The metabolic activity of any tissue is limited by its blood supply; the more active any organ, the more blood it needs and the more extensive its vascularization.

The changes in metabolic activity associated with endothermy and the change from gill to lung respiration has led to changes in vertebrate circulatory systems.

In general, blood is pumped by heart to arteries -> arterioles -> capillaries.

Capillaries come together to form venioles -> veins -> major venous trunks

-> heart

Veins between two capillary networks are portal systems.

Closed circulatory system, but fluid constituents of blood leak out of capillaries and return to the heart by the second component of the circulatory system, the lymphatic system.

Considerable variation in blood vessels, as seen in shark

Due to developmental origin of blood vessels: many channels form, some enlarge to form major blood vessels, some of which atrophy and die.

A piece of a vein grafted into an artery transforms structurally to become an artery.

Nearly any vessel can be tied off gradually and system can enlarge alternate routes.

Blood can, and does, flow in either direction in several vessels.

Blood can be diverted towards or away from any part of the body, volume of circulating blood can be changed, rate of circulation can be changed 5-fold.

Despite this variability, the structure of the heart and major vessels tells us a lot about the evolutionary history of vertebrates and the evolutionary changes that have greatly modified vertebrate circulatory systems.

Circulatory system is the first organ system to become functional during development.

On each side of embryo, an aorta forms ventrally and swings dorsally.

The paired aortae in ventral position fuse along a short section and form a single vessel, the beginning of the heart.

The posterior part of the fusion forms the sinus venosus, receiving the major venous trunks flowing back to the heart.

Four sequential chambers of the heart exist, from posterior to anterior:

1. thin-walled sinus venosus

2. single atrium

3. thick walled single ventricle

4. conus arteriosus

The adult heart (fish or amniote) develops from this simple pattern.

The heart takes on its final adult form from a number of possible modifications:

differential growth of certain parts

fusion of adjacent regions

disappearance of partitions

formation of new partitions

In amniotes, the heart overgrows its pericardial space and doubles up on itself to form a loop that swings to the right side of the pericardial cavity.

This twisting results in the shape of the heart and the positioning of the atria and ventricles seen in adult amniotes.

The large sinus venosus receives blood from the common cardinal veins on the side of the body and the hepatic veins from the liver.

Single chambered atrium balloons out dorsally on each side of the muscular ventricle.

Blood flows into ventricle, which opens into the conus arteriosus where a series of valves prevent back flow of blood.

The regions of the heart form an S-shaped loop, to fit into pericardial cavity.

The heart of the fish contains completely deoxygenated blood and has a single circulatory system.

In lungfish, the heart is partially divided into a right and left atrium.

The sinus venosus opens into the right side of the atrium.

Vessels from the lung return oxygenated blood to the left atrium (pulmonary vein).

The ventricle and conus arteriosus are also partially divided, although there is some mixing of deoxygenated and oxygenated blood.

As blood goes through the conus arteriosus, a branch carries oxygenated blood from the left side of the ventricle to the anterior gills.

A second branch of the conus carries deoxygenated blood to posterior gills and the lungs from the right side of the ventricle.

This is the beginning of the double circulatory system.

The sinus venosus has shifted to the right and empties into right atrium, which is completely separated from left atrium by a thin interatrial septum.

From the right atrium, the blood goes into a single large muscular ventricle.

In the ventricle, muscular folds or trabeculae reduce the mixing of blood between the right and left sides of the ventricle.

Blood from the right side of the ventricle flows into the conus arteriosus, where a spiral valve through the middle of the conus separates the flow of blood into two channels.

The deoxygenated blood from the right side of the ventricle passes on one side of the spiral valve and flows through the pulmonary artery to lungs, skin or gills.

Pulmonary veins return oxygenated blood to the left atrium, to the left side of the ventricle and then on the other side of the spiral valve into the systemic arteries.

Left and right sides of the heart become more separated.

Atria are completely separate, ventricles are almost completely separated, except for a small gap that allows some blood to spill between chambers, resulting in some mixing of blood.

In crocodiles, the gap is closed, the ventricle is completely divided and there is complete separation.

The conus arteriosus is split into the pulmonary trunk and two aortic trunks.

The left aortic trunk emerges from the right ventricle and the right aortic trunk emerges from the left ventricle.

Pulmonary veins return oxygenated blood to the left atrium.

Blood from the pulmonary vein passes to the left ventricle and from there to the right aortic arch.

Heart has completely separated: 2 atria, 2 ventricles, 4 chambers, and adult bird has complete double circulation: low-pressure pulmonary circuit using the right side of the heart and a high-pressure systemic circuit using the left side of the heart.

The sinus venosus is completely incorporated into the wall of the right atrium.

Blood passes from the right atrium to the small right ventricle and from there to the pulmonary trunk.

Pulmonary veins return blood to the left atrium, goes to the thick walled left ventricle, then to the single right aortic arch then on to body.

Also 4 chambered heart, with full double circulation.

Sinus venosus is incorporated into the wall of the right atrium.

Atria and ventricles are completely divided.

Blood is forced from the right ventricle to the pulmonary trunk and lungs.

Pulmonary veins return oxygenated blood to left atrium, passed to left ventricle, then on to left aortic arch for distribution to body.

Birds and mammals have double circulation.

During the fetal development of mammals, the interatrial septum has an opening covered by a valve-like flap. This opening allows the blood from the right atrium to pass into the left atrium and bypass pulmonary circulation. Claps shut at birth.

