Vertebrate Life Research Articles

Feeding live invertebrate prey in zoos and aquaria: Are there welfare concerns?

Invertebrates constitute more than 90% of all species on earth, however, as a rule, humans do not regard invertebrates as creatures that can suffer and they are generally seen as creatures that should be eliminated. As a result, the importance of their welfare may be grossly unappreciated. For instance, the feeding of live food is often viewed as a good method of enrichment and invertebrates are commonly used as live prey in many zoological facilities. As a result, zoos may send mixed messages to their patrons in that welfare is considered only for the invertebrates that are part of their zoological collection and not necessarily for the invertebrates used as feed. Research indicates that many invertebrates possess nociceptors, opioid receptors, and demonstrate behavioral responses indicative of pain sensation. In addition, in some taxa, there may be evidence of higher cognitive functions such as emotions and learning, although studies in this area of research are preliminary and sparse. Therefore, the possibility for suffering exists in many invertebrate species and as such, zoological facilities have an ethical responsibility to take their welfare into consideration. This paper discusses the current research regarding invertebrates' capacity for suffering and discusses methods facilities can use to improve the welfare of their invertebrate live prey.

High-altitude champions: birds that live and migrate at altitude.

High altitude is physiologically challenging for vertebrate life for many reasons, including hypoxia (low environmental oxygen); yet, many birds thrive at altitude. Compared with mammals, birds have additional enhancements to their oxygen transport cascade, the conceptual series of steps responsible for acquiring oxygen from the environment and transporting it to the mitochondria. These adaptations have allowed them to inhabit a number of high-altitude regions. Waterfowl are a taxon prolific at altitude. This minireview explores the physiological responses of high-altitude waterfowl (geese and ducks), comparing the strategies of lifelong high-altitude residents to those of transient high-altitude performers, providing insight into how birds champion high-altitude life. In particular, this review highlights and contrasts the physiological hypoxia responses of bar-headed geese (Anser indicus), birds that migrate biannually through the Himalayas (4,500-6,500 m), and Andean geese (Chloephaga melanoptera), lifelong residents of the Andes (4,000-5,500 m). These two species exhibit markedly different ventilatory and cardiovascular strategies for coping with hypoxia: bar-headed geese robustly increase convective oxygen transport elements (i.e., heart rate and total ventilation) whereas Andean geese rely predominantly on enhancements that are likely morphological in origin (i.e., increases in lung oxygen diffusion and cardiac stroke volume). The minireview compares the short- and long-term cardiovascular and ventilatory trade-offs of these different physiological strategies and offers hypotheses surrounding their origins. It also draws parallels to high-altitude human physiology and research, and identifies a number of areas of further research. The field of high-altitude avian physiology offers a unique and broadly applicable insight into physiological enhancements in hypoxia.

Regulation of life span by the gut microbiota in the short-lived African turquoise killifish.

Gut bacteria occupy the interface between the organism and the external environment, contributing to homeostasis and disease. Yet, the causal role of the gut microbiota during host aging is largely unexplored. Here, using the African turquoise killifish (Nothobranchius furzeri), a naturally short-lived vertebrate, we show that the gut microbiota plays a key role in modulating vertebrate life span. Recolonizing the gut of middle-age individuals with bacteria from young donors resulted in life span extension and delayed behavioral decline. This intervention prevented the decrease in microbial diversity associated with host aging and maintained a young-like gut bacterial community, characterized by overrepresentation of the key genera Exiguobacterium, Planococcus, Propionigenium and Psychrobacter. Our findings demonstrate that the natural microbial gut community of young individuals can causally induce long-lasting beneficial systemic effects that lead to life span extension in a vertebrate model.

