Evolution of air breathing: oxygen homeostasis and the transitions from water to land and sky

Abstract

Life originated in anoxia, but many organisms came to depend upon oxygen for survival, independently evolving diverse respiratory systems for acquiring oxygen from the environment. Ambient oxygen tension (PO2) fluctuated through the ages in correlation with biodiversity and body size, enabling organisms to migrate from water to land and air and sometimes in the opposite direction. Habitat expansion compels the use of different gas exchangers, for example, skin, gills, tracheae, lungs, and their intermediate stages, that may coexist within the same species; coexistence may be temporally disjunct (e.g., larval gills vs. adult lungs) or simultaneous (e.g., skin, gills, and lungs in some salamanders). Disparate systems exhibit similar directions of adaptation: toward larger diffusion interfaces, thinner barriers, finer dynamic regulation, and reduced cost of breathing. Efficient respiratory gas exchange, coupled to downstream convective and diffusive resistances, comprise the "oxygen cascade"-step-down of PO2 that balances supply against toxicity. Here, we review the origin of oxygen homeostasis, a primal selection factor for all respiratory systems, which in turn function as gatekeepers of the cascade. Within an organism's lifespan, the respiratory apparatus adapts in various ways to upregulate oxygen uptake in hypoxia and restrict uptake in hyperoxia. In an evolutionary context, certain species also become adapted to environmental conditions or habitual organismic demands. We, therefore, survey the comparative anatomy and physiology of respiratory systems from invertebrates to vertebrates, water to air breathers, and terrestrial to aerial inhabitants. Through the evolutionary directions and variety of gas exchangers, their shared features and individual compromises may be appreciated.

Figure 1

(A) Origin of oxygen and reactive oxygen species (ROS). Molecular O₂ is generated during photolysis (ultraviolet range) and photosynthesis (visible light range via chlorophyll). (B) Photosynthesis and irradiation are equivalent processes that successively remove electrons from water to yield O₂. Aerobic respiration is the reciprocal process that adds electrons to O₂ to generate water. The same intermediate ROS are involved in all of these processes. Adapted from Lane (407).

Figure 2

(A) Transitional metals ions functioned as signaling and antioxidant molecules in the earliest organisms. A molecular cage, for example, prophyrin ring, trapped these metal ions, for example, forming a heme molecule. Adding various polypeptides modulated the action of heme, resulting in heme proteins. By exaptation heme proteins participated in the neutralization of reactive O₂ species as well as the sensing, storage, transport, and release of O₂. (B) Structure of heme (containing iron) is remarkably similar to that of chlorophyll (containing magnesium).

Figure 3

Heme proteins trace to the Last Universal Common Ancestor (LUCA), which is thought to have arisen approximately 3.8 billion years ago and evolved into the three domains of life: bacteria, archea, and eucarya. Adapted from the phylogenetic tree of all extant organisms based on 16S rRNA gene sequence data, originally proposed by Woese et al. (836).

Figure 4

A general model of early evolution and atmospheric O₂ concentration. Last Universal Common Ancestor (LUCA) was anaerobic and unicellular, but possessed heme proteins and their equivalents for antioxidation and reactive O₂ species-mediated cell signaling and possibly ATP production. Photosynthesis by cyanobacteria led to O₂ accumulation, which was initially stored in rocks and sediments but later enriched the atmosphere. Eukaryotic plant and animal cells evolved that can more efficiently produce and utilize O₂, leading to multicellular organisms of increasing complexity. Around 500 Ma, atmospheric O₂ level reached the contemporary range, coinciding with an explosive appearance of terrestrial plants and animals.

Figure 5

Phanerozoic time line shows atmospheric O₂ concentration and major evolutionary events, including major mass extinctions (indicated by *: Ordovician-Silurian, late Permian, and Cretaceous-Paleogene). Based on data from various sources (55,335,775). See text for explanation.

