Tobin L. Hieronymus

Palaeontological evidence for an Oligocene divergence between Old World monkeys and apes

Apes and Old World monkeys are prominent components of modern African and Asian ecosystems, yet the earliest phases of their evolutionary history have remained largely undocumented. The absence of crown catarrhine fossils older than ∼20 million years (Myr) has stood in stark contrast to molecular divergence estimates of ∼25–30 Myr for the split between Cercopithecoidea (Old World monkeys) and Hominoidea (apes), implying long ghost lineages for both clades. Here we describe the oldest known fossil ‘ape’, represented by a partial mandible preserving dental features that place it with ‘nyanzapithecine’ stem hominoids. Additionally, we report the oldest stem member of the Old World monkey clade, represented by a lower third molar. Both specimens were recovered from a precisely dated 25.2-Myr-old stratum in the Rukwa Rift, a segment of the western branch of the East African Rift in Tanzania. These finds extend the fossil record of apes and Old World monkeys well into the Oligocene epoch of Africa, suggesting a possible link between diversification of crown catarrhines and changes in the African landscape brought about by previously unrecognized tectonic activity in the East African rift system.

The evolution of mammal-like crocodyliforms in the Cretaceous Period of Gondwana

Fossil crocodyliforms discovered in recent years have revealed a level of morphological and ecological diversity not exhibited by extant members of the group. This diversity is particularly notable among taxa of the Cretaceous Period (144–65 million years ago) recovered from former Gondwanan landmasses. Here we report the discovery of a new species of Cretaceous notosuchian crocodyliform from the Rukwa Rift Basin of southwestern Tanzania. This small-bodied form deviates significantly from more typical crocodyliform craniodental morphologies, having a short, broad skull, robust lower jaw, and a dentition with relatively few teeth that nonetheless show marked heterodonty. The presence of morphologically complex, complementary upper and lower molariform teeth suggests a degree of crown–crown contact during jaw adduction that is unmatched among known crocodyliforms, paralleling the level of occlusal complexity seen in mammals and their extinct relatives. The presence of another small-bodied mammal-like crocodyliform in the Cretaceous of Gondwana indicates that notosuchians probably filled niches and inhabited ecomorphospace that were otherwise occupied by mammals on northern continents.

The facial integument of centrosaurine ceratopsids: morphological and histological correlates of novel skin structures.

The horned dinosaur Pachyhinosaurus possesses rugose bony bosses across the skull roof in lieu of the projecting bony horn cores seen in most ceratopsians. This elaboration of typical ceratopsian ornaments provides an opportunity to test hypotheses of ceratopsian facial skin morphology and function. We analyze bone morphology and histology associated with several classes of skin features in extant amniotes using a classification tree analysis. We isolate key osteological and histological correlates for unpreserved skin structures, including both a pattern of pitting and resorption characteristic of muskox (Ovibos) frontal horn boss, and a pattern of metaplastic ossification characteristic of rhinoceros nasal horn boss. We also describe correlates for other skin features, such as epidermal scales and horn sheaths. Dermatocranial elements from centrosaurine ceratopsians are then examined for the same osteological and histological correlates. From this comparison we propose that the rugose bosses that replace horn cores in many centrosaurine dinosaurs, most notably Achelousaurus and Pachyrhinosaurus, were covered by a thick pad of cornified skin derived from the caudodorsal side of the primitive horn sheath comparable to the horny boss of extant muskoxen (Ovibos). We examine extant taxa with skin morphologies similar to Pachyrhinosaurus for consistent adaptive relationships between structure and behavior. We determine that high‐energy headbutting is consistently associated with the acquisition of thick cornified pads, seen in muskoxen as well as helmeted hornbills [Buceros (=Rhinoplax) vigil] and African buffalo (Syncerus). The association of the bony ornaments of Pachyrhinosaurus with risky agonistic behaviors casts doubt on the role of species recognition as a primary selection pressure driving the diversity of all ceratopsian horns. We conclude that social selection (a broad form of intraspecific competition) is a more appropriate explanation for the diversity of centrosaurine ceratopsian ornaments in the Late Cretaceous. Anat Rec, 292:1370–1396, 2009.

Homology and Evolution of Avian Compound Rhamphothecae

ABSTRACT. We show that the topology of separate elements in avian compound rhamphothecae are strongly similar among different clades, not only in external appearance but in how these elements conform to underlying structures. We conducted a morphological survey of 81 extant bird species and tested superficial similarities in external beak morphology for substantive similarity in associated skeletal structures and nerve courses. A revised set of morphological characters for compound rhamphothecae was optimized onto three recent phylogenetic trees to assess the relationships of homology and homoplasy in rhamphothecal morphology. Osteological correlates of rhamphothecae from the extinct basal ornithurine birds Hesperornis and Ichthyornis show that compound rhamphothecae are the primitive state for the clade including extant birds (Neornithes). Simple rhamphothecae are the result of the loss of softer keratinous grooves between rhamphothecal components, and there are many examples of transitional forms between compound and simple rhamphothecae in which the grooves remain as shallow depressions without a pronounced edge. Ancestral-character-state reconstructions of rhamphothecal morphology within Neornithes also show a considerable amount of homoplasy. We suggest that frequent homoplasy in rhamphothecal morphology is the result of underlying similarity in facial development.