Recent Progress and Future Prospects in Fossil Xenarthran Studies, with Emphasis on Current Methodology in Sloth Taxonomy

Among the several positive developments in xenarthran studies over the past 20 years have been the training of and active participation by many new researchers, prospecting of previously unexplored or poorly known localities in northwestern South America, pioneering and expansion of paleobiological studies, and revisiting of classic sites in Argentine Patagonia. While these developments have resulted in much new information, including description of new taxa, correlation with faunas previously known from the classic regions of Argentina and Brazil, and enhanced understanding of the modes of life of extinct vertebrates, there remain several areas of research that require more effort from our community. Among these are the need for improved descriptions and illustration of skeletal structures such as those of the auditory and basicranial regions of the skull and the vertebral and autopodial elements. Although perhaps the more difficult and less well-documented regions, much is to be gained for phylogenetic and taxonomic analyses by enhanced efforts in these regards, and several recent publications help provide standard references to their description and illustration. Also, as alpha taxonomy forms the foundation of higher-level analyses, more attention must be paid to intraspecific variation and the quality of specimens in the recognition of diagnostic characters in descriptions of new taxa. Critical assessment of such variation and specimen choice in several recently erected taxa is conducted here, with the goal of inspiring more cautious assessment of characters and relying on a population rather than typological approach in reaching decisions on potential new taxa.

Pdgf signalling guides neural crest contribution to the haematopoietic stem cell specification niche.

Haematopoietic stem cells (HSCs) support maintenance of the haematopoietic and immune systems throughout the life of vertebrates, and are the therapeutic component of bone marrow transplants. Understanding native specification of HSCs, to uncover key signals that might help improve in vitro directed differentiation protocols, has been a longstanding biomedical goal. The current impossibility of specifying true HSCs in vitro suggests that key signals remain unknown. We speculated that such signals might be presented by surrounding “niche” cells, but no such cells have been defined. Here we demonstrate in zebrafish, that trunk neural crest (NC) physically associate with HSC precursors in the dorsal aorta (DA) just prior to initiation of the definitive haematopoietic programme. Preventing association of the NC with the DA leads to loss of HSCs. Our results define NC as key cellular components of the HSC specification niche that can be profiled to identify unknown HSC specification signals.

Supporting cells remove and replace sensory receptor hair cells in a balance organ of adult mice.

Vestibular hair cells in the inner ear encode head movements and mediate the sense of balance. These cells undergo cell death and replacement (turnover) throughout life in non-mammalian vertebrates. However, there is no definitive evidence that this process occurs in mammals. We used fate-mapping and other methods to demonstrate that utricular type II vestibular hair cells undergo turnover in adult mice under normal conditions. We found that supporting cells phagocytose both type I and II hair cells. Plp1-CreERT2-expressing supporting cells replace type II hair cells. Type I hair cells are not restored by Plp1-CreERT2-expressing supporting cells or by Atoh1-CreERTM-expressing type II hair cells. Destruction of hair cells causes supporting cells to generate 6 times as many type II hair cells compared to normal conditions. These findings expand our understanding of sensorineural plasticity in adult vestibular organs and further elucidate the roles that supporting cells serve during homeostasis and after injury.

Comparative Physiology of Energy Metabolism: Fishing for Endocrine Signals in the Early Vertebrate Pool.

Energy is the common currency of life. To guarantee a homeostatic supply of energy, multiple neuro-endocrine systems have evolved in vertebrates; systems that regulate food intake, metabolism, and distribution of energy. Even subtle (lasting) dysregulation of the delicate balance of energy intake and expenditure may result in severe pathologies. Feeding-related pathologies have fueled research on mammals, including of course the human species. The mechanisms regulating food intake and body mass are well-characterized in these vertebrates. The majority of animal life is ectothermic, only birds and mammals are endotherms. What can we learn from a (comparative) study on energy homeostasis in teleostean fishes, ectotherms, with a very different energy budget and expenditure? We present several adaptation strategies in fish. In recent years, the components that regulate food intake in fishes have been identified. Although there is homology of the major genetic machinery with mammals (i.e., there is a vertebrate blueprint), in many cases this does not imply analogy. Although both mammals and fish must gain their energy from food, the expenditure of the energy obtained is different. Mammals need to spend vast amounts of energy to maintain body temperature; fishes seem to utilize a broader metabolic range to their advantage. In this review, we briefly discuss ecto- and endothermy and their consequences for energy balance. Next, we argue that the evolution of endothermy and its (dis-)advantages may explain very different strategies in endocrine regulation of energy homeostasis among vertebrates. We follow a comparative and evolutionary line of thought: we discuss similarities and differences between fish and mammals. Moreover, given the extraordinary radiation of teleostean fishes (with an estimated number of 33,400 contemporary species, or over 50% of vertebrate life forms), we also compare strategies in energy homeostasis between teleostean species. We present recent developments in the field of (neuro)endocrine regulation of energy balance in teleosts, with a focus on leptin.

