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When features vanish in the haze…

Hair and external ears are features that define mammals. However, many mammal species are hairless (like whales) and have no external ears (like seals and, again, whales). In the same way, many acanthomorph species do not have hollow and non segmented spines in front of the anal and dorsal fins (represented by red arrows on the following image of the sea bass (Dicentrarchus labrax, Dicentrarchidae)), no matter how useful these attributes are to identify the animals of this group:

Dicentrarchus labrax, Dicentrarchidae
From Chanet et al. (2009).

Flatfishes, sand eels, puffers and seahorses, among many others, lack these spines. The study of the interrelationships of acanthomorphs on the basis of other characters and types of data (molecular for instance) leads to the conclusion that these spines have been lost several times independently during the evolution of the group.

The same occurred to the gasbladder (= swimbladder)*, an organ present or absent depending on the species, and it is an occasion to link sciences and History.

*: the term gasbladder is here prefered to swimbladder, as the first one describes what it is, i.e. the structure of the organ (an internal cavity full with gas), and the second one describes what it does, i.e. one of its functions.

In 1859, in Origin of species, Charles Darwin indicated in his usual style:

… hence there is no reason to doubt that the swimbladder has actually converted into lungs, or an organ exclusively for respiration.

So what do we think about it now? In 2009, our understanding of biological evolution is based on a tree of related species and no more on an linear narrative where recent species « give birth » to some other recent species. We know that structures present in extant “fishes” are not necessarily the outlines of the structures of tetrapods. In other words, do lungs come from gasbladders or do gasbladders come from lungs? Which one occurred first?

If we draw a linear representation of evolution, we would have :
fish (S) → amphibians (L) →  reptiles (L) → mammals (L)
and then, we might think: gasbladder (S) → lung (L).

But … evolution is not linear! It has a branching structure. Moreover, as Charles Devillers (1914-1999) liked to stress during his comparative anatomy lessons: « outside a kitchen, the word "fish" means nothing … ».

So in fact we may have two solutions:
1. lung → gasbladder
2. gasbladder → lung

Are there no other alternatives ?

Probably not, for two reasons. First, there is no organism with both a lung and a gasbladder. Second, lung and gasbladder have the same position, the same structure, the same relations with other organs (digestive track, blood vessels …): they are homologous organs. But we have to keep in mind that comparing the lung of a mammal or a bird with the gasbladder of a teleost is nonsense. Amniote lungs are too highly derived; the comparison is more meaningful using the lung of a dipnoan.

In Teleosteans and other bony fishes, like sturgeons, the gasbladder is an internal cavity full of gas (next image), which is dorsal to the digestive tract. It is sometimes connected to it via a pneumatic duct (however, many teleost fishes have their gasbladder free from the digestive tract).

Radiography of a pick-perch (Sander lucioperca)
Radiograph of a Pike-perch, Sander lucioperca, Percidae,
modified after Chanet et al. (2009). The star (*) indicates the gasbladder.

Its main role is the control of buoyancy, but depending on the species, this air bladder sometimes possesses expansions, and plays a role in respiration, as well as the reception and production of sounds (next image) :

dissection of a gurnard (Aspitrigla cuculus)
Dissection of a gurnard (Aspitrigla cuculus, Triglidae) showing the gasbladdder with its two lateral expansions.
They are involved in the production of sounds by the gurnard.  (image: R. Daoudi (ENVN)).

Just like spines in many acanthomorphs or hair in many mammals, the gasbladder has regressed independently in several teleostean groups : Atlantic mackerel (Scombridae), several antarctic fishes (Liparidae, notothenioids), some sand eels (Ammodytidae), some tunas (Thunnidae), some blennies (Blennidae), adult sole (Soleidae) and all adult flatfishes (Pleuronectiformes) have no gasbladder … For a more exhaustive list, see McCune et Carlson (2004)).

In summary, this bladder is absent in benthic forms (=living on the see-bottom, like flatfishes and some blennies), in forms swimming at high speed (in such conditions this full of gas bladder is energetically disadvantageous, as in Atlantic mackerel and several species of tunas) and in forms with a benthic common ancestor (as notothenioids).
Basal actinoperygians (reedfishes, Cladistia) do not possess a gasbladder but two lunges and gills as well... What about dipnoans and cœlacanths? They have gills, no gasbladder, and one or two lungs (one in the cœlacanth, one in Neoceratodus, two in other dipnoans (Protopterus and Lepidosiren)). Such a distribution of character states might be viewed as puzzling, but there is a simple explanation.

