Extreme variation in the atrial septation of caecilians (Amphibia: Gymnophiona)

Abstract

Caecilians (order Gymnophiona) are elongate, limbless, snake-like amphibians that are the sister-group (closest relatives) of all other recent amphibians (frogs and salamanders). Little is known of their cardiovascular anatomy and physiology, but one nearly century old study suggests that Hypogeophis (family Indotyphlidae), commonly relied upon as a representative caecilian species, has atrial septation in the frontal plane and more than one septum. In contrast, in other vertebrates there generally is one atrial septum in the sagittal plane. We studied the adult heart of Idiocranium (also Indotyphlidae) using immunohistochemistry and confirm that the interatrial septum is close to the frontal plane. Additionally, a parallel right atrial septum divides three-fourths of the right atrial cavity of this species. Idiocranium embryos in the Hill collection reveal that atrial septation initiates in the sagittal plane as in other tetrapods. Late developmental stages, however, see a left-ward shift of visceral organs and a concordant rotation of the atria that reorients the atrial septa towards the frontal plane. The gross anatomies of species from six other caecilian families reveal that (i) the right atrial septum developed early in caecilian evolution (only absent in Rhinatrematidae) and that (ii) rotation of the atria evolved later and its degree varies between families. In most vertebrates a prominent atrial trabeculation associates with the sinuatrial valve, the so-called septum spurium, and the right atrial septum seems homologous to this trabeculation but much more developed. The right atrial septum does not appear to be a consequence of body elongation because it is absent in some caecilians and in snakes. The interatrial septum of caecilians shares multiple characters with the atrial septum of lungfishes, salamanders and the embryonic septum primum of amniotes. In conclusion, atrial septation in caecilians is based on evolutionarily conserved structures but possibly exhibits greater variation than in any other vertebrate order.

Convergent evolutionary reduction of atrial septation in lungless salamanders

“…Given the presence of AS1 and AS2 in cryptobranchid, amphiumid, ambystomatid and salamandrid salamanders (present study; Davies & Francis, ; Johansen, ; Putnam & Parkerson, ), combined with published data on septation in frogs and caecilians (Noble, ; de Bakker et al . ), we infer the basal condition for salamanders to be fully septate. Hence, the morphology of lungless salamanders represents an evolutionary loss of a prominent portion of the atrial septum, AS2 (Fig.…”

“…A number of caecilians with reduced reliance on pulmonary respiration also show partial reduction or fenestration of the atrial septum (Wilkinson & Nussbaum, ; de Bakker et al . ). We did not observe AS fenestration in lunged or lungless specimens.…”

“…; de Bakker et al . ). Our results on AS growth are consistent with these findings (Figs S1 and S2), but we did not examine the earliest stages of A. mexicanum to determine the precise origin of the AS.…”

“…; de Bakker et al . ). As in mammals, the amphibian atrial septum emerges from the dorsal wall of the atrium and grows posteroventrally towards the atrioventricular aperture (Mohun et al .…”

Development of the atrial septum in relation to postnatal anatomy and interatrial communications

“…(1) mesenchymal cap, (2) atrioventricular cushions, (3, 4) dorsal mesocardium, vestibular spine, (5) primary myocardial septum, (6) primary foramen, (7) secondary perforations, (8) closure of the primary foramen, (9) coalescence of the secondary perforations to form the secondary foramen, (10, 11) superior fold of the atrial roof, (12) muscularised mesenchyme of the vestibular spine, (13) muscularised mesenchyme of the mesenchymal cap, (14) oval fossa (based on de Bakker et al ,23 Rowlatt,24 Robertson,25 Icardo et al ,26 Jensen et al ,27 Icardo et al 28…”