Structural evolution of Otx genes in craniates

Using a degenerate PCR approach, we performed an exhaustive search of Otx genes in the reedfish Erpetoichthys calabaricus, the dogfish Scyliorhinus canicula, and the hagfish Myxine glutinosa. Three novel Otx genes were identified in each of these species, and their deduced protein sequences were determined over a large C-terminal fragment located immediately downstream of the homeodomain. Like their lamprey and osteichthyan counterparts, these nine genes display a tandem duplication of a 20--25-residue C-terminal domain, which appears to be a hallmark of all craniate Otx genes identified thus far, including the highly divergent Crx gene. Phylogenetic analyses show that, together with their osteichthyan counterparts, the dogfish and reedfish genes can be classified into three gnathostome orthology classes. Two of the three genes identified in each of these species belong to the Otx1 and Otx2 orthology classes previously characterized in osteichthyans. The third one unambiguously clusters with the Otx5/Otx5b genes recently characterized in Xenopus laevis, thus defining a novel orthology class. Our results also strongly suggest that the highly divergent Crx genes identified in humans, rodents, and oxen are the mammalian representatives of this third class. The hagfish genes display no clear relationships to the three gnathostome orthology classes, but one of them appears to be closely related to the LjOtxA gene, previously identified in Lampetra japonica. Taken together, these data support the hypothesis that the Otx multigene families characterized in craniates all derive from duplications of a single ancestral gene which occurred after the splitting of cephalochordates but prior to the gnathostome radiation. Using site-by-site sequence comparisons of the gnathostome Otx proteins, we also identified structural constraints selectively acting on each of the three gnathostome orthology classes. This suggests that specialized functions for each of these orthology classes were fixed in the gnathostome lineage prior to the splitting between osteichthyans and chondrichthyans.     

Sensory system evolution at the origin of craniates

The multiple events at the transition from non-craniate invertebrate ancestors to craniates included the gain and/or elaboration of migratory neural crest and neurogenic placodes. These tissues give rise to the peripherally located, bipolar neurons of all non-visual sensory systems. The brain was also elaborated at or about this same time. Were the peripheral and central events simultaneous or sequential? A serial transformation hypothesis postulates that paired eyes and an enlarged brain evolved before the elaboration of migratory neural crest placodal sensory systems. Circumstantial evidence for this scenario is derived from the independent occurrence of the combination of large, paired eyes plus a large, elaborated brain in at least three taxa (cephalochordates, arthropods and craniates) and partly from the exclusivity of the diencephalon for visual system-related distal sensory components versus the restricted distribution of migratory neural crest-placodal sensory systems to the remaining parts of the neuraxis. This scenario accounts for the similarity of all central sensory system pathways due to the primary establishment of descending visual pathways via the diencephalon and midbrain tectum to brainstem motor regions and the subsequent exploitation of the same central beachhead by the migratory neural crest-placodal systems as a template for their organization.     

Molecular ecology and adaptation of visual photopigments in craniates

In craniates, opsin‐based photopigments expressed in the eye encode molecular ‘light sensors’ that constitute the initial protein in photoreception and the activation of the phototransduction cascade. Since the cloning and sequencing of the first vertebrate opsin gene (bovine rod opsin) nearly 30 years ago (Ovchinnikov Yu 1982, FEBS Letters, 148, 179–191; Hargrave et al. 1983, Biophysics of Structure & Mechanism, 9, 235–244; Nathans & Hogness 1983, Cell, 34, 807–814), it is now well established that variation in the subtypes and spectral properties of the visual pigments that mediate colour and dim‐light vision is a prevalent mechanism for the molecular adaptation to diverse light environments. In this review, we discuss the origins and spectral tuning of photopigments that first arose in the agnathans to sample light within the ancient aquatic landscape of the Early Cambrian, detailing the molecular changes that subsequently occurred in each of the opsin classes independently within the main branches of extant jawed gnathostomes. Specifically, we discuss the adaptive changes that have occurred in the photoreceptors of craniates as they met the ecological challenges to survive in quite differing photic niches, including brightly lit aquatic surroundings; the deep sea; the transition to and from land; diurnal, crepuscular and nocturnal environments; and light‐restricted fossorial settings. The review ends with a discussion of the limitations inherent to the ‘nocturnal‐bottleneck’ hypothesis relevant to the evolution of the mammalian visual system and a proposition that transition through a ‘mesopic‐bottleneck’ may be a more appropriate model.     