In the common ancestor of actinopterygians and dipnoans, coelacanths and tetrapods, there was an internal cavity full of gas. Was its role a respiratory one? It might have been, but we cannot assess it anymore. Moreover, organs do not have a unique function. This organ existed then as a lung in reedfishes and dipnoans, it regressed in a fatty organ in coelacanths (its pulmonary structure can be still identified). In tetrapods, this organ specialized with internal ramifications and a different anatomic position. In this group, lungs are latero-ventral with regard to the digestive tract, while they are in a dorsal position in the other groups. Nevertheless, in all of them, the lung or lungs, is/are connected ventrally to the digestive tract.

It we take in consideration the whole data and put the presence of a gasbladder or lung on a tree of osteichthyans (next image), it appears more parsimonious to consider that the lung came first, and that the gasbladder came from lung.

interrelationships tree of osteichthyans

This new structure appeared before the common ancestor of teleosteans and chondrosteans. Some internal elements of a sole specimen of placoderms (a group of aquatic Palaeozoic vertebrates) have been considered to be lungs by Denison (1941). But the identification remains truly uncertain; those structures could also be interpreted as oesophagus or pharyngal expansions with an alimentary/respiratory function (Janvier et al, 2007). In 2010, Daniel Goujet totally rejects this presence of "lungs" on these fossils on the basis of taphonomic, anatomic and phylogenetic data.
One may consider that a S→L scenario is possible with multiple and independent transformations in reedfishs and sarcopterygians (cœlacanths+dipnoans+tetrapods). But such a scenario implies that the very same event (transformation into a lung) occurred twice in two different lineages. It is more complex and less probable than the L→ S scenario.

 “Darwin’s blunder”(Pauly, 2004 :200), the S→L scenario, can be easily understood in the context of an erroneous definition of « fish », with fish= teleosteans, as they represent the main diversity of extant vertebrates. Darwin made this mistake... But did he know about the lung of dipnoans and reedfishes ? These species are mentioned in chapters IV and XI of Origin of species (1872  6th and last edition), but their anatomy is not know at the time. Dipnoans were definitively identified as « fishes » by Günther in 1871.

In science, do we have to consider great authors as mentors or gurus? No, of course and after celebrating the 200th anniversary of the birth of Charles Darwin we have to continue to celebrate his work and ideas without neglecting his blunders. We may criticize them and laugh about them. But they enlighten us about past ways of thinking and reveal both the history of sciences and discoveries.

Then, between lung and gasbladder, which one was the first ?

« Le Poumon. Le poumon, vous dis-je !! » (The lung, the lung, I tell you !!)

Molière, Le Malade imaginaire (acte III, scène 10).


So let’s take care of not judging a book by the cover, nor to see a group through a unique feature. The living world is diverse; regressing and vanishing are quite common for characters.


Some further readings

  • Chanet B., C. Guintard, C. Picard, P. Bugnon, F. Touzalin et E. Betti (2009). Atlas anatomique d’ichtyologie, CD-ROM diffusé par la Société Française d’ichtyologie.
  • Chanet B. (2009). Le Poumon, Le poumon, vous dis-je !! SFI-Infos, 49:9-11.
  • Desoutter-Meniger M. et B. Chanet (2009). The swim bladder of the adults soleids [Acanthomorpha : Pleuronectiformes, Soleidae]: fact or fiction. Cahiers d'Anatomie Comparée, 2:40-49.
  • Darwin C.R. (1859). On the origin of species by means of natural selection or the preservation of favored races in the struggle for life. John Murray (ed.), London, 490 p.
  • Darwin C.R. (1872). The origin of species by means of natural selection or the preservation of favored races in the struggle for life. (6ème édition), John Murray (ed.), London, 433 p.
  • Denison R. H. (1941). The soft anatomy of Bothriolepis. Journal of Paleontology, 15:553–561.
  • Gould S.J. (1996). Des paroles en l'air. In: Comme les huit doigts de la main, Points Sciences, Seuil, S137:138-153.
  • Janvier P. (1996). Early Vertebrates. Oxford Science publications, New York, 393 pp.
  • Janvier P., Desbiens S. et J.A. Willett (2007). New evidence for the controversial “lungs” of the late Devonian antiarch Bothriolepis canadensis (Whiteaves, 1880) (Placodermi: Anatiarcha), Journal of Vertebrate Paleontology, 27(3):709–710.
  • McCune, A.R. et R.L. Carlson (2004). Twenty ways to lose your bladder: common natural mutants in zebrafish and widespread convergence of swim bladder loss among teleost fishes, Evolution & Development, 6:4, 246–259.
  • Pauly, D. (2004). Darwin’s fishes. An encyclopedia of ichthyology, ecology and evolution. Cambridge, Cambridge University Press, 340 pp.