Willem J. Hillenius

The evolution of nasal turbinates and mammalian endothermy

Complex nasal turbinal bones are associated with reduction of respiratory water loss in desert mammals and have previously been described as an adaptation to xeric conditions. However, complex turbinates are found in virtually all mammals. Experimental data presented here indicate that turbinates also substantially reduce respiratory water loss in five species of small mammals from relatively mesic environments. The data support the conclusion that turbinates did not evolve primarily as an adaptation to particular environmental conditions, but in relation to high ventilation rates, typical of all mammals. Complex turbinates appear to be an ancient attribute of mammals and may have originated among the therapsid ancestors of mammals, in relation to elevated ventilation rates and the evolution of endothermy.

The Evolution of Endothermy in Terrestrial Vertebrates: Who? When? Why?

Avian and mammalian endothermy results from elevated rates of resting, or routine, metabolism and enables these animals to maintain high and stable body temperatures in the face of variable ambient temperatures. Endothermy is also associated with enhanced stamina and elevated capacity for aerobic metabolism during periods of prolonged activity. These attributes of birds and mammals have greatly contributed to their widespread distribution and ecological success. Unfortunately, since few anatomical/physiological attributes linked to endothermy are preserved in fossils, the origin of endothermy among the ancestors of mammals and birds has long remained obscure. Two recent approaches provide new insight into the metabolic physiology of extinct forms. One addresses chronic (resting) metabolic rates and emphasizes the presence of nasal respiratory turbinates in virtually all extant endotherms. These structures are associated with recovery of respiratory heat and moisture in animals with high resting metabolic rates. The fossil record of nonmammalian synapsids suggests that at least two Late Permian lineages possessed incipient respiratory turbinates. In contrast, these structures appear to have been absent in dinosaurs and nonornithurine birds. Instead, nasal morphology suggests that in the avian lineage, respiratory turbinates first appeared in Cretaceous ornithurines. The other approach addresses the capacity for maximal aerobic activity and examines lung structure and ventilatory mechanisms. There is no positive evidence to support the reconstruction of a derived, avian‐like parabronchial lung/air sac system in dinosaurs or nonornithurine birds. Dinosaur lungs were likely heterogenous, multicameral septate lungs with conventional, tidal ventilation, although evidence from some theropods suggests that at least this group may have had a hepatic piston mechanism of supplementary lung ventilation. This suggests that dinosaurs and nonornithurine birds generally lacked the capacity for high, avian‐like levels of sustained activity, although the aerobic capacity of theropods may have exceeded that of extant ectotherms. The avian parabronchial lung/air sac system appears to be an attribute limited to ornithurine birds.

The metabolic status of some Late Cretaceous dinosaurs

Analysis of the nasal region in fossils of three theropod dinosaurs (Nanotyrannus, Ornithomimus, and Dromaeosaurus) and one ornithischian dinosaur (Hypacrosaurus) showed that their metabolic rates were significantly lower than metabolic rates in modern birds and mammals. In extant endotherms and ectotherms, the cross-sectional area of the nasal passage scales approximately with increasing body mass M at M0.72. However, the cross-sectional area of nasal passages in endotherms is approximately four times that of ectotherms. The dinosaurs studied here have narrow nasal passages that are consistent with low lung ventilation rates and the absence of respiratory turbinates.

Cursoriality in bipedal archosaurs

Modern birds have markedly foreshortened tails and their body mass is centred anteriorly, near the wings. To provide stability during powered flight, the avian centre of mass is far from the pelvis, which poses potential balance problems for cursorial birds. To compensate, avians adapted to running maintain the femur subhorizontally, with its distal end situated anteriorly, close to the animals centre of mass; stride generation stems largely from parasagittal rotation of the lower leg about the knee joint. In contrast, bipedal dinosaurs had a centre of mass near the hip joint and rotated the entire hindlimb during stride generation. Here we show that these contrasting styles of cursoriality are tightly linked to longer relative total hindlimb length in cursorial birds than in bipedal dinosaurs. Surprisingly, Caudipteryx , described as a theropod dinosaur, possessed an anterior centre of mass and hindlimb proportions resembling those of cursorial birds. Accordingly, Caudipteryx probably used a running mechanism more similar to that of modern cursorial birds than to that of all other bipedal dinosaurs. These observations provide valuable clues about cursoriality in Caudipteryx , but may also have implications for interpreting the locomotory status of its ancestors.