Figure 6

Oxygen cascade—the series of convective, diffusive, and biochemical barriers that progressively lower O₂ tension until it reaches the near-anoxic level necessary for optimal mitochondrial function within cells.

Figure 7

Lungs of isopods, a taxon of crustaceans that include woodlice and pill bugs. From dry to humid environments the size of the lungs and the type of embedding into the body is reduced. After Hoese (328).

Figure 8

Phylogeny of the the Arachnida, which includes spiders, scorpions, ticks, mites, harvest-men, and their relatives. This tree relates especially to the feature “loss of lungs.” Whether this loss really happened remains speculative. After Weygoldt und Paulus (820),

Figure 9

Lungs and tracheae in arachnids. Lungs are present in Scorpiones, Amblipygi, and Uropygi and also spiders (Araneae). In the other groups a tracheal system is present. After various authors (227, 365, 366, 695). A atrium of the tracheae, Ch chelicera, OpSp opisthosomal spiracle, PrSp prosomal spiracle, and STr secondary tracheae.

Figure 10

Lungs, tracheae, and spiracles in spiders. Orthognatha species possess two pairs of book lungs lying directly behind the thorax. In Dysdera, tracheal spiracles are situated just behind the lungs, which are markedly reduced. In most Araneae, for example, wolf spiders or garden spiders and also shown in the spider in the middle of the figure, two lungs and a tracheal system with four simple tube tracheae are realised. In Misumena, for example, crab spiders, tracheae are restricted to the pleon. In Argyroneta, for example, water spider, lungs are completely reduced and tracheae fill the entire body. In Nops only tracheae exist, while in Pholcus only one pair of lungs is realised. In jumping spiders, shown for Salticus and Euophrys, the secondary tracheae reach into the thorax. Two electron micrographs show sections through the thorax with tracheae in the gut epithelium (Gu) and the nervous system (NS). At tracheal atrium, He heart, Lu lungs, Mu muscles, Ptr primary tracheae, and STr secondary tracheae.

Figure 11

Tracheae and spiracles in myriapods. A Lithobius (Chilopoda, Lithobiomorpha), B Scutigerella (Progoneata, Symphyta), C and D Scutigera (Chilopoda, Notostigmophora) the dorsal side of the animal with spiracles (C) and one segment is shown in detail (D). Adapted from Westheide and Rieger (817).

Figure 12

Discontinuous respiration in insects. A Hyalophora cecropia at the end of diapause, a stage of dormancy, B Periplaneta americana resting at 20°C, after Kestler (371).

Figure 13

Hagfish. Schematic frontal section of a gill pouch from the left side of a hagfish shows the path of water flow (black area and white arrows) and blood flow (black arrows). Stippled blood vessels indicate oxygen-poor blood. After Perry (615), with kind permission from Springer Science+Business Media.

Figure 14

Lamprey. Schematic frontal section of a gill pouch from the left side of a lamprey, during expiration (A) and inspiration (B). The + and − signs indicate pressure. Note pressure reduction as water leaves the gill pouch during expiration (A). Black arrows show path of water flow. After Perry (615), with kind permission from Springer Science+Business Media.

Figure 15

Shark gill. Schematic section of a gill element in frontal plane from the left side of a shark, showing (A) most important anatomical structures, (B) terminology and functional units. (C) Block diagram and cross section of gill filaments. Black arrows indicate direction of water flow; white arrows, blood flow. After Perry (615), based on Kempton (368) and Mallat (508) with kind permissions from Springer Science+Business Media, the Marine Biological Laboratory, Woods Hole, MA, and John Wiley & Sons, Inc.

Figure 16

Fish breathing. Comparison of breathing movements in sharks (A,B) and bony fishes (C,D), schematically illustrated in frontal sections. Left-hand diagrams indicate expiration; right-hand, inspiration. The + and − signs indicate pressure. Thick arrows indicate movement of external body wall or operculum; thin arrows, direction of water flow. After Perry (615), with kind permission from Springer Science+Business Media.

