The evolution of air-breathing respiratory faculties in craniotes

The origin of lungs from a swim bladder, swim bladder from lungs, or both from a relatively undifferentiated respiratory pharynx remains unresolved. Once present, the lungs can be ventilated by a positive-pressure buccal pump, which can be easily derived from the gill ventilation sequence in a lungfish, or by negative-pressure aspiration. Although aspiration breathing is characteristic of amniotes, it has also been observed in a lungfish and body wall muscle contraction in response to respiratory stimuli has even been reported in lamprey larvae. The hypaxial body wall musculature used for aspiration breathing is also necessary for locomotion in most amniotes, just when respiratory demand is greatest. This paradox, called Carrier’s constraint, is a major limiting factor in the evolution of high-performance faculties, and the evolution of anatomical and physiological specializations that circumvent it characterize most major amniote groups. Serendipitous combinations have resulted in evolutionary cascades and high-performance groups such as birds and mammals. Complementing evolution are the capacities for acclimatization and adaptation not only in the structure and function of the gas exchanger, but also in the control of breathing and the composition of the blood.

Control of breathing in craniotes

Craniote gills are arranged sequentially along the pharynx and accordingly are ventilated from anterior to posterior by a wave of muscle contraction, beginning with the mouth. Each gill pair appears to have its own set of neurons in the brainstem that coordinate the muscle activity and stimulate the next gill pair in the sequence. This system appears to have been maintained from hagfish to teleosts. In tetrapods, on the other hand, various centres in the brainstem coordinate different phases of breathing: expiration, inspiration, and post-inspiration. The location of these centres in the brainstem is similar in amphibians and mammals. The stimulus for regulating ventilatory frequency in water-breathing species is oxygen, whereas for air-breathing species it is blood pH/PCO2—just as in invertebrates.

A primer on respiratory physiology

According to the principle ‘before you can do what you want to do, you always have to do something else’, this chapter first delves into the basics of respiratory physiology. It begins with summarizing the physical gas laws and their physiological applications to the core process of respiration: diffusion. The chapter finally arrives at introducing the different gas exchange models that can be observed in the various lineages of animals and the basics of ventilatory mechanics. Equipped with this knowledge, it is hoped that the reader will better understand the functional and evolutionary discussions of the respiratory faculties in the following chapters.

The bottom line

This chapter summarizes the most important aspects of the entire book. Writing an abstract of a summary can result in a ‘bouillon cube’ of information that is nearly incomprehensible, so this sticks to the most far-reaching observations and conclusions. The structure–function unit referred to here as the respiratory faculty did not just suddenly appear, but rather bits and pieces of it are recognizable even in most basally branching metazoan lineages. The use of mitochondria in an aerobic atmosphere to produce large amounts of energy-carrying molecules precipitated a kind of arms race, whereby the individuals that could compete better for food sources or become predatory could become part of an evolutionary cascade. These new animals moved into another realm, but the old ones did not necessarily disappear: they just did what they always did, maybe a little better. In the most diverse lineages of invertebrates and craniotes we see similar changes appearing: gills with counter-current exchange, highly specialized oxygen-carrying proteins, a partly or completely closed circulatory system that includes the gas exchange organs, lungs. The more extreme the grounds for specialization, the more similar are these structures and functions. Often the functional result remains unchanged or becomes improved while the anatomical cause changes dramatically, but just as often structures change little but minor functions become major ones: a phenomenon called exaptation. This book has looked at most major animal groups and these principles turn up everywhere. It talks about multidimensional forces at work in a multidimensional world, and respiration is the keystone to it all.

The evolution of water-breathing respiratory faculties in craniotes

The major components of the respiratory faculty (gill structure, muscular ventilation, central heart and erythrocyte-containing blood, and pH-sensitive control of breathing) appear to have been present in craniotes from the very beginning. But the details are so different in the most basally radiating group, hagfish, corroborating that they separated very early from the stem line. In the other groups, progressive changes are seen in the structure of the gills, heart, haemoglobin, as well as in the control of breathing. In particular, a major and progressive change in gill structure is seen when comparing sharks to teleosts, with several intermediary forms realized.

