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Full Review the Evolution of Blood Pressure and the Rise of Mankind

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Full Review the Evolution of Blood Pressure and the Rise of Mankind NDT Advance Access published August 18, 2014 Nephrol Dial Transplant (2014) 0: 1–11 doi: 10.1093/ndt/gfu275 Full Review The evolution of blood pressure and the rise of mankind Kevin Schulte, Uta Kunter and Marcus J. Moeller Downloaded from Department of Nephrology and Clinical Immunology (Internal Medicine II), RWTH Aachen University Hospital, Aachen, Germany Correspondence and offprint requests to: Marcus J. Moeller; E-mail: [email protected] http://ndt.oxfordjournals.org/ still outrun antelopes—or even the cheetah, the fastest land ABSTRACT animal [1]. ‘Persistence hunting’ requires that humans run for ∼2–5 h over some 25–35 km (16–22 miles) until their prey is Why is it that only human beings continuously perform acts of too exhausted to continue [2–4]. Out of all mammals, only heroism? Looking back at our evolutionary history can offer us humans are able to deliver such high physical performances some potentially useful insight. This review highlights some of — fi over such prolonged periods of time. the major steps in our evolution more speci cally, the evolu- Today, running a marathon has become a popular sport at Pontificia Universidad Católica de Chile on August 23, 2014 tion of high blood pressure. When we were fish, the first kidney fi ‘ ’ among modern humans; the average nishing time has re- was developed to create a standardized internal milieu preserv- mained quite constant (∼4.5 h) over the past decades. Unlike ing the primordial sea within us. When we conquered land as the first official marathon runner, the messenger Pheidippides, amphibians, the evolution of the lung required a low systemic who according to the legend collapsed dead after exclaiming blood pressure, which explains why early land vertebrates (am- victory to the Athenians in the Battle of Marathon in 490 BC, phibians, reptiles) are such low performers. Gaining independ- the mortality rate does not increase significantly from running ence from water required the evolution of an impermeable skin a marathon. In a recent analysis of more than a million mara- and a water-retaining kidney. The latter was accomplished twice thon runs, the mortality rate was only 0.00075% within the with two different solutions in the two major branches of verte- first 24 h [5]. brate evolution: mammals excrete nitrogenous waste products as In the present review, we will investigate why humans are urea, which can be utilized by the kidney as an osmotic agent to such extraordinary long-distance performers and why appar- produce more concentrated urine. Dinosaurs and birds have a ently only our species persistently delivers heroic acts. Special distinct nitrogen metabolism and excrete nitrogen as water-in- — emphasis will be placed on the central role of the kidney on soluble uric acid therefore, their kidneys cannot use urea to our long and ever-lasting pursuit of personal bliss. concentrate as well. Instead, some birds have developed the cap- ability to reabsorb water from their cloacae. The convergent de- velopment of a separate small circulation of the lung in THE PRIMORDIAL OCEAN WITHIN US: mammals and birds allowed for the evolution of ‘high blood- INVENTION OF THE KIDNEY pressure animals’ with better capillarization of the peripheral tissues allowing high endurance performance. Finally, we inves- We will begin our journey towards personal happiness with tigate why mankind outperforms any other mammal on earth the fish, which evolved ∼500–350 million years ago (Figure 1). and why, to this day, we continue to perform acts of heroism on As already well illustrated by Homer W. Smith [6], one of the our eternal quest for personal bliss. major novel inventions of the fish was its capability to actively Keywords: blood pressure, evolution, kidney stabilize its internal milieu. Remarkably, the relative ionic composition (sodium, potassium, chloride and calcium) of the extracellular fluid is virtually identical in fish as well as in all INTRODUCTION subsequent animal species (including amphibians, reptiles and mammals) [7] (Table 1). In some Aboriginal parts of our world (e.g. the African Kala- Because the salt concentration of the ocean has increased hari, the northwestern parts of Mexico or Australia), humans steadily over time, saltwater fish have a hypoosmolar internal © The Author 2014. Published by Oxford University Press 1 on behalf of ERA-EDTA. All rights reserved. Downloaded from http://ndt.oxfordjournals.org/ at Pontificia Universidad Católica de Chile on August 23, 2014 FULL REVIEW FIGURE 1: Chronological overview. From fishes, two major continuous separate evolutionary pathways can be traced which lead either to mammals (including humans) or to birds (including dinosaurs). Both branches show similar phenotypic stages of development (e.g. the stages of the lungfish and amphibian-like and reptilian-like animals). However, as evidenced by the different anatomy of the lung, the evolution of