Septomaxilla of nonmammalian synapsids: Soft-tissue correlates and a new functional interpretation

The function of the septomaxilla of nonmammalian synapsids has long been problematic. Distinctive features of this bone, including a prominent intranarial process and a septomaxillary canal and foramen, are characteristic of pelycosaurs and nonmammalian therapsids, but are lost in their mammalian descendants. Numerous contradictory reconstructions have been proposed for the soft anatomy associated with the septomaxilla of nonmammalian synapsids. This review supports the following conclusions: 1) No particular correlation exists between the septomaxilla and the vomeronasal organ (VNO), and the most likely location for the VNO is on the dorsal surface of the palatal process of the vomer; 2) The most likely occupant of the septomaxillary canal is the nasolacrimal duct, which opened either anterior or medial to the intranarial process, near the opening of the VNO duct; and 3) The occupant of the septomaxillary foramen remains uncertain. These conclusions suggest that the functional significance of the septomaxilla in the nonmammalian synapsids is tied to that of the nasolacrimal duct. The association of this duct and the VNO in these animals resembles the condition in Recent amphibians and lepidosaurs, in which the nasolacrimal duct supplies orbital fluids to the VNO, apparently to enhance vomeronasal function. The peculiar shape of the synapsid septomaxilla may have served to collect vomeronasal odor molecules. The changes of the septomaxilla in early mammals, and its nearly complete loss in extant mammals, are probably correlated with a dissociation of the nasolacrimal duct and VNO, and functional changes in both structures. J. Morphol. 245:29–50, 2000

Towards a comprehensive model of feather regeneration

Understanding of the regeneration of feathers, despite a 140 year tradition of study, has remained substantially incomplete. Moreover, accumulated errors and mis‐statements in the literature have confounded the intrinsic difficulties in describing feather regeneration. Lack of allusion to Rudalls (Rudall [ 1947 ] Biochem Biophys Acta 1:549–562) seminal X‐ray diffraction study that revealed two distinct keratins, β‐ and α‐, in a mature feather, is one of the several examples where lack of citation long inhibited progress in understanding. This article reviews and reevaluates the available literature and provides a synthetic, comprehensive, morphological model for the regeneration of a generalized, adult contour feather. Particular attention is paid to several features that have previously been largely ignored. Some of these, such as the β‐keratogenic sheath and the α‐keratogenic, supra‐umbilical, pulp caps, are missing from mature, functional feathers sensu stricto because they are lost through preening, but these structures nevertheless play a critical role in development. A new developmental role for a tissue unique to feathers, the medullary pith of the rachis and barb rami, and especially its importance in the genesis of the superior umbilical region (SUR) that forms the transition from the spathe (rachis and vanes) to the calamus, is described. It is postulated that feathers form through an intricate interplay between cyto‐ and histodifferentiative processes, determined by patterning signals that emanate from the dermal core, and a suite of interacting biomechanical forces. Precisely regulated patterns of loss of intercellular adhesivity appear to be the most fundamental aspect of feather morphogenesis and regeneration: rather than a hierarchically branched structure, it appears more appropriate to conceive of feathers as a sheet of mature keratinocytes that is “full of holes. J. Morphol. 2009.

Getting Warmer, Getting Colder: Reconstructing Crocodylomorph Physiology

Seymour et al. (2004) deserve credit for a provocative article. The question they raise—why crocodilians have a four-chambered heart when other reptiles get along with just three—is valid and interesting, and it deserves far more attention than it has thus far received. However, their suggestion that crocodilians once had endothermic ancestors and reverted back to ectothermy when they invaded aquatic niches is less than compelling for a number of reasons. Seymour et al. actually deal with two separate questions: What was the metabolic status of the early crocodylomorphs? and What selective factors might account for the attributes of modern crocodilians and the transformation that distinguishes this lineage from the ancestral forms? With regard to the first question, they argue not merely that crocodilian biology was modified from that of their Triassic and Early Jurassic ancestors but explicitly that these ancestors had attained full endothermic status. Unfortunately, they provide no compelling evidence that endothermy was in fact present in the ancestral forms. The authors point to the agile body sizes, delicate bones, and erect, possibly bipedal gait of early crocodylomorphs as evidence of a terrestrial, cursorial lifestyle and then postulate that “upright stance and the capacity for highly active, terrestrial behavior are characteristic of endotherms” (p. 1054). However, as the authors themselves acknowledge, attributes such as posture, gait, and bone structure are not compelling evidence of endothermy (in addition to the reviews cited by the authors, see also Farlow 1990; Farlow et al. 1995; Ruben 1995; Chinsamy and Hillenius 2004; Hillenius and Ruben 2004). Early croco-