Evolutionary changes in vertebrate heart are tied to change from single to double circuit heart, with increased separation of oxygenated and deoxygenated blood, allowing more efficient respiration and circulation to fuel high activity and increased oxygen demands associated with endothermy.

1. Sinus venosus of birds and mammals merges into wall of right atrium.

2. Atrium is partly divided in lungfishes (and salamanders), completely divided in other tetrapods

3. Conus is partly divided by a spiral fold in lungfishes and frogs. It is completely divided into three trunks in reptiles and into two trunks in birds and mammals

The changes to the heart were accompanied by changes to the aortic arches and thus to the rest of the circulatory system.

The dorsal aorta is a continuous vessel in embryo, bent to form a series of aortic arches.

1st bend = 1st aortic arch

When the pharyngeal arches develop, cross links are formed between the dorsal and ventral aortae, one for each pharyngeal arch.

Almost all vertebrate embryos exhibit 6 aortic arches.

Ancestral condition (shown in some vertebrate embryos) may have more.

In gill breathing fishes, the aortic arches are retained and provide afferent branchial arteries to the gill arches.

In adult vertebrates that lack gills, the embryonic and ancestral pattern of 6 aortic arches is highly modified with development.

The most extreme modifications occur in birds and mammals, but the beginnings of these changes can be seen in fish.

These modifications revolve around change from gill to lung respiration and the evolution of the double circulatory system.

Figure 11.13A shows ancestral condition, seen from side of animal, with 6 aortic arches (anterior arches have been lost).

Fish:

Figure 11.13B - gill respiration

The aortic arches of gill bearing vertebrates are primarily for bringing blood from the heart via the ventral aorta through the gills, where the blood is oxygenated and drained via the efferent branchial arteries into the dorsal aorta for circulation to the body.

Fish embryos have 6 arteries, but the first arch (I) is generally lost or modified.

The 2nd arch (II) is present in elasmobranchia, but is lost in many other fish.

Lungfish

Figure 11.13D - gills and lungs present

Lungfish depend on lungs for breathing and have lost the capillary networks associated with gills of arches III and IV. The corresponding arches III and IV are uninterrupted vessels.

When arches I and II are lost, the anterior extensions of the dorsal aorta from arch III continues to the head as the internal carotid arteries.

V & VI still have gill capillary networks.

Pulmonary arteries arise as vessels from arch VI, go to lungs of lungfish or swim bladder in coelocanth.

Pulmonary veins return blood to heart via the left atrium.

Not a highly efficient system, but has some ability to shunt blood to regions of the body where increased demand for oxygen is necessary

Changes from elasmobranch -> lungfish, with evolution of pulmonary circulation, are one of the most important steps in the evolution of circulatory systems of vertebrates

Anuran (frog)

Figure 11.13G

Changes become more pronounced

Arches I and II disappear during development.

Arch V disappears in anurans, but is present in some urodeles (salamanders), leaving intact arches III, IV, VI

Dorsal link between III and IV gets thin in urodeles (salamanders) and almost disappears in anurans.

Arch III is now the internal carotid artery.

Right and left arches of arch IV are now right and left sides of systemic aorta.

Arch VI is intact and goes to lung.

Figure 11.13H

Aortic arches I, II, V disappear.

Dorsal connection between III and IV may be lost (not shown in diagram)

Arch III forms part of the internal carotid arteries and forward extensions of ventral aortae form external carotid arteries.

3 vessels emerge from the ventricle:

1. a pulmonary trunk that branches to the pulmonary arteries, formed from arch VI from right ventricle

2 & 3: a right and left systemic aortic arch derived from arch IV

generally right systemic arch (IV) comes from left side of ventricle and

left systemic arch (IV) comes from right side of ventricle

Arch VI -> lung

Arches I, II, V disappear

Arch IV forms systemic aorta on right side and first part of subclavian artery on left side

Left root of dorsal aorta disappears, while the one on the right remains and becomes the aortic arch.

Arch VI -> lung

Arch III -> internal and external carotid arteries

Figure 11.13I

Aortic arches of mammals have same developmental history and fate as those of birds, with one big exception.

Outstanding difference between bird and mammal is that the aortic arch in the bird is derived from the right side of aortic arch IV and that of the mammals is derived from the left side of aortic arch IV.

Systemic aorta in mammals emerges from left ventricle and goes sharply to the left.

The right aortic arch forms the first part of the right subclavian artery.

From the right subclavian artery emerges the right common carotid, going to the head and neck.

The common trunk of the right subclavian and the right common carotid is called the brachiocephalic artery.

Separation of right and left atrium

increasing separation of right and left ventricles

Deoxygenated blood on right side of the heart, oxygenated blood on left side of the heart

In ancestral condition, separation is not complete, but structures like trabeculae help to maintain separation.

Aortic arches: changes associated with heart changes

Loss of Arches I, II, V

Modification of arches III, VI (pulmonary circulation)

Retention of both sides of arch IV to form aortic arch in reptiles

Birds lose left side, mammals lose right side of arch IV.

Trend for separation of oxygenated and deoxygenated blood

These changes resulted from the changes from gill to lung respiration, change from aquatic to terrestrial life.

Changes led to the development (in lungfish) of a double circulatory system from a single circulatory system.

These changes provided a more efficient circulatory and respiratory system to fuel the high activity levels and active metabolism associate with endothermy.