Structure and vascularization of the ventricular myocardium in Holocephali: their evolutionary significance

Abstract

It was generally assumed that the ventricle of the primitive vertebrate heart was composed of trabeculated, or spongy, myocardium, supplied by oxygen-poor luminal blood. In addition, it was presumed that the mixed ventricular myocardium, consisting of a compacta and a spongiosa, and its supply through coronary arteries appeared several times throughout fish evolution. Recent work has suggested, however, that a fully vascularized, mixed myocardium may be the primitive condition in gnathostomes. The present study of the heart ventricles of four holocephalan species aimed to clarify this controversy. Our observations showed that the ventricular myocardium of Chimaera monstrosa and Harriotta raleighana consists of a very thin compacta overlying a widespread spongiosa. The ventricle of Hydrolagus affinis is composed exclusively of trabeculated myocardium. In these three species there is a well-developed coronary artery system. The main coronary artery trunks run along the outflow tract, giving off subepicardial ventricular arteries. The trabeculae of the spongiosa are irrigated by branches of the subepicardial arteries and by penetrating arterial vessels arising directly from the main coronary trunks at the level of the conoventricular junction. The ventricle of Rhinochimaera atlantica has only spongy myocardium supplied by luminal blood. Small coronary arterial vessels are present in the subepicardium, but they do not enter the myocardial trabeculae. The present findings show for the first time that in a wild living vertebrate species, specifically H. affinis, an extensive coronary artery system supplying the whole cardiac ventricle exists in the absence of a well-developed compact ventricular myocardium. This is consistent with the notion derived from experimental work that myocardial cell proliferation and coronary vascular growth rely on distinct developmental programs. Our observations, together with data in the literature on elasmobranchs, support the view that the mixed ventricular myocardium is primitive for chondrichthyans. The reduction or even lack of compacta in holocephali has to be regarded as a derived anatomical trait. Our findings also fit in with the view that the mixed myocardium was the primitive condition in gnathostomes, and that the absence of compact ventricular myocardium in different actinopterygian groups is the result of a repeated loss of such type of cardiac muscle during fish evolution.

Heart Anatomy of Rhincodon typus: Three‐Dimensional X‐Ray Computed Tomography of Plastinated Specimens

“…Our study revealed that despite its large body size, the whale shark has a type III ventricle with extremely thin compacta, accounting only for ~3% of the ventricular wall thickness. This percentage is similar to that in Holocephali (Durán et al, ). We consider that this finding corresponds to the nature of whale sharks as placid, slow swimmers.…”

Heart structure in the Amazonian teleost Arapaima gigas (Osteoglossiformes, Arapaimidae)

“…In this classification, the authors used the relationship between the myoarchitecture and the distribution of coronary vessels to group the ventricle into four main types. However, as demonstrated for Hydrolagus affinis, some species may have a morphology that does not fit any of the types described (Dur an et al 2015). Of the four types, type II ventricles are characterized by the presence of a mixed myocardium associated with coronary vessels that are restricted to the compact layer.…”

Morphological arrangement of the coronary vasculature in a shark (Squalus sucklei) and a teleost (Oncorhynchus mykiss)

“…We are confident of the methodological approach used for this work because our measurements of vascular density in the compact myocardium of rainbow trout are comparable with previous measurements of the capillary density in rainbow trout (Egginton and Cordiner, ; Table ). Therefore, the method seems appropriate to examine the vascular architecture of the highly branched vascularized trabeculae that predominate the myocardium of the dogfish and potentially a vast number other vertebrates species, namely chondrichthyan and reptile species (Tota, ; Kohmoto et al, ; Durán et al, ). The spongy myocardium of cyclostomes and amphibians as well as some fishes are exempt because they lack penetrating coronary vessels in the myocardium.…”

“…Chondrichthyans are of special interest because they are living representatives of an early clade of vertebrates to have developed coronary arteries. Like most teleosts, they have a predominately spongy ventricular myocardium in the species studied to date (Santer and Greer Walker, ; Emery et al, ; Durán et al, ). Nevertheless, the chondrichthyan spongy myocardium contains a coronary arterial network, similar to the compact myocardium and unlike the spongy myocardium of most teleost fishes and all fetal mammals during the first trimester (Santer and Greer Walker, ; Helle et al, ; Tota, ; Tomanek, ).…”

“…Nevertheless, the chondrichthyan spongy myocardium contains a coronary arterial network, similar to the compact myocardium and unlike the spongy myocardium of most teleost fishes and all fetal mammals during the first trimester (Santer and Greer Walker, ; Helle et al, ; Tota, ; Tomanek, ). This is true even in a chondrichthyan species that are though to have secondarily lost their compact myocardium (Durán et al, ). Thus, while the compact myocardium of the ventricle and conus arteriosus of the chondrichthyan heart only has a coronary oxygen supply, the spongy myocardium of the atrium and ventricle has two potential oxygen supply routes, the coronary and luminal supplies.…”