Symmorphosis and the insect respiratory system: a comparison between flight and hopping muscle.

Weibel and Taylor's theory of symmorphosis predicts that the structural components of the respiratory system are quantitatively adjusted to satisfy, but not exceed, an animal's maximum requirement for oxygen. We tested this in the respiratory system of the adult migratory locust Locusta migratoria by comparing the aerobic capacity of hopping and flight muscle with the morphology of the oxygen cascade. Maximum oxygen uptake by flight muscle during tethered flight is 967±76 µmol h(-1) g(-1) (body mass specific, ±95% confidence interval CI), whereas the hopping muscles consume a maximum of 158±8 µmol h(-1) g(-1) during jumping. The 6.1-fold difference in aerobic capacity between the two muscles is matched by a 6.4-fold difference in tracheole lumen volume, which is 3.5×10(8)±1.2×10(8) µm(3) g(-1) in flight muscle and 5.5×10(7)±1.8×10(7) µm(3) g(-1) in the hopping muscles, a 6.4-fold difference in tracheole inner cuticle surface area, which is 3.2×10(9)±1.1×10(9) µm(2) g(-1) in flight muscle and 5.0×10(8)±1.7×10(8) µm(2) g(-1) in the hopping muscles, and a 6.8-fold difference in tracheole radial diffusing capacity, which is 113±47 µmol kPa(-1) h(-1) g(-1) in flight muscle and 16.7±6.5 µmol kPa(-1) h(-1) g(-1) in the hopping muscles. However, there is little congruence between the 6.1-fold difference in aerobic capacity and the 19.8-fold difference in mitochondrial volume, which is 3.2×10(10)±3.9×10(9) µm(3) g(-1) in flight muscle and only 1.6×10(9)±1.4×10(8) µm(3) g(-1) in the hopping muscles. Therefore, symmorphosis is upheld in the design of the tracheal system, but not in relation to the amount of mitochondria, which might be due to other factors operating at the molecular level.

Scaling of resting and maximum hopping metabolic rate throughout the life cycle of the locust Locusta migratoria.

The hemimetabolous migratory locust Locusta migratoria progresses through five instars to the adult, increasing in size from 0.02 to 0.95 g, a 45-fold change. Hopping locomotion occurs at all life stages and is supported by aerobic metabolism and provision of oxygen through the tracheal system. This allometric study investigates the effect of body mass (Mb) on oxygen consumption rate (MO2, µmol h(-1)) to establish resting metabolic rate (MRO2), maximum metabolic rate during hopping (MMO2) and maximum metabolic rate of the hopping muscles (MMO2,hop) in first instar, third instar, fifth instar and adult locusts. Oxygen consumption rates increased throughout development according to the allometric equations MRO2=30.1Mb(0.83±0.02), MMO2=155Mb(1.01±0.02), MMO2,hop=120Mb(1.07±0.02) and, if adults are excluded, MMO2,juv=136Mb(0.97±0.02) and MMO2,juv,hop=103Mb(1.02±0.02). Increasing body mass by 20-45% with attached weights did not increase mass-specific MMO2 significantly at any life stage, although mean mass-specific hopping MO2 was slightly higher (ca. 8%) when juvenile data were pooled. The allometric exponents for all measures of metabolic rate are much greater than 0.75, and therefore do not support West, Brown and Enquist's optimised fractal network model, which predicts that metabolism scales with a 3/4-power exponent owing to limitations in the rate at which resources can be transported within the body.

Symmorphosis and the insect respiratory system: allometric variation.