Figure 17

Teleost gill. Semischematic diagram of a portion of teleost gill arch, showing filaments, lamellae, blood vessels, and supporting elements. Thick arrow, direction of water flow; thin arrow, blood flow. After Perry (615), with kind permission from Springer Science+Business Media.

Figure 18

Gill pouches. Frontal views of the posterior pharynx region in a sturgeon (A,B) and a gymnophione amphibian (C,D). Note the dorsal swimbladder anlage (Sb) in the sturgeon and the ventral paired origin of the lungs (Lu) in the amphibian, in this case with the formation of a pseudotrachea (Pt). Abbreviations: Dl, dorsolateral ridge: Dm, dorsomedial ridge; Es, esophagus; St, stomach. Numbers represent gill pouch numbers. After Perry (611), with permission from Elsevier.

Figure 19

Respiratory pharynx. Relationships of the major lineages of jawed vertebrates (Gnathostomata) and a plausible scenario for the origin of their derivatives of the posterior pharynx. Note that lungs (L, L′) and swimbladder (SB, SB′) each originated twice, either directly from the respiratory pharynx (RP), or from the pulmonoid swimbladder (PSB) in the more derived ray-finned fishes (Actinopterygii). The RP most likely was present in the most basal bony fishes (Osteichtyes = Osteognathostomata), but could even predate the origin of the cartilaginous fishes (Chondrichthyes). Upper row: Schematic cross-sections show the origin of the lungs/swimbladder as well as their principal blood supply. Swimbladder and pulmonary veins are not labeled. Abbreviations: BA6, artery of the sixth branchial arch; FL, fat filled lung; RL, right lung. After Perry and Sander (620), with permission from Elsevier.

Figure 20

Parenchyma. Semischematic diagram of lung parenchyma of an amphibian or reptile is shown. Capillary net is not shown on surface of vertical septum (S). Abbreviations: A, artery; C, capillary; Ce, ciliated epithelium; Ed, edicula; Is, intercapillary space; Sm, smooth muscle; St, striated muscle; Ps, perivascular lymphatic space; Tr, trabecula; V, vein. After Perry (611), with permission from Elsevier.

Figure 21

Interaction of central neural control element, active pump, passive pump, and exchanger in an amniote respiratory apparatus. Light gray arrows indicate neural control pathways; dark gray arrow, biomechanical force; black arrows, oxygen-poor blood; and white arrows, oxygen-rich blood (Lambertz and Perry, original).

Figure 22

Macroscopic structure. Schematic diagram of the three principal macroscopic variables in amniote lung structure: type of lung, type of parenchyma, and parenchymal distribution. After Perry (612) with permission from Taylor and Francis.

Figure 23

Amniote tree that shows the relationships among the major amniote lineages, their principal lung types, and the occurrence of a postpulmonary septum (PPS). In underlined taxa all representatives possess a PPS, whereas in the Iguania only the Chamaeleonidae do (indicated by parentheses). For taxa with a dashed underline, the situation remains unclear and mainly depends on the unknown plesiomorphic condition for the Lepidosauria (indicated by arrows). Either (scenario 1), a PPS was present and was independently lost in most groups (black squares) but retained in varanoids (open square) and chamaeleonids (black and white square), or (scenario 2, inset) was plesiomorphically not present and reevolved independently in varanoids (red square) and chamaeleonids (red and white square). After Lambertz et al. (402) with permission from Elsevier.

Figure 24

Body wall muscles of tuatara (Sphendon punctatus) in lateral view shows sequential removal of muscle layers from A to F. Note that several groups are disposed in deep and superficial layers, UP means uncinate processes. After Perry et al. (621) with permission from Elsevier.