both branches was separate, even though similar (convergent) developments occurred (e.g. water-impermeable skin, separation of the pulmonary cir- culation, high blood pressure, warm-bloodedness etc.). The position of each animal klades (species) indicates the approximate time point of the ‘last most common ancestor’ [8]. Each transition of the geological ages (indicated on the left) was accompanied by mass animal extinctions and a subsequent rise in novel animal klades (species). Examples for monotremes and marsupials are the platypus and kangaroo. milieu and lose water constantly to the hyperosmolar environ- via the gill epithelium [11, 12]. From an evolutionary perspec- ment. To cope with this problem, saltwater fish drink up to tive, one might say that fish ‘invented’ the kidney. In fact, 25% of their total body weight per day [9, 10]. To excrete the glomeruli and tubuli evolved independently and were com- electrolytes of the ocean water, most of the sodium and chlor- bined only later into a single functional unit, the kidney. The ide is excreted in an adenosintriphosphate-dependent process kidney’s predominant role in saltwater fish is the excretion of 2 K. Schulte et al. Table 1. Extracellular electrolyte concentration of the major inorganic ions exchange by diffusion (∼1 µm). Such a thin air-blood barrier in vertebrates in comparison to the salt concentration of the ocean limits the pulmonary perfusion pressure to less than ∼30–40 – Sodium Chloride Potassium Calcium mmHg (407 543 mmH2O). If the perfusion pressure were fi fi fl Ocean 100 116.4 2.17 2.19 higher, signi cant pressure-driven ltration of uid into Fish 100 89.6 1.95 1.87 the alveoli would occur. The consequences of even a minor Amphibians 100 91.6 3.03 1.74 increase in pulmonary pressure are illustrated in clinical prac- Reptiles 100 68.5 4.15 2.22 tice in patients with myocardial failure. These patients charac- Mammals 100 71.4 2.85 1.78 teristically develop pulmonary oedema and respiratory distress To enable the comparison of the chloride, potassium and calcium concentration, sodium because of increased pressures within the pulmonary veins was standardized to 100 mmol/L, and the same correction factor was applied for the and subsequently impaired gas exchange. other ions. Because the lung developed from the front gut, its blood supply was first identical to that of all other tissues (Figure 2). divalent ions (especially magnesium) [7, 13]. Saltwater fish es- For this reason, the systemic blood pressure had to be relatively sentially form only the equivalent of the proximal tubule; thus, low in early air breathers (i.e. lungfish, amphibians, reptiles). their urine osmolarity is always similar to the serum osmolar- As evolution proceeded, the circulatory system of the lung was Downloaded from ity [13]. gradually isolated from the systemic circulation. An incom- When the fish conquered freshwater, the situation was re- plete septum separating the heart ventricle first introduced the versed: the internal milieu of the fish was of a higher osmolar- advantage that oxygen-rich blood could be diverted into the ity with respect to freshwater, resulting in potential systemic circulation. When the animal was holding its breath hyperhydration. The problem was solved in part by increasing (e.g. when diving), the lung could be shunted. This is because http://ndt.oxfordjournals.org/ the glomerular filtration rate (GFR) and with the development pulmonary vasoconstriction occurs when oxygen tension in of a distal tubulus. Freshwater fish are capable of excreting a the lung is low. The venous blood is diverted directly into the hypoosmolar urine relative to plasma (the first—but inefficient systemic circulation via the gap in the septum of the heart —salt-retaining kidney). This is why thiazide diuretics (target- (Euler–Liljestrand mechanism [20]). Hypoxic pulmonary ing the distal tubule) induce more of a saliuresis rather than an vasoconstriction is evolutionarily preserved due to various aquaresis (i.e. the relative loss of salt in the urine exceeds that additional advantages. However, it is also the reason for pul- of water). In addition, the urinary bladder and the gills also re- monary oedema in mountaineers at high altitudes. FULL REVIEW absorb sodium and chloride in freshwater fish [14, 15]. The at Pontificia Universidad Católica de Chile on August 23, 2014 GFR is quite variable in fish. In saltwater fish, up to 90% of the glomeruli may not actually be filtering [16]. The glomeruli WHY FROGS ARE NOT GOOD RUNNERS may be reactivated in states of hydration. This phenomenon is called ‘glomerular intermittency’ and is relevant particularly A low systemic blood pressure is the reason why early land in fish transitioning between salt- and freshwater. animals are unable to deliver a sustained high physical per- In summary, from our early days as fish, we have taken the formance. The adaptive changes in the microcirculation of primordial ocean with us. The kidney was developed to main- low-pressure animals explain why these animals are not good tain a standardized internal milieu within us.
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