Cross Sectional Geometry of the Forelimb Skeleton and Flight Mode in Pelecaniform Birds

Avian wing elements have been shown to experience both dorsoventral bending and torsional loads during flapping flight. However, not all birds use continuous flapping as a primary flight strategy. The pelecaniforms exhibit extraordinary diversity in flight mode, utilizing flapping, flap‐gliding, and soaring. Here we (1) characterize the cross‐sectional geometry of the three main wing bone (humerus, ulna, carpometacarpus), (2) use elements of beam theory to estimate resistance to loading, and (3) examine patterns of variation in hypothesized loading resistance relative to flight and diving mode in 16 species of pelecaniform birds. Patterns emerge that are common to all species, as well as some characteristics that are flight‐ and diving‐mode specific. In all birds examined, the distal most wing segment (carpometacarpus) is the most elliptical (relatively high Imax/Imin) at mid‐shaft, suggesting a shape optimized to resist bending loads in a dorsoventral direction. As primary flight feathers attach at an oblique angle relative to the long axis of the carpometacarpus, they are likely responsible for inducing bending of this element during flight. Moreover, among flight modes examined the flapping group (cormorants) exhibits more elliptical humeri and carpometacarpi than other flight modes, perhaps pertaining to the higher frequency of bending loads in these elements. The soaring birds (pelicans and gannets) exhibit wing elements with near‐circular cross‐sections and higher polar moments of area than in the flap and flap‐gliding birds, suggesting shapes optimized to offer increased resistance to torsional loads. This analysis of cross‐sectional geometry has enhanced our interpretation of how the wing elements are being loaded and ultimately how they are being used during normal activities. J. Morphol., 2011.

Evolutionary aspects of the development of teeth and baleen in the bowhead whale.

In utero, baleen whales initiate the development of several dozens of teeth in upper and lower jaws. These tooth germs reach the bell stage and are sometimes mineralized, but toward the end of prenatal life they are resorbed and no trace remains after birth. Around the time that the germs disappear, the keratinous baleen plates start to form in the upper jaw, and these form the food‐collecting mechanism. Baleen whale ancestors had two generations of teeth and never developed baleen, and the prenatal teeth of modern fetuses are usually interpreted as an evolutionary leftover. We investigated the development of teeth and baleen in bowhead whale fetuses using histological and immunohistochemical evidence. We found that upper and lower dentition initially follow similar developmental pathways. As development proceeds, upper and lower tooth germs diverge developmentally. Lower tooth germs differ along the length of the jaw, reminiscent of a heterodont dentition of cetacean ancestors, and lingual processes of the dental lamina represent initiation of tooth bud formation of replacement teeth. Upper tooth germs remain homodont and there is no evidence of a secondary dentition. After these germs disappear, the oral epithelium thickens to form the baleen plates, and the protein FGF‐4 displays a signaling pattern reminiscent of baleen plates. In laboratory mammals, FGF‐4 is not involved in the formation of hair or palatal rugae, but it is involved in tooth development. This leads us to propose that the signaling cascade that forms teeth in most mammals has been exapted to be involved in baleen plate ontogeny in mysticetes.

Macroevolutionary developmental biology: Embryos, fossils, and phylogenies

The field of evolutionary developmental biology is broadly focused on identifying the genetic and developmental mechanisms underlying morphological diversity. Connecting the genotype with the phenotype means that evo‐devo research often considers a wide range of evidence, from genetics and morphology to fossils. In this commentary, we provide an overview and framework for integrating fossil ontogenetic data with developmental data using phylogenetic comparative methods to test macroevolutionary hypotheses. We survey the vertebrate fossil record of preserved embryos and discuss how phylogenetic comparative methods can integrate data from developmental genetics and paleontology. Fossil embryos provide limited, yet critical, developmental data from deep time. They help constrain when developmental innovations first appeared during the history of life and also reveal the order in which related morphologies evolved. Phylogenetic comparative methods provide a powerful statistical approach that allows evo‐devo researchers to infer the presence of nonpreserved developmental traits in fossil species and to detect discordant evolutionary patterns and processes across levels of biological organization. Developmental Dynamics 244:1184–1192, 2015.

