Are some chromosomes particularly good at sex? Insights from amniotes

Several recent studies have produced comparative maps of genes on amniote sex chromosomes, revealing homology of gene content and arrangement across lineages as divergent as mammals and lizards. For example, the chicken Z chromosome, which shares homology with the sex chromosomes of all birds, monotremes, and a gecko, is a striking example of stability of genome organization and retention, or independent acquisition, of function in sex determination. In other lineages, such as snakes and therian mammals, well conserved but independently evolved sex chromosome systems have arisen. Among lizards, novel sex chromosomes appear frequently, even in congeneric species. Here, we review recent gene mapping data, examine the evolutionary relationships of amniote sex chromosomes and argue that gene content can predispose some chromosomes to a specialized role in sex determination.     

Vertebrate lungs: structure, topography and mechanics. A comparative perspective of the progressive integration of respiratory system, locomotor apparatus and ontogenetic development

Vertebrate lungs are highly diverse in their structure, topographical position, ventilation mechanisms, constructional integration into the locomotor apparatus, and the interrelationships with the mode of their ontogenetic development. Vertebrate lungs evolved as supplementary air-breathing organs in primary fishes, being ventilated by buccal pumping. In most recent fishes the lungs are transformed into the hydrostatic swimbladder. This basic type of unicameral lungs and their buccal pumping ventilation are also found in recent amphibians. Land vertebrates developed a very efficient aspiration type of ventilation. In most recent reptiles the lungs are subdivided into three rows of lung chambers, enlarging the exchange surface in correlation to their increasing metabolic needs. The avian respiratory apparatus, with its volume-constant lungs and highly compliant air sacs, and the mammalian broncho-alveolar lung, with its very low compliance, are both derived from multicameral lungs. The avian and the mammalian respiratory systems are integrated very differently with the specific constructions of their locomotor apparatusses and the specific mode of their ontogenetic development.     

Effects of age and size in the ears of gekkonomorph lizards: middle-ear morphology with evolutionary implications

The function of the ear depends in part on its absolute size and internal proportions. Thus, in both young individuals and small species, the middle ear is expected to be allometrically enlarged despite its smaller absolute size. Here we aim to compare the ontogenetic allometry of relevant middle-ear structures as observed within gecko (gekkonomorph lizards) species, with the evolutionary allometry observed interspecifically. These observations also provide middle-ear data for future evaluation of variation in auditory sensitivity. The material comprised 84 museum specimens of geckos, representing nine species of three gekkonomorph subfamilies. The results of dissections and measurements show that different reports notwithstanding, the middle-ear ossicular chain is indeed structured as described for geckos by Werner and Wever. Some sexual dimorphism is indicated, but this requires further study. During postnatal ontogeny, the allometric growth in the ratio of the columellar footplate area to body length differed between the intraspecific and interspecific levels, hence species differences in the middle ear do not merely result from animal size. The ratio of the tympanic membrane area to the columellar footplate area increased during ontogeny. In this, geckos resemble birds and probably also mammals. Similarly, when the comparison was among adults representing different species, the ratio of the tympanic membrane area to the columellar footplate area increased with body size. In this, however, the geckos differed from birds and mammals, in which this ratio varied taxonomically, irrespective of body size. It would thus seem that middle-ear proportions have evolved among geckos to produce small interspecific differences, but among amniote tetrapods they have evolved according to different principles in the classes reptiles, birds, and mammals.     

Pontine influences on respiratory control in ectothermic and heterothermic vertebrates

Respiratory rhythm generators appear both evolutionarily and developmentally as paired segmental rhythm generators in the reticular formation, associated with the motor nuclei of cranial nerves V, VII, IX, X, and XII. Those associated with the Vth and VIIth motor nuclei are "pontine" in origin and in fishes that employ a buccal suction/force pump for breathing the primary pair of respiratory rhythm generators are associated with the trigeminal nuclei. In amphibians, while the basic respiratory pump remains the same, the dominant site of respiratory rhythm generation has been assumed by the facial, glossopharyngeal and vagal motor nuclei. In reptiles, birds and mammals, in general there is a switch to an aspiration pump driven by thoraco-lumbar muscles innervated by spinal nerves. In these groups, the critical sites necessary for respiratory rhythmogenesis now sit near the ponto-medullary border, in the parafacial region (which may underlie expiratory-dominated, intercostal-abdominal breathing in non-mammalian tetrapods) and in a more caudal region, the preBotzinger complex (which may underlie inspiratory-dominated diaphragmatic breathing in mammals).     

Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms

Quantitative functional anatomy of amniote thoracic and abdominal regions is crucial to understanding constraints on and adaptations for facilitating simultaneous breathing and locomotion. Crocodilians have diverse locomotor modes and variable breathing mechanics facilitated by basal and derived (accessory) muscles. However, the inherent flexibility of these systems is not well studied, and the functional specialisation of the crocodilian trunk is yet to be investigated. Increases in body size and trunk stiffness would be expected to cause a disproportionate increase in muscle force demands and therefore constrain the basal costal aspiration mechanism, necessitating changes in respiratory mechanics. Here, we describe the anatomy of the trunk muscles, their properties that determine muscle performance (mass, length and physiological cross-sectional area [PCSA]) and investigate their scaling in juvenile Alligator mississippiensis spanning an order of magnitude in body mass (359 g–5.5 kg). Comparatively, the expiratory muscles (transversus abdominis, rectus abdominis, iliocostalis), which compress the trunk, have greater relative PCSA being specialised for greater force-generating capacity, while the inspiratory muscles (diaphragmaticus, truncocaudalis ischiotruncus, ischiopubis), which create negative internal pressure, have greater relative fascicle lengths, being adapted for greater working range and contraction velocity. Fascicle lengths of the accessory diaphragmaticus scaled with positive allometry in the alligators examined, enhancing contractile capacity, in line with this muscle's ability to modulate both tidal volume and breathing frequency in response to energetic demand during terrestrial locomotion. The iliocostalis, an accessory expiratory muscle, also demonstrated positive allometry in fascicle lengths and mass. All accessory muscles of the infrapubic abdominal wall demonstrated positive allometry in PCSA, which would enhance their force-generating capacity. Conversely, the basal tetrapod expiratory pump (transversus abdominis) scaled isometrically, which may indicate a decreased reliance on this muscle with ontogeny. Collectively, these findings would support existing anecdotal evidence that crocodilians shift their breathing mechanics as they increase in size. Furthermore, the functional specialisation of the diaphragmaticus and compliance of the body wall in the lumbar region against which it works may contribute to low-cost breathing in crocodilians.     

Reconstruction of ancestral brains: Exploring the evolutionary process of encephalization in amniotes

There is huge divergence in the size and complexity of vertebrate brains. Notably, mammals and birds have bigger brains than other vertebrates, largely because these animal groups established larger dorsal telencephali. Fossil evidence suggests that this anatomical trait could have evolved independently. However, recent comparative developmental analyses demonstrate surprising commonalities in neuronal subtypes among species, although this interpretation is highly controversial. In this review, we introduce intriguing evidence regarding brain evolution collected from recent studies in paleontology and developmental biology, and we discuss possible evolutionary changes in the cortical developmental programs that led to the encephalization and structural complexity of amniote brains. New research concepts and approaches will shed light on the origin and evolutionary processes of amniote brains, particularly the mammalian cerebral cortex.     

