Genesis of air breathing in basal tetrapods

The genesis of limbs and toes 
from lobes and fins gets most of the publicity in transitional fish-tetrapods.

Today we look at the less popular transition
from water breathing with gills to air breathing with a nose and lungs.

Like most fish,
Onychodus (Fig. 1) drew in oxygenated water by opening its mouth. At this moment, the gill covers are closed to prevent backdraft. Closing the mouth and raising the basihyal (medial bone between the mandibles) until it presses against the solid palate reduces the mouth volume, pushing that mouthful of  water posteriorly past the gills where oxygen and carbon dioxide are transferred. At this time the gill covers are open to permit that water to exit, completing the cycle. The dual nares have nothing to do with respiration at this point, only olfaction, with water passively entering the anterior opening and passively exiting the posterior opening (Fig. 1). The air bladder arising from the gut tube anterior to the stomach is not involved in respiration at this stage.

Among lobefin fish,
coelacanths, like Latimeria, have this primitive system.

Figure 1. Onychodus is typical of most fish having dual external nares strictly for olfactory sensing. Gill covers are part of the respiratory apparatus.

Figure 1. Onychodus is typical of most fish having dual external nares strictly for olfactory sensing. Gill covers are part of the respiratory apparatus.

Among lobefin lungfish (Late Silurian to present),
like Kenichthys (Fig. 2), Youngolepis, Polypterus (the extant bichir) and Howidipterus, oxygen-poor water, supplemented by gulps of dry air, once again enters the mouth and is passed back over the gills and out the gill covers. Both the incurrent and excurrent nares migrate ventrally. (Not sure why.) Worthy of a Nature article, the excurrent opening is parked on the jaw margin between the premaxilla and maxilla in Kenichthys, so half the excurrent exited outside the mouth, while the other half exited inside the mouth (see ventral view in Fig. 2), all passively. (Not sure why this migration took place either, except that with the lips sealed inhalation and exhalation can still take place… slowly… in and out of both openings, perhaps to retain mouth moisture during aestivation (hibernation in dry mud.) Note the pinprick size of each opening.

Figure 1. Kenichthys Images from Zhu and Ahlberg 2004, colors added. The authors made a convincing argument that Kenichthys represented a transitional taxon between Youngolepis and Eusthenopteron. Note the lack of vomer fangs and a distinctly different set of skull sutures in Kenichthys, which does not nest with Eusthenopteron in the LRT.

Figure 2. Kenichthys Images from Zhu and Ahlberg 2004, colors added. The authors made a convincing argument that Kenichthys represented a transitional taxon between Youngolepis and Eusthenopteron. Note the lack of vomer fangs and a distinctly different set of skull sutures in Kenichthys, which does not nest with Eusthenopteron in the LRT.

Among basal lobefin crossopterygians (Early to Late Devonian),
like Gogonasus, Eusthenopteron, and elongate, flattened Cabonnichthys, Elpistostege, Tiktaalik and Panderichthys the tiny excurrent nasal opening just barely enters the rim of the mouth cavity and is thereafter considered a choana. The tiny external incurrent opening is thereafter considered a naris. Based on their tiny sizes, both remain useless for respiration. Large gill covers and a solid palate are retained for traditional water respiration supplemented by dry air gulping as needed.

Figure 4. Panderichthys palates. Note the lateral line below the naris is not continuous, contra Lombard and Bolt.

Figure 3. Panderichthys palates. Note the lateral line below the naris is not continuous, contra Lombard and Bolt.

When the gill covers disappear in fossil taxa
that signals the genesis of air-breathing from mouth to paired air bladders (now called ‘lungs’) rather than past the disappearing gills. According to the LRT, this occurred twice (if we don’t count the ontogenetic transformation of juvenile tadpoles (with gills) to adult frogs (with lungs) and other similar basal tetrapods).

In clade one: primitive Koilops retained and operculum (gill cover). Derived, but lobe-finned Tiktaalik and Spathicephalus did not have an operculum.

In clade two: weak limbed, four-fingered Trypanognathus (Fig. 4), Deltaherpeton, Collosteus, PholidogasterGreererpeton and Ossinodus, all lacked an operculum.

Figure 2. Animation of air-breathing in basal tetrapods with weak lungs inflated by contraction and expansion of the throat sac, rather than gill irrigation powered by the reduced here buccal bones.

