Thomas A. Deméré

Morphological and Molecular Evidence for a Stepwise Evolutionary Transition from Teeth to Baleen in Mysticete Whales

The origin of baleen in mysticete whales represents a major transition in the phylogenetic history of Cetacea. This key specialization, a keratinous sieve that enables filter-feeding, permitted exploitation of a new ecological niche and heralded the evolution of modern baleen-bearing whales, the largest animals on Earth. To date, all formally described mysticete fossils conform to two types: toothed species from Oligocene-age rocks ( approximately 24 to 34 million years old) and toothless species that presumably utilized baleen to feed (Recent to approximately 30 million years old). Here, we show that several Oligocene toothed mysticetes have nutrient foramina and associated sulci on the lateral portions of their palates, homologous structures in extant mysticetes house vessels that nourish baleen. The simultaneous occurrence of teeth and nutrient foramina implies that both teeth and baleen were present in these early mysticetes. Phylogenetic analyses of a supermatrix that includes extinct taxa and new data for 11 nuclear genes consistently resolve relationships at the base of Mysticeti. The combined data set of 27,340 characters supports a stepwise transition from a toothed ancestor, to a mosaic intermediate with both teeth and baleen, to modern baleen whales that lack an adult dentition but retain developmental and genetic evidence of their ancestral toothed heritage. Comparative sequence data for ENAM (enamelin) and AMBN (ameloblastin) indicate that enamel-specific loci are present in Mysticeti but have degraded to pseudogenes in this group. The dramatic transformation in mysticete feeding anatomy documents an apparently rare, stepwise mode of evolution in which a composite phenotype bridged the gap between primitive and derived morphologies; a combination of fossil and molecular evidence provides a multifaceted record of this macroevolutionary pattern.

Chapter 3: Pinnipedimorph Evolutionary Biogeography

Abstract Previous hypotheses for the origin and diversification of pinnipeds have followed a narrative approach based mostly on dispersalist (i.e., center of origin) explanations. Using an analytical approach, we present a testable hypothesis to explain the evolutionary biogeography of pinnipedimorphs (fur seals, sea lions, walruses, seals, and their fossil relatives) based on both dispersal and vicariant events in the context of a species-level phylogenetic framework. This integrated hypothesis considers many lines of evidence, including physical and ecologic factors controlling modern pinniped distributions, past geologic events related to opening and closing of seaways, paleoceanographic models, the improving pinniped fossil record, and pinniped phylogenetic analyses based on both morphologic and molecular data sets. Oceanic biogeographic regions and faunal provinces are defined and oceanic circulation patterns discussed with reference to the distribution of extant and fossil species. Paleobiogeographic hypotheses for each of the major pinniped lineages are presented using area cladograms and paleogeographic maps showing oceanographic and tectonic changes during successive intervals of the Cenozoic. Our biogeographic hypothesis supports an eastern North Pacific origin for pinnipedimorphs during the late Oligocene coincident with initiation of glaciation in Antarctica. During the early Miocene, pinnipedimorphs remained restricted to the eastern North Pacific, where they began to diversify. Otariids (fur seals and sea lions) are first known from the late Miocene in the North Pacific, where they remained restricted until the late Pliocene. A transequatorial dispersal into the western South Pacific at this time preceded the rapid diversification of this group that occurred during the Pleistocene in the Southern Ocean. Odobenids (walruses) evolved in the North Pacific during the late early Miocene and underwent dramatic diversification in the late Miocene with later members of the odobenine lineage dispersing into the North Atlantic, most likely via an Arctic route. Extinct archaic phocoids, the desmatophocids, known only from the early to late Miocene, were confined to the eastern and western North Pacific. Phocids, although postulated here to have a North Pacific origin, are first known as fossils from the middle Miocene in the eastern and western North Atlantic region, as well as the Paratethys. Both monachine and phocine seals are distinct lineages beginning in the middle Miocene in the eastern and western provinces of the North Atlantic. During the late Miocene, phocids underwent a dramatic diversification. The early biogeographic history of phocine seals is centered in the Arctic and North Atlantic. Subsequent dispersal of phocines into the Paratethys and Pacific occurred during the Pleistocene. In contrast, monachine seals have a southern hemisphere center of diversity, especially the lobodontines of the Southern Ocean. Southern dispersal of this clade most likely occurred through the Neogene Central American Seaway prior to its closure in the mid-Pliocene. The pagophilic nature of extant phocine and lobodontine seals is largely a function of Pleistocene glacioeustatic events.