Glycogen metabolic enzymes in the skeletal muscles of the developing chick embryo

In the skeletal muscles of the chick embryo from the 10th till the 15th day of embryogenesis, phosphorylase (EC. 2.4.1.1) is represented by two isozymes one of which corresponds, by electrophoretic mobility, to the liver phosphorylase and another to phosphorylase of the skeletal muscles of the adult rat. From the 17th day of embryogenesis on only one isozyme of phosphorylase is found in the skeletal muscles which is identical with that of the skeletal muscles of the adult bird. The isozyme spectrum of phosphorylase of the whole 4 days old embryo contains, besides phosphorylase L, a special "embryonic" isozyme which differs from that of the skeletal muscles by immunochemical characteristics and electrophoretic mobility. From the 10th day of embryogenesis till hatching, the activity of phosphorylase of the skeletal muscles increases more than 50 times and that of glycogen synthetase (EC. 2.4.1.11) only 4 times.     

Comparison of foetal metabolic differentiation in three cattle muscles

Metabolic differentiation of Semitendinosus (ST), Cutaneus trunci (CT) and Masseter (MA) in cattle foetuses aged from 110 to 260 days was studied by measuring isocitrate dehydrogenase (ICDH, oxidative) and lactate dehydrogenase (LDH, glycolytic) activities. The five LDH isoenzymes were separated by electrophoresis and assayed by densitometry. ICDH activity increased from 210 days onwards in the three muscles but more intensively in MA (oxidative). LDH activity increased from 170 days onwards in ST, 180 days onwards in CT and only from 210 days onwards in MA and was higher in the glycolytic muscles (ST and CT). The proportion of the LDH-M subunit increased during foetal life in glycolytic muscles. At 110 days, it was higher in CT, intermediate in ST and lower in MA. These results show that 1) metabolic differentiation of bovine muscle begins during the last third of foetal life and 2) the proportion of the LDH-M subunit seems to be related to the contractile type of adult muscle from the first stages of foetal life.     

Oxygen-dependence of upper thermal limits in crustaceans from different thermal habitats

The critical thermal maximum (CT_MAX) is the temperature at which animals exhibit loss of motor response because of a temperature-induced collapse of vital physiological systems. A central mechanism hypothesised to underlie the CT_MAX of water-breathing ectotherms is insufficient tissue oxygen supply for vital maintenance functions because of a temperature-induced collapse of the cardiorespiratory system. The CT_MAX of species conforming to this hypothesis should decrease with declining water oxygen tension (PO₂) because they have oxygen-dependent upper thermal limits. However, recent studies have identified a number of fishes and crustaceans with oxygen-independent upper thermal limits, their CT_MAX unchanged in progressive aquatic hypoxia. The previous studies, which were performed separately on cold-water, temperate and tropical species, suggest the oxygen-dependence of upper thermal limits and the acute thermal sensitivity of the cardiorespiratory system increases with decreasing habitat temperature. Here we directly test this hypothesis by assessing the oxygen-dependence of CT_MAX in the polar Antarctic krill (Euphausia superba), as well as the temperate Baltic prawn (Palaemon adspersus) and brown shrimp (Crangon crangon). We found that P. adspersus and C. crangon maintain CT_MAX in progressive hypoxia down to 40 mmHg, and that only E. superba have oxygen-dependent upper thermal limits at normoxia. In E. superba, the observed decline in CT_MAX with water PO₂ is further supported by heart-rate measurements showing a plateauing, and subsequent decline and collapse of heart performance at CT_MAX. Our results support the hypothesis that the oxygen-dependence of upper thermal limits in water-breathing ectotherms and the acute thermal sensitivity of their cardiorespiratory system increases with decreasing habitat temperature.     

Allometric estimation of metabolic rate from heart rate in penguins

Studies of the relationship between heart rate (f(H)) and rate of oxygen consumption (V(.) (O(2))), which are then used to predict field metabolic rate, frequently fail to incorporate body mass as a predictive variable. This is a potentially important omission in the study of animals whose body mass fluctuates substantially during their annual cycle. In an attempt further to improve estimates of field metabolic rate from f(H), we re-evaluated data on M(b), f(H) and V(.) (O(2)) from previous studies of macaroni penguins (Eudyptes chrysolophus) and king penguins (Aptenodytes patagonicus) and derived a new relationship to integrate these three quantities. This relationship is at least as accurate and precise as previously determined relationships. We applied this same principle to published data on 11 of the 20 recognised penguin taxa to derive a relationship to predict V(.) (O(2)) from f(H) and M(b) in penguins of any species. This result has interesting implications in terms of reducing the logistical burden in studies of field metabolic rate.     

