The function of the excretory organs in invertebrates and vertebrates is to maintain homeostasis. During evolution, the mammalian kidney developed a mechanism which regulated the redistribution of fluid and ions within the nephron.
As the kidney evolved in vertebrates, the rate of glomerular filtration and proximal reabsorption increased. 
​The microbes and invertebrates used simple methods to excrete their metabolic waste products.Three types of excretory systems evolved in the microbes and invertebrates before the complex kidneys in the vertebrates- contractile vacuoles, flame cells, malpighian tubules.

The single celled amoeba (unicellular Protozoa) were the earliest forms of life that evolved in the ocean. Nitrogenous waste diffused out of the cell membrane. The “contractile vacuole” was mainly for salt and water balance. It merged with the cell membrane and expelled the waste out into the environment by exocytosis. Hence, it was not exactly a true excretory organ. (Figure 1)

Figure 1– Amoeba – Food is taken in by endocytosis. The food vesicle is broken down by lysosomes. The excess water and salt is expelled out by contractile vacuoles via exocytosis.

With the evolution of multicellular organisms, different organ systems for various metabolic functions were formed. Planaria (flatworms) are freshwater worms. Their main excretory organ is the Protonephridia or “flame cells”. The cilia in flame cells facilitated fluid influx from parenchyma to the tubule.The two tubules are connected to the bladder and an exit orifice.

Figure 2(a) Flame cell of a planarian. 2(b) Nephridium of an earthworm

Annelids (Earthworms) developed a more evolved excretory system called “nephridia”. Each segment of the earthworm has a pair of nephridia.They have a tubule with cilia similar to flame cells. Excretion was by a pore called “nephridiopore”. As opposed to flame cells, these nephridia have a tubular system for reabsorption by a capillary network making them more evolved than the flame cells.(Figure 2b) Beyenbach et al.Acta Physiol (Oxf).2011

With further evolution, malpighian tubules, the main excretory organs in insects, were formed (Figure 3). They are usually found in pairs. These tubules are convoluted and have microvilli for absorption and maintenance of osmotic balance. Excretion of waste is mainly by secretion from the malpighian tubules which are bathed in hemolymph. There is no filtration process happening like in the nephridia.There are active ion pumps in tubules for secretion and reabsorption of ions. The malpighian tubules join the gut (coelomic membrane) at the junction of the upper two-thirds and lower third. Here, the gut also performs a major role of solute and water absorption. In dry conditions, water and electrolytes get reabsorbed and uric acid is excreted in the form of a thick paste. This system bears close resemblance to vertebrate kidneys.

Figure 3: Malpighian tubules

Vertebrates

Fish

The hagfish (of the NephMadness fame) is considered to be a bridge in the evolution of vertebrates from invertebrates. Though they come under the scientific classification of  vertebrates, they have only the skull and no vertebra. Hagfish has many features of marine invertebrates.They are osmoconformers. The serum osmolarity of the Hagfish is same as that of sea water (>1000mOsm/L). They regulate only divalent ions (Figure 4).

Figure 4: Hagfish as a bridge between invertebrates and vertebrates.. Visual abstract by Sophia Ambruso

The Cambrian period (Figure 5) opened with the violent formation of mountain ranges. Most of these have withered away.The sediments are visible today in the yellow and brown layers of the Grand Canyon, cut across by the Colorado river.

Figure 5: Synopsis of the evolution of the vertebrates in relation to saltwater (darkly shaded) and freshwater (lightly shaded) habitat. The irregular curve illustrates mountain-building episodes (geologic revolutions) which have influenced this evolutionary history. The time scale is such that the Pleistocene era and recent time are compressed.

During this Cambrian period, with this small equipment of a coelomic membrane (like the malpighian tubules) and segmental ducts, the first chordates started their migration from the sea, ventured into brackish estuary, and swam up the rivers till they reached the inland lakes. As their body was equipped to handle a higher osmolality marine environment, they could not handle hypotonic freshwater habitat. This hypotonic freshwater would cause their salt rich body to swell and die. Hence, they came with waterproofing mechanisms and covered their body from head to tail with shells.They were called “Ostracoderms”- shell skinned fishes (Figure 6). The fossils of vertebrates from the Silurian and Devonian period (Figure 5) are a proof of this insulation process against freshwater.