The Comparative Osteology of the Petrotympanic Complex (Ear Region) of Extant Baleen Whales (Cetacea: Mysticeti)

Background Anatomical comparisons of the ear region of baleen whales (Mysticeti) are provided through detailed osteological descriptions and high-resolution photographs of the petrotympanic complex (tympanic bulla and petrosal bone) of all extant species of mysticete cetaceans. Salient morphological features are illustrated and identified, including overall shape of the bulla, size of the conical process of the bulla, morphology of the promontorium, and the size and shape of the anterior process of the petrosal. We place our comparative osteological observations into a phylogenetic context in order to initiate an exploration into petrotympanic evolution within Mysticeti. Principal Findings The morphology of the petrotympanic complex is diagnostic for individual species of baleen whale (e.g., sigmoid and conical processes positioned at midline of bulla in Balaenoptera musculus; confluence of fenestra cochleae and perilymphatic foramen in Eschrichtius robustus), and several mysticete clades are united by derived characteristics. Balaenids and neobalaenids share derived features of the bulla, such as a rhomboid shape and a reduced anterior lobe (swelling) in ventral aspect, and eschrichtiids share derived morphologies of the petrosal with balaenopterids, including loss of a medial promontory groove and dorsomedial elongation of the promontorium. Monophyly of Balaenoidea (Balaenidae and Neobalaenidae) and Balaenopteroidea (Balaenopteridae and Eschrichtiidae) was recovered in phylogenetic analyses utilizing data exclusively from the petrotympanic complex. Significance This study fills a major gap in our knowledge of the complex structures of the mysticete petrotympanic complex, which is an important anatomical region for the interpretation of the evolutionary history of mammals. In addition, we introduce a novel body of phylogenetically informative characters from the ear region of mysticetes. Our detailed anatomical descriptions, illustrations, and comparisons provide valuable data for current and future studies on the phylogenetic relationships, evolution, and auditory physiology of mysticetes and other cetaceans throughout Earths history.

A 130,000-year-old archaeological site in southern California, USA

The earliest dispersal of humans into North America is a contentious subject, and proposed early sites are required to meet the following criteria for acceptance: (1) archaeological evidence is found in a clearly defined and undisturbed geologic context; (2) age is determined by reliable radiometric dating; (3) multiple lines of evidence from interdisciplinary studies provide consistent results; and (4) unquestionable artefacts are found in primary context. Here we describe the Cerutti Mastodon (CM) site, an archaeological site from the early late Pleistocene epoch, where in situ hammerstones and stone anvils occur in spatio-temporal association with fragmentary remains of a single mastodon (Mammut americanum). The CM site contains spiral-fractured bone and molar fragments, indicating that breakage occured while fresh. Several of these fragments also preserve evidence of percussion. The occurrence and distribution of bone, molar and stone refits suggest that breakage occurred at the site of burial. Five large cobbles (hammerstones and anvils) in the CM bone bed display use-wear and impact marks, and are hydraulically anomalous relative to the low-energy context of the enclosing sandy silt stratum. 230Th/U radiometric analysis of multiple bone specimens using diffusion-adsorption-decay dating models indicates a burial date of 130.7 ± 9.4 thousand years ago. These findings confirm the presence of an unidentified species of Homo at the CM site during the last interglacial period (MIS 5e; early late Pleistocene), indicating that humans with manual dexterity and the experiential knowledge to use hammerstones and anvils processed mastodon limb bones for marrow extraction and/or raw material for tool production. Systematic proboscidean bone reduction, evident at the CM site, fits within a broader pattern of Palaeolithic bone percussion technology in Africa, Eurasia and North America. The CM site is, to our knowledge, the oldest in situ, well-documented archaeological site in North America and, as such, substantially revises the timing of arrival of Homo into the Americas.