Homeostasis and the concept of 'interstitial fluids hierarchy': Relevance of cerebrospinal fluid sodium concentrations and brain temperature control(Review).

In this review, the aspects and further developments of the concept of homeostasis are discussed also in the perspective of their possible impact in the clinical practice, particularly as far as psychic homeostasis is concerned. A brief historical survey and comments on the concept of homeostasis and allostasis are presented to introduce our proposal that is based on the classical assumption of the interstitial fluid (ISF) as the internal medium for multicellular organisms. However, the new concept of a hierarchic role of ISF of the various organs is introduced. Additionally, it is suggested that particularly for some chemico-physical parameters, oscillatory rhythms within their proper set-ranges should be considered a fundamental component of homeostasis. Against this background, we propose that the brain ISF has the highest hierarchic role in human beings, providing the optimal environment, not simply for brain cell survival, but also for brain complex functions and the oscillatory rhythms of some parameters, such as cerebrospinal fluid sodium and brain ISF pressure waves, which may play a crucial role in brain physio-pathological states. Thus, according to this proposal, the brain ISF represents the real internal medium since the maintenance of its dynamic intra-set-range homeostasis is the main factor for a free and independent life of higher vertebrates. Furthermore, the evolutionary links between brain and kidney and their synergistic role in H2O/Na balance and brain temperature control are discussed. Finally, it is surmised that these two interrelated parameters have deep effects on the Central Nervous System (CNS) higher integrative actions such those linked to psychic homeostasis.

Functional (Secondary) Adaptation to an Aquatic Life in Vertebrates: An Introduction to the Symposium.

One of the great transformations in evolution of vertebrates has been the return to the aquatic environment after the conquest of terrestrial ecosystems. With structural and physiological characteristics adapted to function on land, the various non-piscine taxa had to modify these characteristics to perform in water. Secondary aquatic vertebrates successfully transformed mechanisms for feeding, locomotion, osmoregulation, and sensory systems to function and thrive in an aqueous environment. This symposium emphasized the changes that had to be acquired to operate in the water with morphologies previously evolved to function on land. It brought together researchers working on different aspects of functional biology and on various taxa in order to illustrate the diversity in the required adaptations: the numerous convergences as well as the specific adaptive traits. The collection of talks, posters, and of the contributions to this special volume highlights recent advances in the understanding of the functional adaptations associated to secondary adaptation to an aquatic lifestyle in vertebrates.

The Mating System and Reproductive Life History of Female Timber Rattlesnakes in Northwestern Arkansas

Vertebrate mating strategies and life history patterns show great variation within and among species. Variation in reproductive tactics results from a combination of phylogenetic and environmental factors, and detailed natural and life history data among taxa are required to provide a comparative perspective or to infer evolutionary forces. Collection of such data in secretive species can often only be accomplished through long-term monitoring or the use of molecular tools. We used a combination of monitoring via radiotelemetry and microsatellite DNA markers to describe the reproductive ecology of a population of Timber Rattlesnakes, Crotalus horridus, in northwestern Arkansas. Female C. horridus in northwestern Arkansas were smaller at maturity and produce small litters compared to most estimates for other populations. Female snout–vent length and not the body condition of preparturient females was positively related to litter size and total litter mass. Both pregnant females and females found in associa...

