Differentiation of the cardiac outflow tract components in alevins of the sturgeon Acipenser naccarii (Osteichthyes, Acipenseriformes): Implications for heart evolution

Abstract

Previous work showed that in the adult sturgeon an intrapericardial, nonmyocardial segment is interposed between the conus arteriosus of the heart and the ventral aorta. The present report illustrates the ontogeny of this intermediate segment in Acipenser naccarii. The sample studied consisted of 178 alevins between 1 and 24 days posthatching. They were examined using light and electron microscopy. Our observations indicate that the entire cardiac outflow tract displays a myocardial character during early development. Between the fourth and sixth days posthatching, the distal portion of the cardiac outflow tract undergoes a phenotypical transition, from a myocardial to a smooth muscle-like phenotype. The length of this region with regard to the whole outflow tract increases only moderately during subsequent developmental stages, becoming more and more cellularized. The cells soon organize into a pattern that resembles that of the arterial wall. Elastin appears at this site by the seventh day posthatching. Therefore, two distinct components, proximal and distal, can be recognized from the fourth day posthatching in the cardiac outflow tract of A. naccarii. The proximal component is the conus arteriosus, characterized by its myocardial nature and the presence of endocardial cushions. The distal component transforms into the intrapericardial, nonmyocardial segment mentioned above, which is unequivocally of cardiac origin. We propose to designate this segment the "bulbus arteriosus" because it is morphogenetically equivalent to the bulbus arteriosus of teleosts. The present findings, together with data from the literature, point to the possibility that cells from the cardiac neural crest are involved in the phenotypical transition that takes place at the distal portion of the cardiac outflow tract, resulting in the appearance of the bulbus arteriosus. Moreover, they suggest that the cardiac outflow tract came to be formed by a bulbus arteriosus and a conus arteriosus from an early period of the vertebrate evolutionary story. Finally, we hypothesize that the embryonic truncus of birds and mammals is homologous to the bulbus arteriosus of fish.

The Development of the Epicardium in the Sturgeon Acipenser naccarii

“…At this point, it should be noted that, at stages 4-5 dph, the outflow tract is completed by the formation of a new segment, the intermediate (conus-aorta transition) segment (Icardo et al, 2002) or bulbus arteriosus (Guerrero et al, 2004), which is added to the cranial end of the heart, between the conus arteriosus and the ventral aorta. We could not find evidence for the progression of the epicardium into this segment (Fig.…”

“…EPICARDIAL DEVELOPMENT IN THE STURGEON dph (see Icardo et al, 2004). Another feature of developmental significance occurring at these stages was the formation of the septum transversum.…”

“…In birds and mammals, the entire heart is invested by epicardium at the time of valve development, before the completion of the heart septa. In the sturgeon, the conus epicardium also develops at the time of conus valve formation (see Icardo et al, 2004). However, since septa do not form in the fish heart, temporal and spatial correlations are difficult to establish not only between fish, birds, and mammals but also particularly between fish species.…”

“…The sturgeons exhibit primitive features that relate them to both the chondrichthyans and the amphibians (see Dettlaff et al, 1993). Previous studies (Guerrero et al, 2004;Icardo et al, 2004Icardo et al, , 2009) have revealed that the sturgeons share cardiac developmental mechanisms with birds and mammals. The present work indicates that many epicardial developmental mechanisms are also similar in sturgeons and in phylogenetically apical groups of vertebrates.…”

“…The present work indicates that many epicardial developmental mechanisms are also similar in sturgeons and in phylogenetically apical groups of vertebrates. The characteristic large size and slow rate of development of the Acipenser naccarii heart (Icardo et al, 2004(Icardo et al, , 2009) makes it a suitable model to study many of the developmental sequences involved in heart and epicardium formation.…”