Qualitative skeletal correlates of wing shape in extant birds (Aves: Neoaves)

BackgroundAmong living fliers (birds, bats, and insects), birds display relatively high aspect ratios, a dimensionless shape variable that distinguishes long and narrow vs. short and broad wings. Increasing aspect ratio results in a functional tradeoff between low induced drag (efficient cruise) and increased wing inertia (difficult takeoff). Given the wide scope of its functional effects, the pattern of aspect ratio evolution is an important factor that contributes to the substantial ecological and phylogenetic diversity of living birds. However, because the feathers that define the wingtip (and hence wingspan and aspect ratio) often do not fossilize, resolution in the pattern of avian wing shape evolution is obscured by missing information. Here I use a comparative approach to investigate the relationship between skeletal proxies of flight feather attachment and wing shape.ResultsAn accessory lobe of the internal index process of digit II-1, a bony correlate of distal primary attachment, shows weak but statistically significant relationships to aspect ratio and mass independent of other skeletal morphology. The dorsal phalangeal fossae of digit II-1, which house distal primaries VIII and IX, also show a trend of increased prominence with higher aspect ratio. Quill knobs on the ulna are examined concurrently, but do not show consistent signal with respect to wing shape.ConclusionsAlthough quill knobs are cited as skeletal correlates of flight performance in birds, their relationship to wing shape is inconsistent among extant taxa, and may reflect diverging selection pressures acting on a conserved architecture. In contrast, correlates of distal primary feather attachment on the major digit show convergent responses to increasing aspect ratio. In light of the diversity of musculoskeletal and integumentary mophology that underlies wing shape in different avian clades, it is unlikely that a single skeletal feature will show consistent predictive power across Neoaves. Confident inference of wing shape in basal ornithurine birds will require multiple lines of evidence, together with an understanding of clade-specific evolutionary trends within the crown.

A comparison of postnatal arterial patterns in a growth series of giraffe (Artiodactyla: Giraffa camelopardalis)

Nearly all living artiodactyls (even-toed ungulates) possess a derived cranial arterial pattern that is highly distinctive from most other mammals. Foremost among a suite of atypical arterial configurations is the functional and anatomical replacement of the internal carotid artery with an extensive, subdural arterial meshwork called the carotid rete. This interdigitating network branches from the maxillary artery and is housed within the cavernous venous sinus. As the cavernous sinus receives cooled blood draining from the nasal mucosa, heat rapidly dissipates across the high surface area of the rete to be carried away from the brain by the venous system. This combination yields one of the most effective mechanisms of selective brain cooling. Although arterial development begins from the same embryonic scaffolding typical of mammals, possession of a rete is typically accompanied by obliteration of the internal carotid artery. Among taxa with available ontogenetic data, the point at which the internal carotid obliterates is variable throughout development. In small-bodied artiodactyls, the internal carotid typically obliterates prior to parturition, but in larger species, the vessel may remain patent for several years. In this study, we use digital anatomical data collection methods to describe the cranial arterial patterns for a growth series of giraffe (Giraffa camelopardalis), from parturition to senescence. Giraffes, in particular, have unique cardiovascular demands and adaptations owing to their exceptional body form and may not adhere to previously documented stages of cranial arterial development. We find the carotid arterial system to be conserved between developmental stages and that obliteration of the giraffe internal carotid artery occurs prior to parturition.

Flight feather attachment in rock pigeons (Columba livia): covert feathers and smooth muscle coordinate a morphing wing.

Mechanisms for passively coordinating forelimb movements and flight feather abduction and adduction have been described separately from both in vivo and ex vivo studies. Skeletal coordination has been identified as a way for birds to simplify the neuromotor task of controlling flight stroke, but an understanding of the relationship between skeletal coordination and the coordination of the aerodynamic control surface (the flight feathers) has been slow to materialize. This break between the biomechanical and aerodynamic approaches – between skeletal kinematics and airfoil shape – has hindered the study of dynamic flight behaviors. Here I use dissection and histology to identify previously overlooked interconnections between musculoskeletal elements and flight feathers. Many of these structures are well‐placed to directly link elements of the passive musculoskeletal coordination system with flight feather movements. Small bundles of smooth muscle form prominent connections between upper forearm coverts (deck feathers) and the ulna, as well as the majority of interconnections between major flight feathers of the hand. Abundant smooth muscle may play a role in efficient maintenance of folded wing posture, and may also provide an autonomically regulated means of tuning wing shape and aeroelastic behavior in flight. The pattern of muscular and ligamentous linkages of flight feathers to underlying muscle and bone may provide predictable passive guidance for the shape of the airfoil during flight stroke. The structures described here provide an anatomical touchstone for in vivo experimental tests of wing surface coordination in an extensively researched avian model species.