The anatomical components of the cardiac outflow tract of chondrichthyans and actinopterygians

Abstract

The outflow tract of the fish heart is the segment interposed between the ventricle and the ventral aorta. It holds the valves that prevent blood backflow from the gill vasculature to the ventricle. The anatomical composition, histological structure and evolutionary changes in the fish cardiac outflow tract have been under discussion for nearly two centuries and are still subject to debate. This paper offers a brief historical review of the main conceptions about the cardiac outflow tract components of chondrichthyans (cartilaginous fish) and actinopterygians (ray-finned fish) which have been put forward since the beginning of the nineteenth century up to the current day. We focus on the evolutionary origin of the outflow tract components and the changes to which they have been subject in the major extant groups of chondrichthyans and actinopterygians. In addition, an attempt is made to infer the primitive anatomical design of the heart of the gnathostomes (jawed vertebrates). Finally, several areas of further investigation are suggested. Recent work on fish heart morphology has shown that the cardiac outflow tract of chondrichthyans does not consist exclusively of the myocardial conus arteriosus as classically thought. A conus arteriosus and a bulbus arteriosus, devoid of myocardium and mainly composed of elastin and smooth muscle, are usually present in cartilaginous and ray-finned fish. This is consistent with the suggestion that both components coexisted from the onset of the gnathostome radiation. There is evidence that the conus arteriosus appeared in the agnathans. By contrast, the evolutionary origin of the bulbus is still unclear. It is almost certain that in all fish, both the conus and bulbus develop from the embryonic second heart field. We suggest herein that the primitive anatomical heart of the jawed vertebrates consisted of a sinus venosus containing the pacemaker tissue, an atrium possessing trabeculated myocardium, an atrioventricular region with compact myocardium which supported the atrioventricular valves, a ventricle composed of mixed myocardium, and an outflow tract consisting of a conus arteriosus, with compact myocardium in its wall and valves at its luminal side, and a non-myocardial bulbus arteriosus that connected the conus with the ventral aorta. Chondrichthyans have retained this basic anatomical design of the heart. In actinopterygians, the heart has been subject to notable changes during evolution. Among them, the following two should be highlighted: (i) a decrease in size of the conus in combination with a remarkable development of the bulbus, especially in teleosts; and (ii) loss of the myocardial compact layer of the ventricle in many teleost species.

The valves of the cardiac outflow tract of the starry ray, Raja asterias (Chondrichthyes; Rajiformes): Anatomical, histological and evolutionary aspects

“…Early work was principally concerned with the number, shape, size and spatial arrangement of the valves (reviewed in Sans‐Coma et al, ). Moreover, the function of the conus arteriosus and its valves has focused the attention of several authors (reviewed in Satchell & Jones, , and Lorenzale et al, ). Nonetheless and despite the importance of the conal valves in preventing blood backflow into the ventricle, little attention has been paid to their histomorphology.…”

“…At that time, the bulbus arteriosus of chondrichthyans had not yet been identified. Currently, it is known that the intrapericardial, non‐myocardial segment interposed between the conus and the ventral aorta in cartilaginous fish is not a backward extension of the aorta, but a cardiac component in its own; it is the bulbus arteriosus (Durán et al, ; Lorenzale et al, ; Rodríguez et al, ). Thus, the relationships between the conus and the ventral aorta at the level of the anterior row of valves described by Sans‐Coma et al () were inaccurate.…”

“…The cardiac outflow tract of chondrichthyans, namely the intrapericardial portion of the heart interposed between the ventricle and the ventral aorta, consists of the conus arteriosus and the bulbus arteriosus (Durán et al, ; Lorenzale et al, ). The conus arteriosus is a contractile segment with myocardium in its walls and valves, the conal valves, at its luminal side.…”

Development and evolution of the metazoan heart

“…The delineation of the OFT and its components has received much attention and discussion in comparative cardiac embryology . This has rendered sometimes conflicting hypotheses about compartmental properties and homologies in comparative vertebrate studies and the description of congenital malformations in the human population, with consequences for more recent aspects of gene regulatory networks and protein interactions.…”

“…The delineation of the OFT and its components has received much attention and discussion in comparative cardiac embryology. 83,[119][120][121][122][123] This has rendered sometimes conflicting hypotheses about compartmental properties and homologies in comparative vertebrate studies and the description of congenital malformations in the human population, with consequences for more recent aspects of gene regulatory networks and protein interactions. It seems evident that the OFT in fish, for example, consists of a proximal myocardial conus arteriosus as well as the more distal bulbus arteriosus rich in smooth muscle cells as well as elastin.…”