Evidence for avian intrathoracic air sacs in a new predatory dinosaur from Argentina

Background

Living birds possess a unique heterogeneous pulmonary system composed of a rigid, dorsally-anchored lung and several compliant air sacs that operate as bellows, driving inspired air through the lung. Evidence from the fossil record for the origin and evolution of this system is extremely limited, because lungs do not fossilize and because the bellow-like air sacs in living birds only rarely penetrate (pneumatize) skeletal bone and thus leave a record of their presence.

Methodology/Principal Findings

We describe a new predatory dinosaur from Upper Cretaceous rocks in Argentina, Aerosteon riocoloradensis gen. et sp. nov., that exhibits extreme pneumatization of skeletal bone, including pneumatic hollowing of the furcula and ilium. In living birds, these two bones are pneumatized by diverticulae of air sacs (clavicular, abdominal) that are involved in pulmonary ventilation. We also describe several pneumatized gastralia (“stomach ribs”), which suggest that diverticulae of the air sac system were present in surface tissues of the thorax.

Conclusions/Significance

We present a four-phase model for the evolution of avian air sacs and costosternal-driven lung ventilation based on the known fossil record of theropod dinosaurs and osteological correlates in extant birds:(1) Phase I—Elaboration of paraxial cervical air sacs in basal theropods no later than the earliest Late Triassic.(2) Phase II—Differentiation of avian ventilatory air sacs, including both cranial (clavicular air sac) and caudal (abdominal air sac) divisions, in basal tetanurans during the Jurassic. A heterogeneous respiratory tract with compliant air sacs, in turn, suggests the presence of rigid, dorsally attached lungs with flow-through ventilation.(3) Phase III—Evolution of a primitive costosternal pump in maniraptoriform theropods before the close of the Jurassic.(4) Phase IV—Evolution of an advanced costosternal pump in maniraptoran theropods before the close of the Jurassic.In addition, we conclude:(5) The advent of avian unidirectional lung ventilation is not possible to pinpoint, as osteological correlates have yet to be identified for uni- or bidirectional lung ventilation.(6) The origin and evolution of avian air sacs may have been driven by one or more of the following three factors: flow-through lung ventilation, locomotory balance, and/or thermal regulation.     

The evolution of the scrotum: a new hypothesis

The adaptive significance of the scrotum is unresolved after more than 60 years of debate and experimentation. The "training hypothesis" introduced here suggests that testicular descent is a mechanism for improving sperm quality. The hypothesis proposes that: (1) testicular descent decreases blood supply to maturing sperm cells, (2) sperm mitochondria respond to the resulting oxygen stress by enhancing their enzymatic machinery for oxidative metabolism, as do oxygen-stressed muscle cell mitochondria, and (3) the resulting increase in aerobic fitness of sperm cells is advantageous in inter-ejaculate competition. The hypothesis suggests that there is a quantity-quality trade-off in sperm production, where taxa with internal testes produce large volumes of low-quality sperm while taxa with scrotal testes produce smaller volumes of higher-quality sperm.     

Intron phylogeny: a new hypothesis

The three major classes of intron are clearly of unequal antiquity. Structured (often self-splicing and sometimes mobile) introns are the most ancient, probably dating (at least for group I) from the ancestral (eubacterial) cell 3500 million years ago, and were originally restricted to tRNA. Protein-spliced introns (usually in tRNA) probably evolved from them by a radical change in splicing mechanism in the common ancestor of eukaryotes and archaebacteria, perhaps only about 1700 million years ago. Spliceosomal introns probably evolved from group-II-like self-splicing introns after the origin of the nucleus between 1700 and 1000 million years ago, and were probably mostly inserted into previously unsplit protein-coding genes after the origin of mitochondria 1000 million years ago.     

Roles of microfilaments in exocytosis: a new hypothesis

We observed the dynamic changes in the localization of microfilaments during the exocytic secretion of rat parotid and submandibular gland acinar cells, and obtained results which led us to propose a new concept of microfilament function in exocytosis. With the electron microscopy, NBD-Phallacidin (NBD-PL) fluorescence technique and immunohistochemistry for myosin, microfilaments consisting of F-actin and myosin were localized mainly underneath the luminal plasma membrane. Microfilaments were not detectable around the secretory granules which were stored in the cytoplasm, but were clearly observed around them whose membranes were continuous with the luminal plasma membrane. When viewed with NBD-PL and myosin fluorescence, the area of fused granule membranes revealed bright fluorescence in association with the luminal border, so that the luminal membrane undergoing exocytosis appeared like a 'bunch of grapes'. When excess exocytosis was stimulated by isoproterenol (IPR), the number of individual 'grapes' increased dramatically, indicating that the secretory granules are surrounded by microfilaments after the fusion with the luminal membrane. Microfilaments thus continuously undercoat the luminal membrane during exocytosis although the exocytic process involves the dilation and subsequent reduction of the luminal membrane due to the addition and removal of secretory granule membranes. This reduction of the dilated luminal membrane following exocytosis was, however, inhibited when the microfilaments were disrupted by cytochalasin D. Following this treatment, the lumina was expanded extraordinarily and the secretory products remained in the enlarged lumina, showing that the release of secretory products is inhibited when the microfilament function is disturbed. These results indicate that 1) microfilaments are localized mainly underneath the luminal plasma membrane and act as an obstacle to exocytosis when cells are at the resting phase and 2) at the secretory phase microfilaments allow exocytosis by disorganizing their barrier system and then, by encircling the discharged secretory granule membranes, provide forces for the extrusion of secretory products through the action of the acto-myosin contractile system.     