Diversity in primary palate ontogeny of amniotes revealed with 3D imaging

The amniote primary palate encompasses the upper lip and the nasal cavities. During embryonic development, the primary palate forms from the fusion of the maxillary, medial nasal and lateral nasal prominences. In mammals, as the primary palate fuses, the nasal and oral cavities become completely separated. Subsequently, the tissue demarcating the future internal nares (choanae) thins and becomes the bucconasal membrane, which eventually ruptures and allows for the essential connection of the oral and nasal cavities to form. In reptiles (including birds), the other major amniote group, primary palate ontogeny is poorly studied with respect to prominence fusion, especially the formation of a bucconasal membrane. Using 3D optical projection tomography, we found that the prominences that initiate primary palate formation are similar between mammals and crocodilians but distinct from turtles and lizards, which are in turn similar to each other. Chickens are distinct from all non-avian lineages and instead resemble human embryos in this aspect. The majority of reptiles maintain a communication between the oral and nasal cavities via the choanae during primary palate formation. However, crocodiles appear to have a transient separation between the oral and nasal cavities. Furthermore, the three lizard species examined here, exhibit temporary closure of their external nares via fusion of the lateral nasal prominences with the frontonasal mass, subsequently reopening them just before hatching. The mechanism of the persistent choanal opening was examined in chicken embryos. The mesenchyme posterior/dorsal to the choana had a significant decline in proliferation index, whereas the mesenchyme of the facial processes remained high. This differential proliferation allows the choana to form a channel between the oral and nasal cavities as the facial prominences grow and fuse around it. Our data show that primary palate ontogeny has been modified extensively to support the array of morphological diversity that has evolved among amniotes.     

Comparative ontogeny and phylogeny of the upper jaw skeleton in amniotes.

The morphology, position, and presence of the upper jaw bones vary greatly across amniote taxa. In this review, we compare the development and anatomy of upper jaw bones from the three living amniote groups: reptiles, birds, and mammals. The study of reptiles is particularly important as comparatively little is known about the embryogenesis of the jaw in this group. Our review covers the ontogeny and phylogeny of membranous bones in the face. The aim is to identify conserved embryonic processes that may exist among the three major amniote groups. Finally, we discuss how temporal and spatial regulation of preosseous condensations and ossification centers can lead to variation in the morphology of amniote upper jaw bones.     

Bipedal animals, and their differences from humans

Humans, birds and (occasionally) apes walk bipedally. Humans, birds, many lizards and (at their highest speeds) cockroaches run bipedally. Kangaroos, some rodents and many birds hop bipedally, and jerboas and crows use a skipping gait. This paper deals only with walking and running bipeds. Chimpanzees walk with their knees bent and their backs sloping forward. Most birds walk and run with their backs and femurs sloping at small angles to the horizontal, and with their knees bent. These differences from humans make meaningful comparisons of stride length, duty factor, etc., difficult, even with the aid of dimensionless parameters that would take account of size differences, if dynamic similarity were preserved. Lizards and cockroaches use wide trackways. Humans exert a two-peaked pattern of force on the ground when walking, and an essentially single-peaked pattern when running. The patterns of force exerted by apes and birds are never as markedly two-peaked as in fast human walking. Comparisons with quadrupedal mammals of the same body mass show that human walking is relatively economical of metabolic energy, and human running is expensive. Bipedal locomotion is remarkably economical for wading birds, and expensive for geese and penguins.     

The long and the short of tails

Amniote tails display a wide variety of features for adaptation to diverse environments. Each feature originates from its own distinct developmental processes, and these processes in turn attest to an organism's evolutionary history. In this perspective, we discuss the ontogeny of tails from embryonic to adult stages, amniote tail regeneration, the mechanisms underlying tail length and neural systems, and the benefits of studying tails across vertebrates, in mammals, birds, and non-avian reptiles.     

Comparative functional analysis of the hyolingual anatomy in lacertid lizards

The tongue is often considered a key innovation in the evolution of a terrestrial lifestyle as it allows animals to transport food items through the oral cavity in air, a medium with low density and viscosity. The tongue has been secondarily coopted for a wide diversity of functions, including prey capture, drinking, breathing, and defensive behaviors. Within basal lizard groups, the tongue is used primarily for the purpose of prey capture and transport. In more derived groups, however, the tongue appears specialized for chemoreceptive purposes. Here we examine the tongue structure and morphology in lacertid lizards, a group of lizards where the tongue is critical to both food transport and chemoreception. Because of the different mechanical demands imposed by these different functions, regional morphological specializations of the tongue are expected. All species of lacertid lizards examined here have relatively light tongue muscles, but a well developed hyobranchial musculature that may assist during food transport. The intrinsic musculature, including verticalis, transversalis, and longitudinalis groups, is well developed and may cause the tongue elongation and retraction observed during chemoreception and drinking. The papillary morphology is complex and shows clear differences between the tongue tips and anterior fore-tongue, and the more posterior parts of the tongue. Our data show a subdivision between the fore- and hind-tongue in both papillary structure and muscular anatomy likely allowing these animals to use their tongues effectively during both chemoreception and prey transport. Moreover, our data suggest the importance of hyobranchium movements during prey transport in lacertid lizards.     

