Air-breathing adaptation in a marine Devonian lungfish

Abstract

Recent discoveries of tetrapod trackways in 395 Myr old tidal zone deposits of Poland (Niedźwiedzki et al . 2010 Nature 463 , 43–48 ( doi:10.1038/nature.08623 )) indicate that vertebrates had already ventured out of the water and might already have developed some air-breathing capacity by the Middle Devonian. Air-breathing in lungfishes is not considered to be a shared specialization with tetrapods, but evolved independently. Air-breathing in lungfishes has been postulated as starting in Middle Devonian times ( ca 385 Ma) in freshwater habitats, based on a set of skeletal characters involved in air-breathing in extant lungfishes. New discoveries described herein of the lungfish Rhinodipterus from marine limestones of Australia identifies the node in dipnoan phylogeny where air-breathing begins, and confirms that lungfishes living in marine habitats had also developed specializations to breathe air by the start of the Late Devonian ( ca 375 Ma). While invasion of freshwater habitats from the marine realm was previously suggested to be the prime cause of aerial respiration developing in lungfishes, we believe that global decline in oxygen levels during the Middle Devonian combined with higher metabolic costs is a more likely driver of air-breathing ability, which developed in both marine and freshwater lungfishes and tetrapodomorph fishes such as Gogonasus .

Evolution of the Cardiorespiratory System in Air-Breathing Fishes

“…The above reasoning leads to the idea that double circulation in vertebrates initially evolved as a means of reducing oxygen loss to hypoxic surrounding water, in which air breathing probably evolved (Graham 1997;Clack 2002Clack , 2007Clement and Long 2010). Physiological measurements must be made to clarify whether double circulation occurs or not in modern airbreathing fishes.…”

“…Recent findings of new fossil records have substantially expanded our knowledge of osteological transformation during the fish-tetrapod transition that occurred in the Devonian period and inspired some new ideas about environmental settings in which the transition occurred (Clack 2002(Clack , 2007Daeschler et al 2006;Shubin et al 2006;Clement and Long 2010;Laurin 2010;Niedźwiedzki et al 2010). Nevertheless, those findings can give little insight into the question of how the cardiorespiratory system was transformed during the invasion of land by vertebrates.…”

The salmon, the lungfish (or the coelacanth) and the cow: a revival?

“…But while the ability of dipnoans to breath air has been in existence in some capacity since the Middle Devonian (Clement & Long, 2010), mandatory air ventilation, accompanied by a number of physiological and anatomical modifications, as seen in the extant dipnoans Lepidosiren and Protopterus, is likely to have appeared much later. Based primarily on broader comparisons including fossils, the similarities in air-breathing between Dipnoi and Tetrapoda were, consequently, rejected as synapomorphies and deemed non-homologous (cf.…”

“…Therefore, taking into account that Latimeria is understood to comprise highly divergent, water-breathing fishes, these basal, air-breathing actinopterygians would be more suitable candidates for a comparative genomic research program aiming to trace evolutionary changes relevant to the water-to-land transition. Furthermore, it is not unlikely that air breathing and terrestriality may have taken place on more occasions during evolution, as indicated by the large spiracular openings on top of the skull and advanced internal spiracular architecture of †Gogonasus, a fish-like tetrapodomorph from the Late Devonian of Australia (Long et al, 2006;Clement & Long, 2010), and by the digit-like radials of †Sauripterus, a rhizodontid from the Late Devonian of Pennsylvania (Daeschler & Shubin, 1997).…”

“…Although not attainable by direct observation, information on the ecology, habitat, locomotion, respiration, and feeding habits of extinct sarcopterygian fishes may be inferred from an array of anatomical data including body form, axial and appendicular skeletons (form and position of fins), mouth position, size, dentition, jaw suspension, position of eyes, opercular arrangement, gill arches, and hypobranchial apparatus (e.g. Thomson, 1969;Clement & Long, 2010). In other words, our understanding of this specific evolutionary transition benefits from knowledge of living sarcopterygians but mostly relies on the detailed morphological study of numerous 'intermediate' fossils.…”