Figure 6: A Collection of extinct Ostracoderms – Shell skinned armored fishes. Image by Franz Anthony 

The development of external armour was associated with many internal changes as well. The multiple coelomic openings of the various body segments were obliterated, a pair of tubules were now arranged to open into one posterior orifice which pierced the armoured tough skin. This pair of tubules were called “archinephric ducts”(Figure 7)

Figure 7: Hypothetical primitive kidney of ancestral vertebrates – Archinephric duct Balinsky BI et al. An Introduction to Embryology. (5th edn).1981

The armour alone did not provide sufficient protection from freshwater as the mouth, gills, and the intestines absorbed hypotonic freshwater and the heart had to pump out extra water from the body. The easy way out would be to bring the pre-existing arteries in juxtaposition with the coelomate tubules to form a “coelomate glomerulus” (lobulated tuft of capillaries). This can still be seen in some of the lower vertebrates (fishes and amphibians) hanging in the pericardial cavity (heart sac). In the due course of time, a direct connection between the arteries and the tubules was formed outside the coelomic cavity. This is the “glomerulus” found in the mesonephros and metanephros of higher animals. This makes it clear here that the tubules evolved first followed much later by the glomerulus.

With the advent of this high pressure filtration system, most of the osmotically active valuable contents of the plasma such as amino acids, glucose except plasma proteins were filtered into the tubules. The tubules evolved in such a way, so as to reabsorb the filtered valuable contents of the plasma and excrete more water, less salt in freshwater.

This adaptation of freshwater kidney was adequate for survival till the next geological revolution took place. At the close of the Silurian period (Figure 5), the restless earth heaved again. This time a ridge higher than Alps wrinkled up in the North of Europe. The present day low Caledonian mountains in Scotland are the remnants of this mountain. Most of the land was submerged under the sea. The remaining land had extremes of climate, either heavy rainfall or drought. The Devonian fish had to choose between invading salty marshes or small freshwater pools which quite often dried up to form stagnant pools or hard mud flats. Some of the powerful Elasmobranchii (cartilaginous fishes like present-day sharks and stingray) as well as many bony fishes abandoned the freshwaters and went back to the sea. 

The Elasmobranchii (cartilaginous fishes) found a way to survive in the sea water. They developed a unique tubule segment distal to the glomerulus to reabsorb the filtered urea till the blood levels of urea reached as high as 1300mg/dL. This amount of urea in the blood increased the osmolality above that of the sea water, facilitating the absorption of pure water (devoid of salt) through the gills from the sea water.This facilitated continuous movement of free water into the body which was required to excrete the waste products.Hence, none of them have abandoned the glomeruli. There was availability of plenty of free water for the glomeruli to function in these species

When the bony fishes (mostly Ray finned fishes) (Figure 8) migrated from the freshwater to the sea–which was now hypertonic compared to the blood– the water diffused out of the body and many of them died due to dehydration and became extinct. The remaining ones, over the years, slowly lost their glomeruli which had now become a liability. These fishes had to conserve water for survival in the sea,while the glomeruli were busy filtering and eliminating it. Hence, they had to get rid of these glomeruli. The glomeruli became fewer and fewer in number. They were now able to conserve water as much as possible and excrete only as much required to get rid of waste products. Most of the marine teleosts (like eels) have evidence of glomerular degeneration  while some like the seahorse (of NephMadness fame), batfish, and the goosefish (used by Homer Smith) have become totally aglomerular and possess only tubules.

Figure 8: Vertebrate evolution timeline. Image credit Dr. Guojie Zhang

When faced with the choice of whether to stay [in freshwater] or go [to the sea], some fish (lobe finned bony fishes) remained in the stagnant pools and developed lungs; their extinct relative is the lungfish.(Figure 9)

Figure 9: Tiktaalik roseae (now extinct) was a species of lungfish. It had both lungs and gills. It is a fossil fish which bridged the gap between animals of water and land. 

This lineage went on to evolve into terrestrial vertebrates. The fins gradually evolved into feet and thus came the amphibians. These amphibians occasionally visited pools to drink water or lay eggs.