Figure 25

Generalized amniote embryo in frontal (A) and sagittal (B) sections shows the position of anlagen from which the postpulmonary (PPS) and posthepatic septa (PHS) develop. Gall bladder is shown lying in the peritoneal cavity (e.g., archosaurs). In teiioid lizards, PHS develops from a mesentery fold rather than from the capsula fibrosa of the liver, hence the gall bladder is included in the pleurohepatic cavity. Dorsal and ventral mesopneumonia are shown at the left. Note that the PPS and the D. cuvieri encircle the developing lungs. After Perry et al. (621) with permission from Elsevier.

Figure 26

Mammalian lung. (A) Latex cast of the airway system of the pig, Sus scrofa showing dichotomous branching. Tr, trachea. Scale bar, 2 cm. (B) Latex cast of the lung of a baboon, Papio anubis, showing an acinus supplied with air by a respiratory bronchus (RB). Al, alveoli. Scale bar, 100 μm. (C) Latex cast of the lung of the pig, Sus scrofa, showing spherical alveoli (Al). Arrows, interalveolar pores. Scale bar, 0.5 mm. (D) Blood-gas barrier of the lung of a vervet monkey, Chlorocebus aethiops, showing an epithelial cell (arrows), basement membrane (asterisks), and an endothelial cell (stars). Al, alveolar space; BP, blood plasma; RBC, red blood cell. Scale bar, 0.5 μm. (E) Ciliated epithelial cells (CC) line the upper airways of the vervet monkey, C. aethiops. RBC, red blood cells in a subepithelial blood vessel; BM, basement membrane; arrows, cilia. Scale bar, 0.05 mm. (F) Pulmonary macrophage on the alveolar surface of the lung of the vervet monkey, C. aethiops, showing filopodia (arrows) that allow the cells to move, and cytoplasmic vacuoles (asterisks) containing lytic enzymes. RBC, red blood cells. Scale bar, 5 μm. (G) Alveolar capillary of the lung of the baboon, Papio anubis, showing a thick side (white asterisk) containing supporting connective tissue (mainly collagen) and a thin side (box) that is predominantly involved in gas exchange. RBC, red blood cell; Al, alveoli. Scale bar, 10 μm. (H) Alveolar surface showing a granular pneumocyte (type-II cell) (II) and a squamous pneumocyte (type-I cell) (I); both are encircled to show the surfaces they cover. Arrows, interalveolar pore. Scale bar, 10 μm. (I) Type-II (granular) pneumocyte of the lung of the vervet monkey, C. aethiops, attached to a capillary containing RBCs. The type-II cell contains osmiophilic lamellated bodies (arrows) that produce precursors of surfactant. Al, alveolus; stars, mitochondria; boxed areas, blood-gas barrier. Scale bars, 10 μm.

Figure 27

Mammalian lung—continued. (A) Close-up of a type-II cell from the lung of the vervet monkey, Chlorocebus aethiops, secreting surfactant (arrow) onto the alveolar surface (Al). Stars, mitochondria. Scale bar, 0.1 μm. (B and C) Branching pattern of the pulmonary arterial (B) and venous (C) systems of the pig, Sus scrofa. The airway (see A) and the arterial and venous systems pattern each other. Scale bars, 2 cm. (D) Close-up of the surface of an alveolus in the lung of the baboon, Papio anubis, showing blood capillaries (BC) protruding into the alveolar space. Arrows, cellular junctions of type-I pneumocytes. Scale bar, 40 μm. (E) Blood capillaries (BC) protruding into the alveolar space (Al) contain red blood cells (RBC) and are associated with elastic tissue (arrows) and pericytes (stars). Circle, surface lining fluid washed off during tissue preparation. Scale bar, 30 μm.