Figure 4. Animation of air-breathing (tidal ventilation) in basal tetrapods with weak lungs inflated by contraction and expansion of the throat sac, rather than gill irrigation powered by the reduced ceratobranchials, still present at right. Air-tight nose flaps had to be present in order for this system to work. 

Clade two exceptions: Robust-limbed, eight-fingered Acanthostega (Fig. 5) and Ichthyostega retained tiny gill covers (operculum) as adults. And they had primitive tiny nares and choana, still not suitable for air-breathing. These convergent exceptions are here considered reversals due to a suite of derived traits nesting these two famous taxa apart from more primitive tetrapods and apart from each other in the LRT.

Figure 2. the MGUH VP 8160 specimen attributed to Acanthostega. Note the many similarities to Ymeria.

Figure 5. the MGUH VP 8160 specimen attributed to Acanthostega. Note the many similarities to Ymeria. Note the spiracle openings surrounded by the supratemporals. This provides an accessory respiration opening, convergent with bottom-dwelling skates and rays from the shark clade.

The signal that air-breathing respiration through the nostrils had begun
(Fig. 4) is when the nares and choana of fossil taxa enlarge to handle the larger volume of tidal ventilation coming through them. The nares also migrate higher on the skull so that they are at least partly visible in dorsal view. The internal nares are fully inside the mouth, which must be able to seal shut to divert air through the nares, rather than leaking past the lips. Gill covers are absent. Air-tight nose flaps had to be present in order for this system to work. The pterygoids reduce and retreat posteriorly (Fig. 4), creating large, pliable openings in the formerly solid palate (Fig. 3), expanding the potential volume of the mouth.

According to the LRT,
(subset Fig. 5) the enlargement and migration of the nares and choana occurred several times because several clades of derived basal tetrapods retained tiny lateral nares and choana despite having fully developed limbs.

Figure 3. Subset of the LRT focusing on basal tetrapods and their narial openings.

Figure 5. Subset of the LRT focusing on basal tetrapods and their narial openings.

Dorsal ribs
Basal tetrapods depend on an expanding and contracting the gular sac for tidal ventilation of the lungs, mimicking their lobe-finned ancestors. These same basal tetrapods (Fig. 6) were all low and wide with relatively straight, laterally-oriented ribs incapable of expanding and contracting the torso and lungs. Not until dorsal ribs elongated and started curling around the inside of an increasingly round (in cross-section) torso where they able to expand and contract the volume of the torso and the lungs inside. In that way mobile ribs gradually replaced a mobile throat sac for tidal ventilation.

Figure 6. Dorsal and ventral views of Panderichthys and several basal tetrapods demonstrating the low, flat skulls and bodies with small limbs and relatively straight ribs.

Figure 6. Dorsal and ventral views of Panderichthys and several basal tetrapods demonstrating the low, flat skulls and bodies with small limbs and relatively straight ribs, all to scale. Note the brevity of the tail in thee taxa.

The irony is
we know of Ichthyostega-grade tetrapods walking on land in the Middle Devonian. By that I mean, we know of tetrapods with relatively large limbs and supernumerary digits capable of elevating the belly off the substrate. Phylogenetic analysis indicates the trackmaker was a mouth-breather with tiny lateral nares. This was a short-lived experiment (as far as we know at present) leaving only Late Devonian descendants, like Icthyostega, that disappeared by the Early Carboniferous.

The longer lasting clade,
the one that produced all the other tetrapods including reptilomorphs, living amphibians and microsaurs, all had a long, low, flat body and skull with smaller 4-fingered limbs not capable of elevating the belly off the substrate, like Greererpeton and Trimerorhachis (Fig. 6). Only later, and by convergence did descendants rise off their belly with stronger limbs, mimicking those pioneer Middle Devonian tetrapod trackmakers.


References
Schoch RR and Voigt S 2019. A dvinosaurian temnospondyl from the Carboniferous-Permian boundary of Germany sheds light on dvinosaurian phylogeny and distribution. Journal of Vertebrate Paleontology. DOI: 10.1080/02724634.2019.1577874.xxx

This blogpost comes not in response to a new academic paper, but to revisiting some of the taxa in the the large reptile tree (LRT, Figs. 5, 6) at this transition. Thanks to reader Dave M for the impulse to reexamine these taxa.

 

 

 

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