Taylor and Weibel's theory of symmorphosis predicts that structures of the respiratory system are matched to maximum functional requirements with minimal excess capacity. We tested this hypothesis in the respiratory system of the migratory locust, Locusta migratoria, by comparing the aerobic capacity of the jumping muscles with the morphology of the oxygen cascade in the hopping legs using an intraspecific allometric analysis of different body mass (M(b)) at selected juvenile life stages. The maximum oxygen consumption rate of the hopping muscle during jumping exercise scales as M(b)(1.02±0.02), which parallels the scaling of mitochondrial volume in the hopping muscle, M(b)(1.02±0.08), and the total surface area of inner mitochondrial membrane, M(b)(0.99±0.10). Likewise, at the oxygen supply end of the insect respiratory system, there is congruence between the aerobic capacity of the hopping muscle and the total volume of tracheoles in the hopping muscle, M(b)(0.99±0.16), the total inner surface area of the tracheoles, M(b)(0.99±0.16), and the anatomical radial diffusing capacity of the tracheoles, M(b)(0.99±0.18). Therefore, the principles of symmorphosis are upheld at each step of the oxygen cascade in the respiratory system of the migratory locust.

Moulting of insect tracheae captured by light and electron-microscopy in the metathoracic femur of a third instar locust Locusta migratoria.

The insect tracheal system is an air-filled branching network of internal tubing that functions to exchange respiratory gases between the tissues and the environment. The light and electron-micrographs presented in this study show tracheae in the process of moulting, captured from the metathoracic hopping femur of a juvenile third instar locust (Locusta migratoria). The images provide evidence for the detachment of the cuticular intima from the tracheal epithelial cells, the presence of moulting fluid between the new and old cuticle layers, and the withdrawal of the shed cuticular lining through larger upstream regions of the tracheal system during moulting. The micrographs also reveal that the cuticular intima of the fine terminal branches of the tracheal system is cast at ecdysis. Therefore, the hypothesis that tracheoles retain their cuticle lining at each moult may not apply to all insect species or developmental stages.

Role of sphingosine kinase 1 in allergen-induced pulmonary vascular remodeling and hyperresponsiveness.

BACKGROUND: Immunologic processes might contribute to the pathogenesis of pulmonary arterial hypertension (PAH), a fatal condition characterized by progressive pulmonary arterial remodeling, increased pulmonary vascular resistance, and right ventricular failure. Experimental allergen-driven lung inflammation evoked morphologic and functional vascular changes that resembled those observed in patients with PAH. Sphingosine kinase 1 (SphK1) is the main pulmonary contributor to sphingosine-1-phosphate (S1P) synthesis, a modulator of immune and vascular functions. OBJECTIVE: We sought to investigate the role of SphK1 in allergen-induced lung inflammation. METHODS: SphK1-deficient mice and C57Bl/6 littermates (wild-type [WT] animals) were subjected to acute or chronic allergen exposure. RESULTS: After 4 weeks of systemic ovalbumin sensitization and local airway challenge, airway responsiveness increased less in SphK1(-/-) compared with WT mice, whereas pulmonary vascular responsiveness was greatly increased and did not differ between strains. Acute lung inflammation led to an increase in eosinophils and mRNA expression for S1P phosphatase 2 and S1P lyase in lungs of WT but not SphK1(-/-) mice. After repetitive allergen exposure for 8 weeks, airway responsiveness was not augmented in SphK1(-/-) or WT mice, but pulmonary vascular responsiveness was increased in both strains, with significantly higher vascular responsiveness in SphK1(-/-) mice compared with that seen in WT mice. Increased vascular responsiveness was accompanied by remodeling of the small and intra-acinar arteries. CONCLUSION: : The data support a role for SphK1 and S1P in allergen-induced airway inflammation. However, SphK1 deficiency increased pulmonary vascular hyperresponsiveness, which is a component of PAH pathobiology. Moreover, we show for the first time the dissociation between inflammation-induced remodeling of the airways and pulmonary vasculature.

Development of maximum metabolic rate and pulmonary diffusing capacity in the superprecocial Australian Brush Turkey Alectura lathami: an allometric and morphometric study.