Breathing in a box: Constraints on lung ventilation in giant pterosaurs

Pterosaurs were the first vertebrates to achieve active flight, with some derived forms reaching enormous size. Accumulating fossil evidence confirms earlier indications that selection for large size in these flying forms resulted in a light, yet strong skeleton characterized by fusion of many bones of the trunk. However, this process also added mechanical constraints on the mobility of the thorax of large pterosaurs that likely limited the options available for lung ventilation. We present an alternative hypothesis to recent suggestions of an avian‐like mechanism of costosternal pumping as the primary means of aspiration. An analysis of the joints among the vertebrae, ribs, sternum, and pectoral girdle of large pterosaurs indicates limited mobility of the ribcage and sternum. Comparisons with modes of lung ventilation in extant amniotes suggests that the stiffened thorax, coupled with mobile gastralia and prepubic bones, may be most consistent with an extracostal mechanism for lung ventilation in large pterodactyloids, perhaps similar to a crocodile‐like visceral displacement system Anat Rec, 297:2233–2253, 2014.

Is It or Isn't It? A Reexamination of the Anterior Orbital Glands of the Fat-Tailed Dunnart Sminthopsis Crassicaudata (Dasyuridae: Marsupiala) and a Reevaluation of Definitions for the Harderian Gland

The anterior orbital glands of tetrapods, which include the Harderian and nictitans glands, can usually be differentiated either anatomically (nictitans gland is more anterior) or histochemically (Harderian gland secretes lipids). However, conflicting statements exist in the literature about the presence and identity of these glands. Two previous studies on Sminthopsis crassicaudata (Dasyuridae: Marsupiala) either failed to note any anterior ocular glands or used no histochemical analyses. This study reexamined the structure of the anterior orbital glands of S. crassicaudata. Histological, histochemical, and ultrastructural examination revealed three glandular units: two of which are located superficially in the nictitating membrane, the third lying deeper in the connective tissue. The ducts of these three glandular units all open onto the corneal aspect of the nictitating membrane. These cells contain mainly serous granules with sparse intracellular lipid droplets. The nomenclature of these structures depends upon the definition used. According to the anatomical definition, S. crassicaudata has two glands: anteriorly the nictitans and posteriorly the Harderian gland. In contrast, if the histochemical definition is used, there is only one gland, but its precise identity cannot be confirmed until the role of the lipid droplets is established. Moreover, the histochemical definition poses additional problems with respect to the mechanism of secretion, multiple secretions, and glandular plasticity. Finally, the unitary definition identifies one deeply subdivided gland with an anterior and a posterior lobe in S. crassicaudata. This last definition is broad enough to accommodate a wide level of anatomical variation in the anterior ocular glands of tetrapods. Anat Rec 293:1449–1454, 2010.

Development of the nasolacrimal apparatus in the Mongolian gerbil (Meriones unguiculatus), with notes on network topology and function

The nasolacrimal apparatus (NLA) is a multicomponent functional system comprised of multiple orbital glands (up to four larger multicellular exocrine structures), a nasal chemosensory structure (vomeronasal organ: VNO), and a connecting duct (nasolacrimal duct: NLD). Although this system has been described in all tetrapod vertebrate lineages, albeit not always with all three main components present, considerably less is known about its ontogeny. The Mongolian gerbil (Meriones unguiculatus) is a common lab rodent in which the individual components of the adult NLA have been well studied, but as yet nothing is known about the ontogeny of the NLA. In this study, serial sections of 15 fetal and three adult Mongolian gerbil heads show that the development of the NLA falls into three fetal stages: inception (origin of all features), elongation (lengthening of all features), and expansion (widening of all features). No postnatal or juvenile specimens were observed in this study, but considerable growth evidently occurs before the final adult condition is reached. The development of the orbital glands and the VNO in the Mongolian gerbil is largely consistent with those in other mammals, despite a slight nomenclatural conundrum for the anterior orbital glands. However, the Mongolian gerbil NLD follows a more circuitous route than in other tetrapods, due mainly to the convoluted arrangement of the narial cartilages, the development of a pair of enlarged incisors as well as an enlarged infraorbital foramen. The impact of these associated features on the ontogeny and phylogeny of the NLA could be examined through the approach of network science. This approach allows for the incorporation of adaptations to specific lifestyles as potential explanations for the variation observed in the NLA across different tetrapod clades. J. Morphol. 276:1005–1024, 2015.