A flexible, multilayered protein scaffold maintains the slit in between glomerular podocytes.

Vertebrate life critically depends on renal filtration and excretion of low molecular weight waste products. This process is controlled by a specialized cell-cell contact between podocyte foot processes: the slit diaphragm (SD). Using a comprehensive set of targeted KO mice of key SD molecules, we provided genetic, functional, and high-resolution ultrastructural data highlighting a concept of a flexible, dynamic, and multilayered architecture of the SD. Our data indicate that the mammalian SD is composed of NEPHRIN and NEPH1 molecules, while NEPH2 and NEPH3 do not participate in podocyte intercellular junction formation. Unexpectedly, homo- and heteromeric NEPHRIN/NEPH1 complexes are rarely observed. Instead, single NEPH1 molecules appear to form the lower part of the junction close to the glomerular basement membrane with a width of 23 nm, while single NEPHRIN molecules form an adjacent junction more apically with a width of 45 nm. In both cases, the molecules are quasiperiodically spaced 7 nm apart. These structural findings, in combination with the flexibility inherent to the repetitive Ig folds of NEPHRIN and NEPH1, indicate that the SD likely represents a highly dynamic cell-cell contact that forms an adjustable, nonclogging barrier within the renal filtration apparatus.

GR SUMOylation and formation of an SUMO-SMRT/NCoR1-HDAC3 repressing complex is mandatory for GC-induced IR nGRE-mediated transrepression.

Unique among the nuclear receptor superfamily, the glucocorticoid (GC) receptor (GR) can exert three distinct transcriptional regulatory functions on binding of a single natural (cortisol in human and corticosterone in mice) and synthetic [e.g., dexamethasone (Dex)] hormone. The molecular mechanisms underlying GC-induced positive GC response element [(+)GRE]-mediated activation of transcription are partially understood. In contrast, these mechanisms remain elusive for GC-induced evolutionary conserved inverted repeated negative GC response element (IR nGRE)-mediated direct transrepression and for tethered indirect transrepression that is mediated by DNA-bound NF-κB/activator protein 1 (AP1)/STAT3 activators and instrumental in GC-induced anti-inflammatory activity. We demonstrate here that SUMOylation of lysine K293 (mouse K310) located within an evolutionary conserved sequence in the human GR N-terminal domain allows the formation of a GR-small ubiquitin-related modifiers (SUMOs)-NCoR1/SMRT-HDAC3 repressing complex mandatory for GC-induced IR nGRE-mediated direct repression in vitro, but does not affect transactivation. Importantly, these results were validated in vivo: in K310R mutant mice and in mice ablated selectively for nuclear receptor corepressor 1 (NCoR1)/silencing mediator for retinoid or thyroid-hormone receptors (SMRT) corepressors in skin keratinocytes, Dex-induced direct repression and the formation of repressing complexes on IR nGREs were impaired, whereas transactivation was unaffected. In mice selectively ablated for histone deacetylase 3 (HDAC3) in skin keratinocytes, GC-induced direct repression, but not bindings of GR and of corepressors NCoR1/SMRT, was abolished, indicating that HDAC3 is instrumental in IR nGRE-mediated repression. Moreover, we demonstrate that the binding of HDAC3 to IR nGREs in vivo is mediated through interaction with SMRT/NCoR1. We also show that the GR ligand binding domain (LBD) is not required for SMRT-mediated repression, which can be mediated by a LBD-truncated GR, whereas it is mandatory for NCoR1-mediated repression through an interaction with K579 in the LBD.