Protozoan parasites in group-living primates: testing the biological island hypothesis

A series of articles by W.J. Freeland published in the 1970s proposed that social organization and behavioral processes were heavily influenced by parasitic infections, which led to a number of intriguing hypotheses concerning how natural selection might act on social factors because of the benefits of avoiding parasite infections. For example, Freeland [1979] showed that all individuals within a given group harbored identical gastrointestinal protozoan faunas, which led him to postulate that social groups were akin to "biological islands" and suggest how this isolation could select specific types of ranging and dispersal patterns. Here, we reexamine the biological island hypothesis by quantifying the protozoan faunas of the same primate species examined by Freeland in the same location; our results do not support this hypothesis. In contrast, we quantified two general changes in protozoan parasite community of primates in the study area of Kibale National Park, Uganda, over the nearly 35 years between sample collections: (1) the colobines found free of parasites in the early 1970s are now infected with numerous intestinal protozoan parasites and (2) groups are no longer biological islands in terms of their protozoan parasites. Whatever the ultimate explanation for these changes, our findings have implications for studies proposing selective forces shaping primate behavior and social organization.     

Causes of venous ulceration: a new hypothesis

Previous hypotheses about the causes of venous ulceration are inconsistent with recently published data. In patients with chronic venous insufficiency the number of functioning capillary loops visible in the skin on microscopy fell after the legs had been dependent for 30 minutes. Another study had shown that leucocytes became trapped in the circulation in dependent legs. A new hypothesis linking these two findings proposes that the trapped while cells occlude the capillaries and result in ischaemia of the skin of the leg.     

Adoption behaviour by gulls: a new hypothesis

It appears that chicks are selected to run away and seek adoption in a foster-family when the level of investment they receive falls below a certain threshold. Predictions based on this hypothesis are in agreement with the available evidence in the literature.     

Predictors of orbital convergence in primates: a test of the snake detection hypothesis of primate evolution

Traditional explanations for the evolution of high orbital convergence and stereoscopic vision in primates have focused on how stereopsis might have aided early primates in foraging or locomoting in an arboreal environment. It has recently been suggested that predation risk by constricting snakes was the selective force that favored the evolution of orbital convergence in early primates, and that later exposure to venomous snakes favored further degrees of convergence in anthropoid primates. Our study tests this snake detection hypothesis (SDH) by examining whether orbital convergence among extant primates is indeed associated with the shared evolutionary history with snakes or the risk that snakes pose for a given species. We predicted that orbital convergence would be higher in species that: 1) have a longer history of sympatry with venomous snakes, 2) are likely to encounter snakes more frequently, 3) are less able to detect or deter snakes due to group size effects, and 4) are more likely to be preyed upon by snakes. Results based on phylogenetically independent contrasts do not support the SDH. Orbital convergence shows no relationship to the shared history with venomous snakes, likelihood of encountering snakes, or group size. Moreover, those species less likely to be targeted as prey by snakes show significantly higher values of orbital convergence. Although an improved ability to detect camouflaged snakes, along with other cryptic stimuli, is likely a consequence of increased orbital convergence, this was unlikely to have been the primary selective force favoring the evolution of stereoscopic vision in primates.     

The serial transformation hypothesis of vertebrate origins: comment on The new head hypothesis revisited

In The New Head Hypothesis Revisited, R.G. Northcutt (2005. J Exp Zool (Mol Dev Evol) 304B:274-297) evaluates the original postulates of this hypothesis (Northcutt and Gans, 1983. Quart Rev Biol 58:1-28). One of these postulates is that the brain-particularly the forebrain-evolved at essentially the same time as many neural crest and neurogenic placode derivatives-including sensory ganglia, dermal skeleton and sensory capsules of the head, and branchial arches. Northcutt's subsequent paper in 1996 concluded with the idea that transitional forms might not have occurred at the origin of vertebrates. Butler proposed a Serial Transformation hypothesis in 2000, which disputed the latter idea in that paired eyes and an enlarged brain (but lacking telencephalon) were envisioned to have been gained before elaboration of most neural crest and neurogenic placodal derivatives. In 2003, J. Mallatt and J.-Y. Chen analyzed fossils of the Cambrian animal Haikouella, which strongly support its affinity to craniates and aspects of several hypotheses, including Butler's transformational model, because although branchial bars are present, most other neural crest and placodal derivatives are absent, while paired eyes and an enlarged brain (but probably without telencephalon) are present. A more complete picture of vertebrate origins can be realized when the various hypotheses are constructively reconciled.     