Evolution of the axial system in craniates: morphology and function of the perivertebral musculature

The axial musculoskeletal system represents the plesiomorphic locomotor engine of the vertebrate body, playing a central role in locomotion. In craniates, the evolution of the postcranial skeleton is characterized by two major transformations. First, the axial skeleton became increasingly functionally and morphologically regionalized. Second, the axial-based locomotion plesiomorphic for craniates became progressively appendage-based with the evolution of extremities in tetrapods. These changes, together with the transition to land, caused increased complexity in the planes in which axial movements occur and moments act on the body and were accompanied by profound changes in axial muscle function. To increase our understanding of the evolutionary transformations of the structure and function of the perivertebral musculature, this review integrates recent anatomical and physiological data (e.g., muscle fiber types, activation patterns) with gross-anatomical and kinematic findings for pivotal craniate taxa. This information is mapped onto a phylogenetic hypothesis to infer the putative character set of the last common ancestor of the respective taxa and to conjecture patterns of locomotor and muscular evolution. The increasing anatomical and functional complexity in the muscular arrangement during craniate evolution is associated with changes in fiber angulation and fiber-type distribution, i.e., increasing obliqueness in fiber orientation and segregation of fatigue-resistant fibers in deeper muscle regions. The loss of superficial fatigue-resistant fibers may be related to the profound gross anatomical reorganization of the axial musculature during the tetrapod evolution. The plesiomorphic function of the axial musculature -mobilization- is retained in all craniates. Along with the evolution of limbs and the subsequent transition to land, axial muscles additionally function to globally stabilize the trunk against inertial and extrinsic limb muscle forces as well as gravitational forces. Associated with the evolution of sagittal mobility and a parasagittal limb posture, axial muscles in mammals also stabilize the trunk against sagittal components of extrinsic limb muscle action as well as the inertia of the body's center of mass. Thus, the axial system is central to the static and dynamic control of the body posture in all craniates and, in gnathostomes, additionally provides the foundation for the mechanical work of the appendicular system.     

Fossil sister group of craniates: predicted and found

This study investigates whether the recently described Cambrian fossil Haikouella (and the very similar Yunnanozoon) throws light on the longstanding problem of the origin of craniates. In the first rigorous cladistic analysis of the relations of this animal, we took 40 anatomical characters from Haikouella and other taxa (hemichordates, tunicates, cephalochordates, conodont craniates and other craniates, plus protostomes as the outgroup) and subjected these characters to parsimony analysis. The characters included several previously unrecognized traits of Haikouella, such as upper lips resembling those of larval lampreys, the thick nature of the branchial bars, a mandibular branchial artery but no mandibular branchial bar, muscle fibers defining the myomeres, a dark fibrous sheath that defines the notochord, conclusive evidence for paired eyes, and a large hindbrain and diencephalon in the same positions as in the craniate brain. The cladistic analysis produced this tree: (protostomes, hemichordates (tunicates, (cephalochordates, (Haikouella, (conodonts + other craniates))))), with the "Haikouella + craniate" clade supported by bootstrap values that ranged from 81-96%, depending on how the analysis was structured. Thus, Haikouella is concluded to be the sister group of the craniates. Alternate hypotheses that unite Haikouella with hemichordates or cephalochordates, or consider it a basal deuterostome, received little or no support. Although it is the sister group of craniates, Haikouella is skull-less and lacks an ear, but it does have neural-crest derivatives in its branchial bars. Its craniate characters occur mostly in the head and pharynx; its widely spaced, robust branchial bars indicate it ventilated with branchiomeric muscles, not cilia. Despite its craniate mode of ventilation, Haikouella was not a predator but a suspension feeder, as shown by its cephalochordate-like endostyle, and tentacles forming a screen across the mouth. Haikouella was compared to pre-craniates predicted by recent models of craniate evolution and was found to fit these predictions closely. Specifically, it fits Northcutt and Gans' prediction that the change from ciliary to muscular ventilation preceded the change from suspension feeding to predatory feeding; it fits Butler's claim that vision was the first craniate sense to start elaborating; it is consistent with the ideas of Donoghue and others about the ancestor of conodont craniates; and, most strikingly, it resembles Mallatt's prediction of the external appearance of the ancestral craniate head. By contrast, Haikouella does not fit the widespread belief that ancestral craniates resembled hagfishes, because it has no special hagfish characters. Overall, Haikouella agrees so closely with recent predictions about pre-craniates that we conclude that the difficult problem of craniate origins is nearly solved.     