Respiratory faculties of aquatic craniotes

This chapter introduces the ‘who has what’ in terms of water-breathing respiratory faculties for craniotes. A branchial basket and a ventral heart or hearts that perfuse the branchial region with deoxygenated internal fluid is part of the bauplan of all chordates, including craniotes. Cilia ventilate the branchial region of extant non-craniote chordates, which are also predominantly sessile or planktonic filter feeders. In craniotes, the gills are the main gas exchange organs. They are ventilated by muscular activity and perfused with blood that contains haemoglobin in erythrocytes and flows in the opposite direction to the ventilated water (counter-current model). In spite of major differences in the structure of gills and the ventilatory apparatus among jawless craniotes, cartilaginous fish, and bony fish, the basic push–pull, constant, unidirectional flow respiratory mechanism remains unchanged (of course, with a few notable exceptions). In addition, both the blood and the structure of the gills may reflect adaptations of the respiratory faculty to habitual living conditions.

The evolution of water-breathing respiratory faculties in invertebrates

This chapter aims at piecing together the evolution of water breathing in invertebrates. Dedicated respiratory faculties, consisting of an external exchanger, an internal transport system (circulatory system or an equivalent), and some control element are first clearly recognizable among invertebrates in annelids, which excel in the number of different respiratory proteins they display. Molluscs and arthropods use primarily haemocyanin, each group showing evolutionary trends in respiratory proteins that have some bearing on the phylogenetic position. Each major group of molluscs has its own evolutionary story, but in general we see a reduction in the number of gills and often a release from bilateral symmetry. Among arthropods, crustaceans can develop gills on various parts of the legs and the body wall, each group showing a taxon-specific type. Arachnids and hexapods are primarily terrestrial, but several groups have independently and secondarily developed mechanisms for even long-term survival under water.

A very brief history of respiratory biology

A better understanding of what life is and how living organisms function has always been of crucial importance to humans, but ‘biology’ as a scientific discipline is quite young, the term being coined around 1800. Similarly, ‘respiratory biology’ as a discrete branch of biology is much younger and even today the term is not commonly used. However, the knowledge about life and the discovery and study of respiration as parts of other disciplines accumulated as a mosaic over the centuries. Some of the most important persons and their primary achievements in the field that we now call respiratory biology are summarized in this chapter.

The evolution of air-breathing respiratory faculties in invertebrates

This chapter aims at piecing together the evolution of air breathing in invertebrates, the main conclusion here being that it evolved independently several times. In molluscs alone, air breathing has evolved several times, but almost exclusively among snails. Among crustaceans, several groups of crabs have also independently developed terrestrial representatives and transitional stages, particularly in the control of breathing, are evident. Analysis of insects shows few recognizable evolutionary progressions: air sacs and different stigmatal closure mechanisms have appeared and disappeared numerous times, even within closely related groups. But other tracheate groups such as myriapods show an interesting correlation between the presence of tracheal lungs, which end in an open circulatory system, and tracheae that invade the tissue as in insects, and the presence or reduction of respiratory proteins. In arachnids a similar tendency is seen, and the most interesting developments were the (partial) replacement of a ‘perfectly good’ air-breathing organ (book lungs) by another one (tracheae).

Control of breathing in invertebrates

Every animal that has a respiratory faculty has some mechanism for regulating its perfusion and ventilation. A prerequisite for such regulation is some way of sensing internal and external levels of respiratory-relevant gases. The regulatory entities can be peripheral, central, or both. This chapter looks at the control of breathing in aquatic and terrestrial invertebrates and concludes that the main signal for aquatic species is oxygen, whereas the internal pH/PCO2 is most important for the control of air breathing, regardless of the phylogenetic group to which the animal may belong.