The new head hypothesis revisited

In 1983, a new theory, the New Head Hypothesis, was generated within the context of the Tunicate Hypothesis of deuterostome evolution. The New Head Hypothesis comprised four claims: (1) neural crest, neurogenic placodes, and muscularized hypomere are unique to vertebrates, (2) the structures derived from these tissues allowed a shift from filter feeding to active predation, (3) the rostral head of vertebrates is a neomorphic unit, and (4) neural crest and neurogenic placodes evolved from the epidermal nerve plexus of ancestral deuterostomes. These claims are re-examined within the context of evolutionary developmental biology. The first may or may not be valid, depending on whether protochordates have these tissues in rudimentary form. Regarding the second, clearly, the elaboration of these tissues in vertebrates is correlated with a shift from filter feeding to active predation. The third claim is clarified, i.e., that the elaboration of the alar portion of the rostral brain and the development of olfactory organs and their associated connective tissues represent a neomorphic unit, which appears to be valid. The fourth is rejected. When the origin of neural crest and neurogenic placodes is examined within the context of developmental biology, it appears they evolved due to the rearrangement of germ layers in the blastulae of the deuterostomes that gave rise to chordates. Deuterostome evolution and the origin of vertebrates are also re-examined in the context of new data from developmental biology and taxonomy. The Tunicate Hypothesis is rejected, and a new version of the Dipleurula Hypothesis is presented.     

The mechanism of radiation-induced interphase death of lymphoid cells: a new hypothesis

The interphase death of irradiated rat thymocytes depends on their concentration during postirradiation incubation. The kinetics of pycnosis and cell death determined with the trypan blue exclusion test in the samples with the highest cell concentration (1-2 x 10(7) cells/ml) is consistent with the data available in the literature, whereas the samples with the lowest concentration (2 x 10(5) cells/ml) undergo almost no pycnosis and death after irradiation with doses up to 50 Gy. On the basis of these results, we suggest a new mechanism of interphase death involving an interaction between irradiated thymocytes and the fraction of thymus cells possessing cytocidal activity. The observed correlation between the cytocidal activity and interphase death of thymocytes from animals of different ages favors our mechanism. It was found that the inhibitors which prevent the conjugation of killer cells and their targets do not influence interphase death, while the substances which block the secretion of cytotoxic factors or their action on the target membrane do protect from interphase death. Thus we suggest that the irradiation activates the killer cells to secrete some cytotoxic factors which induce pycnosis and interphase death of thymocytes.     

Assessing habitat utilization by neotropical primates: a new approach

This study aims to ascertain habitat utilization, in relation to forest structural variation, by a multi-species group of primates in tropical lowland rainforest in Southeast Peru during dry season. A new approach to assessing habitat utilization was used. Habitat variation was described by structural and indicator variables collected in quadrats along transects through a study area within Terra Firme and Floodplain forest. Variables were grouped into ‘factors’ accounting for most of the variation by means of a Principal Components Analysis (PCA). Presence or absence of the primates within the quadrats, assessed by repeat transect surveys, was taken to indicate habitat preferences. Discrimination between the habitat and forest structure in areas of primate presence as opposed to absence was carried out by means of Discriminant Function Analysis (DFA). This highlighted patterns in most utilized habitat. Vertical utilization of the forest was also assessed along with presence in bamboo and general activity on encounter. Suggestions of habitat preference and utilization are made for each of the six sympatric species studied, based on significantly discriminating habitat factors, vertical stratification on encounter and relationships with bamboo.Saguinus fuscicollis andCebus moloch appeared as habitat generalists.Cebus apella, Saimiri sciureus, andAotus spp., exhibited varying degrees of preference for habitat factors suggesting disturbed forest,Cebus albifrons was more generalistic but with a possible association with primary, naturally disturbed forest.C. appella was encountered in Terra Firme forest significantly more than in Floodplain. ForS. sciureus, C. moloch, andC. apella, upper understory was the most utilized forest layer, forC. albifrons, middle canopy and forS. sciureus andAotus spp., lower understory. Both positive and negative relationships with bamboo were highlighted. Significant positive relationships betweenAotus spp., and bamboo suggest dense bamboo stands provide important daytime resting sites for this nocturnal species.C. moloch was also shown to utilize bamboo whereasS. fuscicollis appeared to actively avoid it. High levels of conformity with past studies in terms of habitat utilization patterns described for the species studied supports the conclusion that the methods used in this study provide an effective means of assessing primate habitat utilization within complex habitat.     