An experimental study concerning the accessory nerve in the chicken and turkey.

The retrograde degeneration consecutive to accessory nerve transection proved that the real origin of this nerve in the chicken and turkey is represented exclusively by the ipsilateral dorso-central motor column described by BECCARI (1943). This nucleus, with a moniliform aspect, extends into the first two cervical neuromeres and enters the bulb, where it is continuous with the alpha subdivision of the hypoglossal nucleus. The accessory nerve of the two species of birds is homologous with the external ramus of the same nerve in mammals. An internal ramus is absent in birds.     

Respiratory cooling and thermoregulatory coupling in reptiles

Comparative physiological research on reptiles has focused primarily on the understanding of mechanisms of the control of breathing as they relate to respiratory gases or temperature itself. Comparatively less research has been done on the possible link between breathing and thermoregulation. Reptiles possess remarkable thermoregulatory capabilities, making use of behavioural and physiological mechanisms to regulate body temperature. The presence of thermal panting and gaping in numerous reptiles, coupled with the existence of head-body temperature differences, suggests that head temperature may be the primary regulated variable rather than body temperature. This review examines the preponderance of head and body temperature differences in reptiles, the occurrence of breathing patterns that possess putative thermoregulatory roles, and the propensity for head and brain temperature to be controlled by reptiles, particularly at higher temperatures. The available evidence suggests that these thermoregulatory breathing patterns are indeed present, though primarily in arid-dwelling reptiles. More importantly, however, it appears that the respiratory mechanisms that have the capacity to cool evolved initially in reptiles, perhaps as regulatory mechanisms for preventing overheating of the brain. Examining the control of these breathing patterns and their efficacy at regulating head or brain temperature may shed light on the evolution of thermoregulatory mechanisms in other vertebrates, namely the endothermic mammals and birds.     

Emotion and phylogeny

Gentle handling of mammals (rats, mice) and lizards (Iguana), but not of frogs (Rana) and fish (Carassius), elevated the set-point for body temperature (i.e., produced an emotional fever) achieved only behaviorally in lizards. Heart rate, another detector of emotion in mammals, was also accelerated by gentle handling, from ca. 70 beats/min to ca. 110 beats/min in lizards. This tachycardia faded in about 10 min. The same handling did not significantly modify the frogs' heart rates. The absence of emotional tachycardia in frogs and its presence in lizards (as well as in mammals), together with the emotional fever exhibited by mammals and reptiles, but not by frogs or fish, would suggest that emotion emerged in the evolutionary lineage between amphibians and reptiles. Such a conclusion would imply that reptiles possess consciousness with its characteristic affective dimension, pleasure. The role of sensory pleasure in decision making was therefore verified in iguanas placed in a motivational conflict. To be able to reach a bait (lettuce), the iguanas had to leave a warm refuge, provided with standard food, and venture into a cold environment. The results showed that lettuce was not necessary to the iguanas and that they traded off the palatability of the bait against the disadvantage of the cold. Thus, the behavior of the iguanas was likely to be produced, as it is in humans, through the maximization of sensory pleasure. Altogether, these results may indicate that the first elements of mental experience emerged between amphibians and reptiles.     