Allometry of resting metabolic rate in cockroaches

1. Resting VO2 at 22.7 degrees C was 0.217 +/- 0.007 ml O2/g/hr in Nauphoeta cinerea of 0.51 +/- 0.008 g body mass. 2. Whole animal resting metabolic rate for 11 cockroach species scaled allometrically: VO2 = 0.261 M0.776. 3. Allometry of resting VO2 among cockroach species is similar to that in vertebrates, and is consistent with models based on both "elastic similarity" and "biological similitude."     

Testosterone metabolic clearance rate and production rate in the male infant rhesus monkey

The male infant rhesus monkey (Macaca mulatta) undergoes a period of testicular activation similar to that seen in the human infant. Plasma testosterone (T) concentrations rise after birth, reaching levels of about 500 ng/dl at 1-3 mo of age and then fall to approximately 50 ng/dl at 60 mo. The plasma T metabolic clearance rates (MCRT) and production rates (PRT) were measured in two rhesus infants at 1 and 6 mo of age to determine the mechanism of the observed increase in plasma T. While there was little change in the MCRT between 1 and 6 mo, PRT was much higher at 1 mo than at 60 mo of age. These observations are consistent with the hypothesis that the increased plasma testosterone levels in infant rhesus monkeys reflect an increased production of testosterone rather than an altered metabolic disposition of the hormone.     

Relation between average daily metabolic rate and resting metabolic rate of the mongolian gerbil (Meriones unguiculatus)

Summary Some early reports have claimed that the Mongolian gerbil is a diurnal rodent, but we found it to be active both night and day, being more active at night. A circadian rhythm was found both in locomotory activity under laboratory conditions and in average daily metabolic rate (ADMR).The ADMR of the Mongolian gerbil observed at 20° C in our study was 2.921 ml O₂/g·h which was near the value expected from Grodzinski's equation (ADMR=19.94 W^-0.50).Both ADMR and RMR were found to be negatively correlated with ambient temperature, with the slope of the regression line for ADMR being less than that for RMR. These two lines intersected at 20° C, lower below 20° C.According to Grodzinski, the ADMR is usually lower than RMR, but in our study the ADMR was found to be lower than the RMR only below 20° C, which suggests that the ambient temperature acts differently on ADMR and RMR. The temperature-dependent variation of both ADMR and RMR as well as their differences should be taken into account in the estimation of the productivity of animal population.     

Functional implication of the basal metabolic rate in homeothermic animals

Data on energetic profile of many species Passeriformes and Non-Passeriformes show that the basal metabolic rate (BMR) is strongly correlated with potential energy (MPE) and potential productive energy (PPE) (MPE is about 4BMR in all homeothermic animals). BMR is the minimal power of animal and strongly correlated with the daily work output, which may be determined by measuring total animal activity. Hence, BMR is the fundamental scale of power which determines the intensity of the actual interaction of an individual with the environment. The increase in BMR of a particular animal should rise the potential energy (MPE), potential productive energy (PPE), and the level of daily work output. BMR in Passerines birds is 1.3-1.5 fold higher than that in Non-Passerines and Mammals. Origin ofendothermy in the course of evolution should be associated with needs of general activity rather than with the requirements of thermoregulation.     

Phenotypic plasticity in the scaling of avian basal metabolic rate

Many birds exhibit short-term, reversible adjustments in basal metabolic rate (BMR), but the overall contribution of phenotypic plasticity to avian metabolic diversity remains unclear. The available BMR data include estimates from birds living in natural environments and captive-raised birds in more homogenous, artificial environments. All previous analyses of interspecific variation in BMR have pooled these data. We hypothesized that phenotypic plasticity is an important contributor to interspecific variation in avian BMR, and that captive-raised populations exhibit general differences in BMR compared to wild-caught populations. We tested this hypothesis by fitting general linear models to BMR data for 231 bird species, using the generalized least-squares approach to correct for phylogenetic relatedness when necessary. The scaling exponent relating BMR to body mass in captive-raised birds (0.670) was significantly shallower than in wild-caught birds (0.744). The differences in metabolic scaling between captive-raised and wild-caught birds persisted when migratory tendency and habitat aridity were controlled for. Our results reveal that phenotypic plasticity is a major contributor to avian interspecific metabolic variation. The finding that metabolic scaling in birds is partly determined by environmental factors provides further support for models that predict variation in scaling exponents, such as the allometric cascade model.