The Strawberry Bank Lagerstätte reveals insights into Early Jurassic life

The Strawberry Bank Lagerstätte provides a rich insight into Early Jurassic marine vertebrate life, revealing exquisite anatomical detail of marine reptiles and large pachycormid fishes thanks to exceptional preservation, and especially the uncrushed, 3D nature of the fossils. The site documents a fauna of Early Jurassic nektonic marine animals (five species of fishes, one species of marine crocodilian, two species of ichthyosaurs, cephalopods and crustaceans), but also over 20 species of insects. Unlike other fossil sites of similar age, the 3D preservation at Strawberry Bank provides unique evidence on palatal and braincase structures in the fishes and reptiles. The age of the site is important, documenting a marine ecosystem during recovery from the end-Triassic mass extinction, but also exactly coincident with the height of the Toarcian Oceanic Anoxic Event, a further time of turmoil in evolution.

A vertebrate trackway from the Twyfelfontein Formation (Lower Cretaceous), Damaraland, Namibia

A trackway of 22 footprints is the first definite evidence of vertebrate life from the Main Aeolian Unit of the Twyfelfontein Formation (Lower Cretaceous), Kunene region, Northwestern Namibia. Footprints were left on the lee slope of an ancient dune in a hyper-arid, erg-dominated paleo environment. The new material is reminiscent of the Mesozoic ichnotaxon Brasilichnium, which is exclusively found on the slip face of sand dunes, from both South and North America. The Twyfelfontein Formation is considered a lateral equivalent of the Brazilian Botucatu Formation in which Brasilichnium is a common trace fossil, but correlation was formerly based exclusively on sedimentologic and lithostratigraphic homologies. Aside from being the first vertebrate evidence from the Cretaceous of Namibia, and possibly the first African Brasilichnium, this new find enforces the correlation between the Botucatu and the Twyfelfontein formations.

Palaeontology: Tracing the backbone in China's rocks

Xu Xing relishes a bilingual book on the evolution of vertebrate life in his fabulously fossil-rich country.

Hemoglobin βCys93 is essential for cardiovascular function and integrated response to hypoxia

Oxygen delivery by Hb is essential for vertebrate life. Three amino acids in Hb are strictly conserved in all mammals and birds, but only two of those, a His and a Phe that stabilize the heme moiety, are needed to carry O2. The third conserved residue is a Cys within the β-chain (βCys93) that has been assigned a role in S-nitrosothiol (SNO)-based hypoxic vasodilation by RBCs. Under this model, the delivery of SNO-based NO bioactivity by Hb redefines the respiratory cycle as a triune system (NO/O2/CO2). However, the physiological ramifications of RBC-mediated vasodilation are unknown, and the apparently essential nature of βCys93 remains unclear. Here we report that mice with a βCys93Ala mutation are deficient in hypoxic vasodilation that governs blood flow autoregulation, the classic physiological mechanism that controls tissue oxygenation but whose molecular basis has been a longstanding mystery. Peripheral blood flow and tissue oxygenation are decreased at baseline in mutant animals and decline excessively during hypoxia. In addition, βCys93Ala mutation results in myocardial ischemia under basal normoxic conditions and in acute cardiac decompensation and enhanced mortality during transient hypoxia. Fetal viability is diminished also. Thus, βCys93-derived SNO bioactivity is essential for tissue oxygenation by RBCs within the respiratory cycle that is required for both normal cardiovascular function and circulatory adaptation to hypoxia.

Glucocorticoid receptor function in health and disease.

Glucocorticoid hormones are essential for life in vertebrates. They act through the glucocorticoid receptor (GR), which is expressed in virtually all cells of the human body. Yet the actions of glucocorticoids (GCs) are specific to particular cell types. Broadly GCs regulate carbohydrate metabolism, inflammation, stress and cell fate. Synthetic GCs are widely used in medicine and are by far the most frequent cause of Cushing's syndrome in routine practice. The advent of novel drugs targeting the GR offers new opportunities to treat patients with immune, or malignant disease, and may also offer new opportunities to manage patients with adrenal insufficiency also. This review covers the latest understanding of how GCs work, how their actions are affected by disease, and where the new drugs may take us.