The Australian Brush Turkey Alectura lathami is a member of the Megapodiidae, the mound-building birds that produce totally independent, "superprecocial" hatchlings. This study examined the post-hatching development of resting and maximal metabolic rates, and the morphometrically determined changes in pulmonary gas exchange anatomy, in chicks during 3.7 months of growth from hatchlings (122 g) to subadults (1.1 kg). Allometric equations of the form y=aM(b) related gas exchange variables (y) to body mass (M, g). Metabolic rates were measured with open-flow respirometry (mL O2 min(-1)) of chicks resting in the dark and running above the aerobic limit on a treadmill. Resting metabolic rate (RMR=0.02 M(0.99)) and maximal metabolic rate (MMR=0.05 M(1.07)) scaled with exponents significantly above those of interspecific allometries of adult birds. However MMR was below that expected for other species of adult birds in flapping flight, consistent with the Brush Turkey's ground-dwelling habits. Total lung volumes (mL) increased faster than isometrically (V(L)=0.0075 M(1.19)), as did the surface area (cm(2)) of the blood-gas barrier (S(t)=7.80 M(1.23)), but the data overlapped those of adult species. Harmonic mean thickness of the blood-gas barrier was independent of body size (mean tau(ht),=0.39 microm) and was about twice that expected for flying birds. Diffusing capacity (mL O2 min(-1) kPa(-1)) of the blood-gas tissue barrier increased faster than isometrically (Dto2=0.049 M(1.23)); in hatchling Brush Turkeys, it was about 30% expected for adult birds, but this difference disappeared when they became subadults. When compared to altricial Australian pelicans that hatch at similar body masses, superprecocial Brush Turkeys had higher MMR and higher Dto2 at the same body size. A parallel allometry between MMR and Dto2 in Brush Turkeys and pelicans is consistent with the concept of symmorphosis during development.

Adhesion is prerequisite, but alone insufficient, to elicit stem cell pluripotency.

Primitive mammalian neural stem cells (NSCs), arising during the earliest stages of embryogenesis, possess pluripotency in embryo chimera assays in contrast to definitive NSCs found in the adult. We hypothesized that adhesive differences determine the association of stem cells with embryonic cells in chimera assays and hence their ability to contribute to later tissues. We show that primitive NSCs and definitive NSCs possess adhesive differences, resulting from differential cadherin expression, that lead to a double dissociation in outcomes after introduction into the early- versus midgestation embryo. Primitive NSCs are able to sort with the cells of the inner cell mass and thus contribute to early embryogenesis, in contrast to definitive NSCs, which cannot. Conversely, primitive NSCs sort away from cells of the embryonic day 9.5 telencephalon and are unable to contribute to neural tissues at midembryogenesis, in contrast to definitive NSCs, which can. Overcoming these adhesive differences by E-cadherin overexpression allows some definitive NSCs to integrate into the inner cell mass but is insufficient to allow them to contribute to later development. These adhesive differences suggest an evolving compartmentalization in multipotent NSCs during development and serve to illustrate the importance of cell-cell association for revealing cellular contribution.

Developmental allometry of pulmonary structure and function in the altricial Australian pelican Pelecanus conspicillatus.

Quantitative methods have been used to correlate maximal oxygen uptake with lung development in Australian pelicans. These birds produce the largest altricial neonates and become some of the largest birds capable of flight. During post-hatching growth to adults, body mass increases by two orders of magnitude (from 88 g to 8.8 kg). Oxygen consumption rates were measured at rest and during exposure to cold and during exercise. Then the lungs were quantitatively assessed using morphometric techniques. Allometric relationships between body mass (M) and gas exchange parameters (Y) were determined and evaluated by examining the exponents of the equation Y=aM(b). This intraspecific study was compared to interspecific studies of adult birds reported in the literature. Total lung volume scales similarly in juvenile pelicans (b=1.05) as in adult birds (b=1.02). However, surface area of the blood-gas barrier greatly increases (b=1.25), and its harmonic mean thickness does not significantly change (b=0.02), in comparison to exponents from adult birds (b=0.86 and 0.07, respectively). As a result, the diffusing capacity of the blood-gas tissue barrier increases much more during development (b=1.23) than it does in adult birds of different sizes (b=0.79). It increases in parallel to maximal oxygen consumption rate (b=1.28), suggesting that the gas exchange system is either limited by lung development or possibly symmorphic. The capacity of the oxygen delivery system is theoretically sufficient for powered flight well in advance of the bird's need to use it.