Ontogeny and Phylogeny

Ontogeny and phylogeny are more strikingly related in the circulatory system compared to any other organ system (1).  Embryonic hearts, arteries and veins of higher vertebrates closely resemble the corresponding organs of remote ancestors. For example, the pattern of circulation changes in embryonic development in much the same way as it must have changed in evolution. These marked similarities are useful in systematics. This is particularly true of the heart and major circuits at levels of the class and subclass, and patterns of arteries, in the limbs and basicranial area at levels of  the order and family. While there are obvious fundamental differences between fish and humans, there is a high level of genetic conservation, and, although morphological differences might suggest distinct developmental processes, it is now clear that evolution has utilized the same basic building blocks to create even the most diverse structures and animals (6).

The heart as an organ originated in the distant past. It is thought that the first organ that resembled a heart is have originated over 500 million years ago in an ancestral bilaterian. It is likely that it was a simple tubular vessel-like organs of tunicates and amphioxus, which contain a myoepithelial layer of cells and lacked chambers or valves.  The diversification of muscle cells led to the origin of skeletal, cardiac, and smooth muscle cells, and additional specialization of cardiac muscle cells ultimately yielded atrial and ventricular myocytes, as well as the cells of the mammalian cardiac conduction system (9). These cells are some of the the first to form and function during embryogenesis (7).

The Developing "Heart" in Amphioxus

Fig. 6. (A) Living 3-day larva with subenteric vessel (arrow) beginning to form ventral to hindgut; scale line, 50 μm. (B) Section through level of arrowhead in (A); the arrow indicates the heart (subenteric vessel); scale line 25 μm. Image Credit: ScienceDirect

The heart is thought to have evolved by the addition of new structures and functions to a primitive pump and is though to be controlled by conserving heart related genes, duplicating cardiac regulatory genes, as well as co-opting additional gene networks.Today, with advances in molecular biology, signaling molecules and transcription factors important for cardiogenesis have been identified. The cellular and molecular events that control early cardiac development are remarkably conserved across vertebrate and even invertebrate embryos. Apparently, an amphioxus-like heart (Fig. 6) was the foundation upon which the vertebrate heart evolved by progressive modular innovations at the genetic and morphological levels of organization (12). These evolutionary events probably allowed for the addition of new accessory structures, such as chambers, valves, and a conduction system, to a primitive vessel-like heart analogous to that of invertebrates and vertebrate embryos.

The early muscle cells resembled the epitheliomuscle cells of Cnideria and amphioxus, which is thought to be the closest living approximation of the invertebrate ancestor of vertebrates (8). Amphioxus has no heart, instead it has pulsating cells that form vessels in the position where heart evolved in vertebrate. These cells probably existed in a primitive gastric pocket where they participated in fluid movement during feeding. These vessels approximate the embryonic primordium of the vertebrate heart and are apparently homologous.Thus, the structure of the adult ancestral vertebrate heart can be reflective of the structure of the embryonic heart of the descendants.

Embryonic Origins of the Heart 

Figure 7. Primary heart-forming fields (indicated in red) during gastrulation, establishment of primary heart fields and fusion of the primitive heart tube in avian embryos. A: Heart progenitors are located in primitive streak at 12-13 hours of development. B, C: Paired heart primordia are present in the anterior lateral plate mesoderm at 19-22 hours of development (B), and 26-29 hours of development (C). D: The heart primordia fuse in anterior-posterior progression to form the beating heart tube by 33-38 hours of development. Image Credit: Wiley Online Library

Muscle cells are derived from mesoderm (the middle of the three germ layers of the embryo - the ectoderm, the endoderm, and the mesoderm), which is thought to have developed from the gastrodermis of a diploblastic ancestor. Mesodermal tissues which contains cells that will give rise to the heart first become evident when embryo is undergoing a process known as gastrulation, which forms a primitive streak - a structure that forms during the early stages of embryonic development. Through this streak, cells migrate from the upper layer to form the three germ layers of the embryo. The presence of the primitive streak will establish bilateral symmetry, determine the site of gastrulation and initiate germ layer formation. In the human, this occurs during the third week of development, while for the mouse, at a comparable stage of development, around seven days will have elapsed from fertilisation, and the embryo will be in the presomitic stage (13).These cells then migrate to an anterior lateral position where they condense to form bilateral heart primordia.

The true heart is defined as chambered pumping organ that is enclosed within a pericardial sac and possesses three tissue layers: endocardium, myocardium and epicardium (6). This definition implies that  adapting a 'homologous' concept of hearts, as opposed to the alternative 'homoplasic' concept.

At its simplest level, the vertebrate heart can be conceptualized as having two compartments: an inflow that receives blood from upstream and an outflow that delivers blood downstream. The atrioventricular valve(s) can be thought of as boundaries between these two compartments (17). Thus  increasing complexity of hearts, from agnathans through to mammals, can be explained by the simple modular repetition of inflow and outflow units. However, it could equally be argued that both morphological considerations and gene expression patterns allow further, more detailed, structural analysis of the heart, and, while all vertebrates have inflow and outflow ‘modules’, some of the complexities of land-based, obligate air-breathing vertebrate hearts are difficult to explain by simple modular repetition.

For example, the outflow tract of the most ancient extant jawed vertebrates, the elasmobranchs  (sharks, skates and rays), has an elongated, myocardial conus arteriosus that is invested with several rows of valves, with the number of rows depending on the species. This structure is proposed to have been modified throughout evolution, with its equivalent being considerably shortened in the ancient teleosts, incorporated into the ventricle in the modern teleosts, septated in amphibians and reptiles, and compacted, remodelled and septated in birds and mammals.

In fact, it has been further proposed that the elasmobranch conus may be homologous to the region of the mammalian embryonic outflow that ultimately gives rise to the right ventricle (18), (13). This variation, along with the augmentation at the distal outflow tract of a smooth muscle-walled structure known as the bulbus arteriosus in teleosts, which presumably performs similar functions to the  myocardial elasmobranch conus arteriosus, that of protecting the gill vasculature from large variations of pressure and prolonging blood flow through the ventral aorta during ventricular systole (Santer, 1985), argues more for modification of an existing module, or perhaps the interposition of a novel module, rather than for modular repetition.