A Late Cretaceous nodosaurid ankylosaur (Dinosauria; Ornithischia) from marine sediments of coastal California

A partial nodosaurid ankylosaur skeleton, consisting primarily of the ilia, hindlimbs, posterior dorsal armor, plus partial forelimb elements and additional armor, was recovered from the marine Point Loma Formation, late Campanian age, north of San Diego, California. The specimen is similar to contemporaneous species of Panoplosaurus and Edmontonia from terrestrial sediments of the western interior, but there are also similarities to the armor of Stegopelta landerensis from marine sediments of earliest Cenomanian age from Wyoming. Skeletal elements critical for generic determination are not preserved, and the specimen is identified as Nodosauridae, incertae sedis. An associated marine invertebrate fauna and nannoplankton flora have revealed some discrepencies in the correlation systems used for Upper Cretaceous marine rocks of coastal California. Hollow limb bones of the specimen are interpreted as a preservational artifact. Nodosaurids had broad ecological tolerances, and visited riparian and coastal environments more frequently than other dinosaurs. However, a review of morphologic and distributional evidence fails to support a theory of amphibious or aquatic habits for nodosaurids.

A reevaluation of Proneotherium repenningi from the Miocene Astoria Formation of Oregon and its position as a basal odobenid (Pinnipedia: Mammalia)

Abstract New crania, dentitions, and postcrania of the fossil pinniped, Proneotherium repenningi are described from the early to middle Miocene-age Astoria Formation of Lincoln County, Oregon. This sample includes specimens of four adult individuals; all probably males. The skull of Proneotherium repenningi shares many generalized features with basal pinnipeds (e.g., species of Enaliarctos) including its overall elongation, low profile, low sagittal crest, well developed lambdoidal crests, slender zygomatic arches, small orbits, slightly arched palate, dental formulae, and distinct embrasure pit. Proneotherium, however, differs from species of Enaliarctos in possession of a continuous and horizontal crest connecting the mastoid and paroccipital processes and in having a less secodont dentition. The molariform premolar dentition of Proneotherium is noteworthy and can be interpreted as representing the initial stage in a morphologic series that extends through Neotherium to Imagotaria. This morphologic series reflects a functional change from a shearing dentition to more of a piercing dentition and from a dentition capable of processing food (i.e., chewing) to a dentition that serves primarily to seize and hold prey. The hindlimb anatomy of Proneotherium provides important information concerning the evolution of aquatic adaptations and clearly shows that many pinniped innovations (short and broad femur, long and slender tibia, and elongated metatarsals I and V [relative to metatarsal III]) evolved very early. Evaluation of available specimens of Proneotherium supports recognition of a single species, Proneotherium repenningi. A cladistic analysis utilizing 24 cranial, dental and postcranial characters supports monophyly of the genus Proneotherium and suggests a close sister group relationship with another basal walrus, Prototaria. The parsimony analysis also confirms the monophyly of the Odobenidae, which is here defined as the clade containing the most recent common ancestor of Proneotherium and Odobenus and all of its descendants including Prototaria, Neotherium, Imagotaria, the dusignathines, and the odobenines.

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.

Unique feeding morphology in a new prognathous extinct porpoise from the Pliocene of California.

Modern porpoises (Odontoceti: Phocoenidae) are some of the smallest cetaceans and usually feed near the seafloor on small fish and cephalopods [1-3]. Within both extinct and extant phocoenids, no evidence for specialized mandibular morphology has been documented [4-7]. Here we describe a new species of extinct porpoise, Semirostrum ceruttii, from the marine Pliocene San Diego (4.2-1.6 mega-annum, Ma) and Purisima (5-2.5 Ma) formations of California. The mandibles comprise a long, fused, and nearly edentulous prognathous symphysis, extending farther beyond the rostrum than in any known mammal. Phylogenetic analyses based on morphology reconstruct Semirostrum ceruttii as sister to extant (crown) porpoise species with moderate support. We describe the spectacularly preserved holotype specimen based on computed tomography (CT) scans, which allowed visualization of the elongate mental and accessory canals within the symphysis. The elongate canals are similar to those found in Rynchops birds [8] and were likely involved in sensory function. Oblique labial wear facets present on numerous small conical mandibular teeth posterior to the symphysis suggest regular contact with benthic substrate. The unique mandibular and dental characteristics, along with robust scapulae, sternum, and unfused cervical vertebrae, support the interpretation that this species employed a form of benthic skim feeding by using its mandible to probe for and obtain prey.

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.

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.