Figure 28

Developing lung of the domestic fowl. (A) Lung bud on embryonic day 3.5. Epithelial cells (EC) extend into surrounding mesenchymal cells (MC). Scale bar, 25 μm. (B) Embryonic day 8. The lung (Ln) begins to engage the ribs (arrows) on its vertebral and costal surfaces. (C) Longitudinal section of an embryonic lung (day 9) shows deep impressions (costal sulci) made by the ribs and the vertebrae (arrows). (D) On embryonic day 10, the primary bronchus (PB) giving rise to secondary bronchi (SB). Arrows, blood vessels. (E) On embryonic day 11, a cluster of ECs is forming a parabronchus surrounded by MC, some of which attach onto the formative basement membrane (stars). Both epithelial and the mesenchymal cells express basic FGF-2 (brown color). Scale bar, 20 μm. (F and G) On embryonic day 12, parabronchi show a central lumen (PL) surrounded by ECs attached onto a basement membrane (arrows). BV, blood vessel; stars, mesenchymal cells attaching onto the outer aspect of the basement membrane. Scale bar (F), 20 μm. (H) A parabronchus on embryonic day 14 shows atria (arrows) projecting into gas-exchange tissue (ET). PL, parabronchial lumen; stars, atrial muscles; dashed curve, interparabronchial septum. Scale bar, 50 μm. (I) On embryonic day 14, a parabronchial lumen opens into an atrium (arrow). The atria (At) give rise to infundibula (If) and air capillaries (asterisks). PL, parabronchial lumen; AM, atrial muscles; circles, type-II pneumocytes confined to the atria and infundibulae (dashed line). Scale bar, 20 μm.

Figure 29

Developing lung (A-C) and mature lung (D-I) of the domestic fowl. (A) The lung on embryonic day 10 shows formative air sacs (arrows) and airways (encircled area) that express bFGF-2 (red). Pr, parabronchi; SB, secondary bronchi. Scale bar, 1 cm. (B) Mesenchymal cells (MC) accumulate hemoglobin (arrows) and transform into nucleated erythroblasts (RBC) on embryonic day 7. Scale bar, 15 μm. (C) Mesenchymal cells differentiate into an erythroblast (star) and angioblasts (arrows) on embryonic day 8. Circles, filopodia. (D) Lateral (side) view of the latex cast of lung-air sac system, showing the relatively smaller lung (asterisk) intercalated between large air sacs (numbered from i-v). Circles, ostia (connections between the lung and air sacs); arrow, trachea. The paired air sacs are: i, abdominal; ii, caudal thoracic; iii, cranial thoracic; iv, interclavicular; v, cervical. Scale bars, 2 cm. (E) Dorsal view of the lung of a juvenile ostrich, Struthio camelus, showing deep vertebral and costal impressions (arrows). Tr, trachea; circles, extrapulmonary primary bronchi. Scale bar, 5 cm. (F) Medial view of the lung showing the costal impressions (arrows) and the elaborate airway system. MVSB, medioventral secondary bronchi; PB, primary bronchus; PPPR, paleopulmonic parabronchi; NPPR, neopulmonic parabronchi; asterisk, ostium. Scale bars, 1 cm. (G) The hexagonal (geodesic) shapes of parabronchi (dashed outlines), parabronchial lumen (PL), exchange tissue (ET), atria (arrows), interparabronchial blood vessels (asterisks), and the interparabronchial septum (circle). Scale bar, 0.1 mm. (H) Latex cast of the arterial vasculature of a parabronchus. Deoxygenated blood flows from peripheral interparabronchial arteries (asterisks) into intraparabronchial arteries (arrows) that enter the exchange tissue. Dashed area, parabronchial lumen. Scale bar, 0.1 mm. (I) Close-up of atria (dashed outlines), separated by atrial muscles (AM), giving rise to infundibulae (If). Scale bar, 1 mm.

Figure 30

Mature lung of the domestic fowl—continued. (A) Latex cast of air capillaries (ACs) showing areas where they anastomose (circles) and interdigitate with blood capillaries (arrows). Scale bar, 25 μm. (B) Latex cast of the blood capillaries (BCs) intertwining with ACs. Scale bar, 20 μm. (C) The network of ACs and BCs containing red blood cells (RBCs). Arrows, blood-gas barrier. Scale bar, 10 μm. (D) The blood-gas barrier (arrow) separates ACs from BCs. Scale bars, 0.5 μm.