Amphibia

These adaptations lasted till the Permian period (Figure 5). Following the great Appalachian revolutions, a new mountain range erupted between what is now known as Newfoundland and Alabama.The southern hemisphere experienced a glacier period. The northern hemisphere was arid and chilly. Due to extremes of aridity, amphibious ancestors were forced to live permanently on land. It was now that they evolved to more terrestrial forms; and so were born reptiles. These new reptiles possessed hard hides and long feet to travel from one water hole to another. For the first time in history, the eggs of these reptiles possessed waterproof shells and the allantoic sac collected the waste products of the embryo. Many adaptations had to take place to convert these amphibians to completely terrestrial reptiles. One of them was protein combustion. So, now they no longer metabolized protein to urea, instead they converted it to uric acid in order to rid the body of waste. This was a water conservation technique. It takes less energy, but more water to excrete nitrogen as urea. Also, uric acid has some amazing properties. It supersaturated and precipitated out of water. So immediately before leaving the cloaca, the water gets reabsorbed and uric acid precipitated to a salty paste which is excreted by the reptiles and birds. These birds were nothing but reptiles with wings. These reptiles dominated the earth during this period.

The reptiles grew their feet long and crawled on their bellies all over the world. Some of the more advanced ones started to walk on their hind feet. This was the Jurassic era. The dinosaurs dominated the land.

Mammals

No, I have not forgotten humans! Humans are just one of the thousands of species of mammals and constitutes a very small fraction of vertebrates. The geological age of man is just 1 million years, much less than the other vertebrates. Now let’s see the evolution of mammals from these reptiles! 

Mammals were seen for the first time at the beginning of the Cenozoic era (Figure 5). The highlight of mammalian kidney is that it can form hypertonic urine. 

Permanian time was the greatest ice age period of all time. In order to cope with the extreme chilly habitat, ”proto mammalians” – warm blooded animals – evolved. To keep the body warm, the heart pumped more blood, increasing the blood pressure and thus, increasing glomerular perfusion. In order to reabsorb the high quantity of filtered water, there was evolution of the middle segment of the tubules. These tubules reabsorbed the large quantity of filtered water. This adaptation helped the mammals survive in conditions of extreme aridity as well by intense water reabsorption and conservation. As mammals were better equipped to tolerate both frigidity and aridity they continued to survive and evolve. Then came the Laramide revolution where the temperature changed to extremes of cold. As reptiles were cold blooded animals and they could not not tolerate extremes of chilly conditions, many of them reached extinction during this period. The warm blooded furry mammals continued to survive.

The reptile kidneys do not have the intermediate tubule (loop of henle) for reabsorption, whereas the mammalian kidneys have it. The bird kidney is intermediate between the two. Some have, while some do not have the intermediate segment (loop of henle) of the tubule.They have retained uric acid excretion habitus like the reptiles, and some can produce hypertonic urine like the mammals.

Towards the end of the Cretaceous period mammals began to grow in number. In the Oligocene and Miocene period, Dryopithecines apes populated Asia, Africa and Europe. Then came in the giant Himalayas. As the mountain ranges of Himalayas buckled up, most of central Asia became inhabitable and these apes were forced to abandon the trees. Some of these apes who managed to survive were driven towards south Asia. From south Asia, the descendants reached Africa. Gradual evolution took place and in the Pliocene period (Figure 5) Plesianthropus transvaalensis and Paranthropus robustus were formed. These species were discovered recently in Africa. They resembled neither man nor ape and were called “ape-man”.Gregory WK et al. Evidence of the Australopithecine man-apes on the origin of man.1938. Human kidneys bear the closest resemblance to its ancestral apes from the Miocene period.

The human glomerulus filters 125 ml of blood every minute. The tubules have to reabsorb 99% of the filtered load. On the other hand, in order to filter 125 ml of blood every minute the heart is constantly pumping 1.2 liters of blood (25% of cardiac output) into the kidneys. The heart is pumping in large quantities of blood and the tubules have a tough job of reabsorbing 99% of it back into the circulation. So, the heart and the kidneys are constantly working against each other. This raises an important question: are human kidneys really efficient or are they still evolving? Meanwhile, the Earth is planning on its next geological revolution…

     Evolution of  Excretion