The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis

Chloroplasts are important sensors of environment change, fulfilling key roles in the regulation of plant growth and development in relation to environmental cues. Photosynthesis produces a repertoire of reductive and oxidative (redox) signals that provide information to the nucleus facilitating appropriate acclimation to a changing light environment. Redox signals are also recognized by the cellular innate immune system allowing activation of non-specific, stress-responsive pathways that underpin cross tolerance to biotic–abiotic stresses. While these pathways have been intensively studied in recent years, little is known about the different components that mediate chloroplast-to-nucleus signalling and facilitate cross tolerance phenomena. Here, we consider the properties of the WHIRLY family of proteins and the REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 (RRTF1) in relation to chloroplast redox signals that facilitate the synergistic co-activation of gene expression pathways and confer cross tolerance to abiotic and biotic stresses. We propose a new hypothesis for the role of WHIRLY1 as a redox sensor in chloroplast-to-nucleus retrograde signalling leading to cross tolerance, including acclimation and immunity responses. By virtue of its association with chloroplast nucleoids and with nuclear DNA, WHIRLY1 is an attractive candidate coordinator of the expression of photosynthetic genes in the nucleus and chloroplasts. We propose that the redox state of the photosynthetic electron transport chain triggers the movement of WHIRLY1 from the chloroplasts to the nucleus, and draw parallels with the regulation of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1).     

The active form of phytochrome: a new hypothesis based on phytochrome pelletability studies

Difficulties arising from the current dogma that the far-red absorbing form of phytochrome (P_fr) is the only active form are discussed.A new hypothesis is proposed in which phytochrome is held to be the photoreceptor for both low energy (pulse) and high energy (HIR) responses. There is a common basic mechanism of action involving interaction between phytochrome and a binding site within the cell. The phytochrome involvement in low energy responses exhibits an action spectrum for binding that matches the P_r absorption spectrum and reversibility by far-red irradiation. Upon prolonged irradiation the phytochrome-binding site interaction acquires different characteristics that are reminiscent of those displayed in HIR, e.g. dependence on sustained irradiation for continual binding, dependence of the degree of binding on irradiance and the similarity of the action spectrum with that of HIR action spectra, e.g. that for inhibition of lettuce hypocotyl lengthening.As expected on the basis of the new hypothesis the particulate fraction of phytochrome contains both P_r and P_fr. Arguments are advanced that the presence of P_r in pellets of particulate phytochrome cannot be accounted for by (i) the “induced fit” hypothesis, (ii) the “pigment cycling” hypothesis, and (iii) the “open phytochrome-receptor model”. We conclude that phytochrome molecules, after being sufficiently energized can interact with their intracellular binding sites irrespective of their chromophoric configuration.     

The oestrogen paradox: a hypothesis

Epidemiological and observational studies suggest that oestrogens, when used as hormonal therapy in post-menopausal women, can increase the risk of breast cancer if used long term. However, more recent data suggest that short-term use in sub-groups of post-menopausal women significantly decreases the risk of breast cancer. This beneficial effect is also observed when high-dose oestrogen is administered to post-menopausal women with breast cancer to cause tumour regression, a phenomenon which commonly occurs. We consider these divergent responses to oestrogen to represent a "paradox". Data from our own and other investigative groups suggest a hypothesis to explain this paradox. Deprivation of oestradiol in model systems causes cells to adapt and to undergo apoptosis in response to oestrogen. This occurs through the Fas/Fas ligand death receptor pathway and through alterations in apoptotic mechanisms mediated by mitochondria. This process of programmed cell death may explain the regression of established breast cancer with oestrogen administration and the diminution in the rate of new breast cancer diagnoses recently reported. Our hypothesis is based upon pathological data indicating the presence of a "reservoir" of undiagnosed breast cancer in the population of women who would be starting on oestrogens as menopausal hormonal therapy. The long-term increased risk of breast cancer may then reflect different mechanisms. Oestrogens can cause mutations through enhancement of the rate of cell division and concomitantly the error rate in DNA replication. In addition, oestrogens can be metabolised to directly genotoxic compounds. These carcinogenic processes take much longer, since a number of mutations must accumulate before resulting in breast cancer. These hypotheses regarding oestrogen-induced apoptosis in the short term and carcinogenesis in the long term now require rigorous verification but would serve to explain the "oestrogen paradox".