Figure 31

Cross-section of histological preparation of a parabronchus from lung of a juvenile ostrich. From the parabronchial lumen (PL), air convectively flows into atria (black dots) that give rise to infundibulae that in turn to air capillaries where air moves by diffusion. Deoxygenated blood flows from peripheral interparabronchial artery (star) into an intraparabronchial artery (asterisk), which gives rise to arterioles and blood capillaries in the exchange tissue (ET). Blood flow in ET (black arrow) is orthogonal (perpendicular) to the axial air flow along parabronchial lumen (dashed arrow in the parabronchial lumen): this forms the crosscurrent system. In the exchange tissue, the flow of blood in the ET (black arrow) runs in opposite direction to that of air (white arrow): this forms the countercurrent-like system.

Figure 32

Mature lung of the domestic fowl. (A) Double latex injection preparation (latex was injected into the airway- and the arterial vascular systems) to show the spatial relationships of the structural components of the lung. It shows the perpendicular “cross-current” disposition between the direction of airflow in the parabronchial lumen (large dashed open arrow) and that of deoxygenated blood (smaller solid black arrows), via the intraparabronchial arteries (asterisks). The circled areas show sites where blood capillaries (BCs) contact the air capillaries (ACs), which project in opposite direction from the infundibulae that in turn arise from the atria (At), forming the countercurrent-like arrangement. Scale bar, 0.5 mm. See also schematic diagrams (Figs. 33 and 34) for orientation. (B) Double latex injection preparation (latex was injected into the airway- and the arterial vascular systems) to show the spatial relationships of the structural components of the lung. It shows the perpendicular “cross-current” disposition between the direction of air flow in the parabronchial lumen (large dashed open arrow) and that of deoxygenated blood (smaller solid black arrow) from an interparabronchial artery (asterisk) via intraparabronchial arteries (stars). The boxed (enclosed) areas show sites where blood capillaries (BCs) contact the air capillaries (ACs), which project in opposite direction, that is, from the infundibulae that in turn arise from the atria (At), forming the countercurrent-like arrangement. Scale bar, 0.2 mm. See also schematic diagrams (Figs. 33 and 34) for orientation.

Figure 33

“Countercurrent-like” and “cross-current” gas exchange in the avian lung. Schematic illustration of air flow (black arrows) through the parabronchial lumen and flow of deoxygenated blood (brown arrows) from the interparabronchial arteries into intraparabronchial arteries that give rise to arterioles and blood capillaries. Oxygenated blood (red arrows) is conveyed by intraparabronchial and interparabronchial veins. The orthogonal directions of air flow within parabronchial lumen relative to the flow of deoxygenated blood into gas-exchange tissue forms the cross-current system. The opposed directions of air flow by diffusion in the air capillaries across the exchange tissue away from parabronchial lumen and that of blood flow in the blood capillaries toward the parabronchial lumen forms the countercurrent-like system.

Figure 34

“Multicapillary serial arterialization system” in the avian lung. Schematic illustration of the multicapillary serial arterialization system between the blood capillaries and air capillaries in the exchange tissue: the respiratory components exchange gases at an infinite number of contact points (dashed circle) along the length of a parabronchus. Increasing shading intensity (red) from the intraparabronchial artery (deoxygenated blood) across the blood capillaries to the intraparabronchial vein (oxygenated blood) illustrates the oxygenation of blood during transit across the exchange tissue and the parabronchus. Increasing shading intensity (gray) in the parabronchial lumen and the air capillaries illustrates the vitiation of air, that is, accumulation of carbon dioxide in respiratory air. The large arrows show the flow of air in a mediodorsal secondary bronchus (arrow with continuous line), in a parabronchus (arrow with short dashes), and in a medioventral secondary bronchus (arrow with long dashes).