On the origin of avian air sacs

For many vertebrates the lung is the largest and lightest organ in the body cavity and for these reasons can greatly affect an organism's shape, density, and its distribution of mass; characters that are important to locomotion. In this paper non-respiratory functions of the lung are considered along with data on the respiratory capacities and gas exchange abilities of birds and crocodilians to infer the evolutionary history of the respiratory systems of dinosaurs, including birds. From a quadrupedal ancestry theropod dinosaurs evolved a bipedal posture. Bipedalism is an impressive balancing act, especially for tall animals with massive heads. During this transition selection for good balance and agility may have helped shape pulmonary morphology. Respiratory adaptations arising for bipedalism are suggested to include a reduction in costal ventilation and the use of cuirassal ventilation with a caudad expansion of the lung into the dorsal abdominal cavity. The evolution of volant animals from bipeds required yet again a major reorganization in body form. With this transition avian air sacs may have been favored because they enhanced balance and agility in flight. Finally, I propose that these hypotheses can be tested by examining the importance of the air sacs to balance and agility in extant animals and that these data will enhance our understanding of the evolution of the respiratory system in archosaurs.     

Multiple sex chromosomes in the light of female meiotic drive in amniote vertebrates

It is notable that the occurrence of multiple sex chromosomes differs significantly between major lineages of amniote vertebrates. In this respect, birds are especially conspicuous, as multiple sex chromosomes have not been observed in this lineage so far. On the other hand, in mammals, multiple sex chromosomes have evolved many times independently. We hypothesize that this contrast can be related to the different involvement of sex-specific sex chromosomes in female meiosis subjected to the female meiotic drive under male versus female heterogamety. Essentially, the male-specific Y chromosome is not involved in female meiosis and is therefore sheltered against the effects of the female meiotic drive affecting the X chromosome and autosomes. Conversely, the Z and W sex chromosomes are both present in female meiosis. Nonrandom segregation of these sex chromosomes as a consequence of their rearrangements connected with the emergence of multiple sex chromosomes would result in a biased sex ratio, which should be penalized by selection. Therefore, the emergence of multiple sex chromosomes should be less constrained in the lineages with male rather than female heterogamety. Our broader phylogenetic comparison across amniotes supports this prediction. We suggest that our results are consistent with the widespread occurrence of female meiotic drive in amniotes.     

Mechanisms of ventilatory periodicities

The study of ventilatory periodicities is relevant to the problem of obstructive sleep apnea. Apneas occur at the nadirs of periodicities during sleep. Periodicities can be caused by chemical instability, related to unstable action of the closed loop feedback system for the chemical regulation of breathing. Such instability occurs when overall loop gain is greater than or equal to unity and the phase lag around the loop is 180°. Periodic breathing during hypoxia and in patients with congestive heart failure is likely to be explained by this mechanism. Periodic breathing can also be the result of state instability. Here ventilation declines at sleep onset and the resultant changes in blood gases trigger an arousal, i.e., sudden transition to a lighter stage of sleep. With arousal, ventilation increases. Thus, periodic breathing is secondary to these changes in sleep state. These processes, chemical instability and state instability, can interact and produce complex patterns of oscillation in ventilation.     

Peripheral arterial chemoreceptors and the evolution of the carotid body

There has been a reduction in the distribution of peripheral respiratory O(2) chemoreceptors from multiple, dispersed sites in fish and amphibia to a single dominant receptor site in birds and mammals. In the process, the cells in the fish gill associated with O(2) chemosensing (5-HT containing neuroepithelial cells often found in association with ACh/catecholamine (CA) containing cells) are replaced by the glomus cells of the mammalian carotid body (which contain multiple putative neurotransmitter substances, including 5-HT, CA and ACh, all within the same cells), although this difference may be more superficial than first appears. While still highly speculative, these trends would appear to be correlated with the transition from aquatic respiration and bimodal breathing, and from animals with intra-cardiac shunts (two situations where the ability to sense O(2) at multiple sites would be an advantage), to strictly air breathing in animals with no intra-cardiac shunts. It is also tempting to speculate that while the basic O(2)-sensing mechanism is the same for all receptor cells, the receptor groups in fish have evolved in such a way to make the responses of some more sensitive to changes in O(2) delivery than others. The net result is that those receptors associated with the first gill arch of fish (the third branchial arch) become the carotid body in higher vertebrates associated with the regulation of ventilation and ensuring oxygen supply to the gas exchange surface. Those receptors associated with the second gill arch (fourth branchial arch) become the aortic bodies capable of sensing changes in oxygen content of the blood and primarily involved in regulating oxygen transport capacity through erythropoiesis and changes in blood volume.