The Development of the Calvarial Bones and Sutures and the Pathophysiology of Craniosynostosis.

The skull vault is a complex, exquisitely patterned structure that plays a variety of key roles in vertebrate life, ranging from the acquisition of food to the support of the sense organs for hearing, smell, sight, and taste. During its development, it must meet the dual challenges of protecting the brain and accommodating its growth. The bones and sutures of the skull vault are derived from cranial neural crest and head mesoderm. The frontal and parietal bones develop from osteogenic rudiments in the supraorbital ridge. The coronal suture develops from a group of Shh-responsive cells in the head mesoderm that are collocated, with the osteogenic precursors, in the supraorbital ridge. The osteogenic rudiments and the prospective coronal suture expand apically by cell migration. A number of congenital disorders affect the skull vault. Prominent among these is craniosynostosis, the fusion of the bones at the sutures. Analysis of the pathophysiology underling craniosynostosis has identified a variety of cellular mechanisms, mediated by a range of signaling pathways and effector transcription factors. These cellular mechanisms include loss of boundary integrity, altered sutural cell specification in embryos, and loss of a suture stem cell population in adults. Future work making use of genome-wide transcriptomic approaches will address the deep structure of regulatory interactions and cellular processes that unify these seemingly diverse mechanisms.

Novel osteogenic factors prevents osteoporosis in obese type 2 diabetes

Bone is a dynamic tissue that undergoes continual adaptation during vertebrate life to attain and preserves skeletal size, shape and structural integrity and to regulate mineral homeostasis. Bone homeostasis, which maintains bone mass, is skillfully regulated through a delicate balance between osteoblastic bone formation and osteoclastic bone resorption [1-3]. Osteoblasts are differentiated from bone marrow mesenchymal stem cells and stimulate bone formation and calcification. Osteoclasts are developed from hematopoietic progenitors and promote bone resorption. Physiologic process of bone turnover through these bone cells underpins development and maintenance of the skeletal system. Bone remodeling and modeling underpin development and maintenance of the skeletal system [1]. Bone modeling is responsible for growth and mechanically induced adaptation of bone, and it requires that the processes of bone formation and bone removal (resorption). Process of bone remodeling that makes bone unique among organs and tissues, and add so many levels of complexity with respect to interactions along remodeling sequence by systemic influences (hormones), stress action (physical activity/weight bearing), and growth factors and cytokines produced by the bone cells or factors that come from nearby cells in the marrow tissues.

The first Late Eocene continental faunal assemblage from tropical North America

To date, the terrestrial faunal record of the North American late Eocene has been recovered from its subtropical and temperate regions. We report the first late Eocene continental faunal assemblage from tropical North America, in southern Mexico. Fossil specimens were collected from mudstones that crop out in the Municipality of Santiago Yolomécatl, in northwestern Oaxaca. Previously published K–Ar ages of 32.9 ± 0.9 and 35.7 ± 1.0 Ma in overlain nearby volcanic rocks and biostratigraphy of these new localities suggests a Chadronian mammal age for this new local fauna. The assemblage is composed by two turtle taxa, Rhineura, two caniform taxa, a sciurid, a jimomyid rodent, a geomyine rodent, Gregorymys, Leptochoerus, Perchoerus probus, Merycoidodon, a protoceratid, Poebrotherium, Nanotragulus, Miohippus assinoboiensis, a chalicotherid, a tapiroid, cf. Amynodontopsis, Trigonias and the hymenopteran ichnofossils Celliforma curvata and Fictovichnus sciuttoi. The records of these taxa in northwestern Oaxaca greatly expand southerly their former geographic distribution in North America. The records of the geomorph rodents and Nanotragulus extend their former known biochronological range to the late Eocene. The hymenopteran ichnofossils in the localities suggest the presence of a bare soil after periodic waterlogging, under a sub-humid to sub-arid climate. This new local fauna represents the first glimpse of Eocene vertebrate and invertebrate terrestrial life from tropical North America.