dental chemistry in early toothed mysticetes tracked the changes in diet and environment. Recent discoveries also demonstrate how this transition was made possible by radical changes in cranial ontogeny. In addition, genetic mutations and the possession of dental pseudogenes in extant baleen whales support a toothed ancestry for mysticetes. Molecular and morphological data also document the dramatic developmental shifts that take place in extant fetal baleen whales, in skull development, resorption of a fetal dentition and growth of baleen. The mechanisms involved in this complex evolutionary transition that entails multiple, integrated aspects of anatomy and ecology are only beginning to be understood, and future work will further clarify the processes underlying this macroevolutionary pattern.

Tongue and hyoid musculature and functional morphology of a neonate gray whale (Cetacea, Mysticeti, Eschrichtius robustus).

Little is known about the anatomy and musculature of the gray whale (Eschrichtius robustus), especially related to the anatomy of the tongue and hyoid region. The recovery of an extremely fresh head of a neonatal female gray whale provided an opportunity to conduct the first in‐depth investigation of the musculoskeletal features of the tongue and hyoid apparatus. Unlike other mysticetes, the gray whale tongue is strong, muscular, and freely mobile inside the buccal cavity. In particular, the genioglossus and hyoglossus muscles are extremely large and robust making up the majority of the body of the tongue. In addition, the genioglossus had a unique position and fiber orientation in the tongue compared to other mammals. The structure of the hyoid apparatus differs between E. robustus and other mysticete species, although there are similarities among individual elements. We provide the first documentation of fungiform papillae that may be associated with taste buds in Mysticeti. The highly mobile, robust tongue and the presence of well‐defined tongue and hyoid musculature are in keeping with observations of gray whale feeding that suggest this group of whales utilize oral suction to draw benthic prey into the buccal cavity. Anat Rec, 298:660–674, 2015.