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Renal Evolution Revisited Annals of Anatomy 233 (2021) 151610 Contents lists available at ScienceDirect Annals of Anatomy j ournal homepage: www.elsevier.com/locate/aanat The struggle to equilibrate outer and inner milieus: Renal evolution revisited ∗ Laura Keogh, David Kilroy, Sourav Bhattacharjee School of Veterinary Medicine, University College Dublin (UCD), Belfield, Dublin, Ireland a r t i c l e i n f o a b s t r a c t Article history: The journey of life, from primordial protoplasm to a complex vertebrate form, is a tale of survival against Received 26 February 2020 incessant alterations in climate, surface topography, food chain, and chemistry of the external environ- Received in revised form ment. Kidneys present with an ensemble embodiment of the adaptations devised by diverse life-forms to 14 September 2020 cope with such challenges and maintain a chemical equilibrium of water and solutes, both in and outside Accepted 15 September 2020 the body. This minireview revisits renal evolution utilizing the classic: From Fish to Philosopher; the story of our internal environment, by Prof. Homer W. Smith (1895–1962) as a template. Prof. Smith’s views Keywords: exemplified the invention of glomeruli, or its abolishment, as a mechanism to filter water. Moreover, Kidneys with the need to preserve water, as in reptiles, the loop of Henle was introduced to concentrate urine. Renal evolution When compared to smaller mammals, the larger ones, albeit having loops of Henle of similar lengths, Loop of Henle Chemical equilibrium demonstrated a distinct packing of the nephrons in kidneys. Moreover, the renal portal system degener- Glomerulus ated in mammals, while still present in other vertebrates. This account will present with a critique of the current concepts of renal evolution while examining how various other factors, including the ones that we know more about now, such as genetic factors, synchronize to achieve renal development. Finally, it will try to assess the validity of ideas laid by Prof. Smith with the knowledge that we possess now, and understand the complex architecture that evolution has imprinted on the kidneys during its struggle to survive over epochs. © 2020 The Author(s). Published by Elsevier GmbH. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). 1. Introduction Being a crucial organ involved in homeostasis (Kotas and Medzhitov, 2015; Modell et al., 2015; Stanger, 2015; Röder et al., Kidneys are indispensable in maintaining the chemical com- 2016), the evolution of kidneys has steadily attracted academic position of extracellular fluids (ECF) that continuously bathe scrutiny due to its role in chemical surveillance of the environ- our internal organs to ensure health and survival (Youn and mental milieu organisms thrive. It is necessary to appreciate that McDonough, 2009; Hoenig and Zeidel, 2014; Blaine et al., 2015; the environment, along with its countless interactions with living Palmer, 2015; Stanhewicz and Larry Kenney, 2015). Renal anatomy cells—from simple unicellular organisms to complex multicellular and physiology, in their existing forms, present with an astound- ones—are chemical processes that, at times, can be incompati- ing level of complexity, incredible precision, and added to its role ble with life. It is thus imperative that our current anatomy is in excretion, exhibit a spectacular ability to monitor, sustain, and the ensemble package of all such protoplasmic reactions, from introduce alterations in the composition of ECF. Despite being only the moment of its emergence on earth to a gamut of environ- 1% of the body weight in humans, kidneys receive 20% of the cardiac mental stimuli received throughout the history of evolution. Being output and contribute 10% to the entire oxygen consumption of the involved in the process of adaptation to an ever-changing envi- body (Chevalier, 2017). In order to demonstrate such remarkable ronment, including varied habitats and fluctuating food chains, as feats, kidneys have emerged as one of the most perfused organs in an organ, kidneys have evolved drastically over epochs to support vertebrates, especially in mammals, such as humans (Fig. 1), where life in its struggle to exist through uneasy geological vicissitudes, the entire pool of blood is circulated multiple times daily through which at times, had been hostile. History of the earth as a stellar them. body is anything but consistent, while it undergoes a circadian, and, at times, unexpected catastrophic changes—as reflected in a con- tinuous background level of extinction of terrestrial biomass with ∗ intercalated mass extinction events noted throughout the history Corresponding author. E-mail address: [email protected] (S. Bhattacharjee). https://doi.org/10.1016/j.aanat.2020.151610 0940-9602/© 2020 The Author(s). Published by Elsevier GmbH. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). 2 L. Keogh, D. Kilroy and S. Bhattacharjee / Annals of Anatomy 233 (2021) 151610 Fig. 1. (A) the human urinary system, (B) cross-section of a human kidney with its internal anatomy, and (C) structure of a typical mammalian nephron with a filtering mechanism. of life on earth (Jablonski, 2001; McElwain and Punyasena, 2007; The objectives of this mini-review are: (i) to understand the Carpenter and Bishop, 2009; Whiteside and Grice, 2016). discourse of renal evolution as a venture of sustaining life on this With an estimated 10% of the global population now affected planet, and maintenance of an equilibrium of water, with dissolved and millions of deaths registered each year, renal ailments, includ- solute, between the exterior and interior milieus of an animal body; ing acute kidney injury (AKI), chronic kidney disease (CKD), and (ii) to examine the evolution of kidneys, from protovertebrates to end-stage kidney disease (ESKD), are an ongoing pandemic (Kam mammals, with gradually increasing anatomical complexity; (iii) Tao Li et al., 2013; Susantitaphong et al., 2013), while the crisis to assess how different geological vicissitudes, with intercalated is aggravated further by the surge of hypertension and diabetes mass extinction events, has influenced the anatomy and develop- cases in association to obesity. The Global Burden of Disease (GBD) ment of kidneys; (iv) to estimate the validity of concepts in renal study conducted in 2015 by the World Health Organization (WHO) evolution, as formulated by Prof. Homer W. Smith, in the light of reported a staggering 1.2 million deaths (Wetmore and Collins, current evidence, and scholastic arguments. 2016; Luyckx et al., 2018) and 19 million disability-adjusted life years (DALYs) due to cardiovascular diseases caused by a com- 2. The troubled history of earth and evolution of life promised glomerular filtration rate (GFR). Even more worrying news is that the mortality due to CKD recorded a 32% growth There remain plenty of gaps in the existing knowledge on the from 2005–2015. Almost two million people, mostly from the USA, timeline of earth. Still, a widespread consensus is that the solar Japan, Germany, Brazil, and Italy—are currently undergoing dialy- system was created almost 4.6 billion years ago from the condensa- sis (Fig. 2). Such a spike in the number of patients suffering from tion of interstellar dust. Some of the superficial rocks on earth were renal diseases is causing a substantial financial burden and human noted to be as old as 4.5 billion years, thus, comparable to the solar suffering on a planetary scale. In the US only, the cost of treating system. Over many epochs, the composition of the earth, encased CKD patients has already exceeded $48 billion per year (Damien within its spherical shape (Fig. 3A) and rich in varied landscapes et al., 2016). Similarly, in the UK, the cost of providing health care with minerals often noticed as rocky lumps (Fig. 3B), has under- to CKD patients is hefty, and more than the combined expendi- gone drastic reorganizations. Thus, the internal structure of the ture of breast, lung, colon, and skin cancer cases (National Kidney earth is heterogeneous and displays layers of concentric spheres, Foundation, Global facts). Given the clinical significance of renal with heavier ones displaced more toward the core while the lighter health, today, more than ever, a critical understanding of renal ones laid gradually on top of them. While moving from the surface anatomy and physiology is necessary as our kidneys present with to core, terrestrial contents are roughly divided into the following an embodiment of the struggle for survival and adaptation of life, layers (Boehler, 1996; Hawkesworth et al., 2017): starting its journey as a simple protoplasmic mass to the complex mammalian form that we now encounter. (i) Crust: the thickness of 2–3 miles below the oceans, and 30–50 Published first in the year 1953, the treatise: From Fish to Philoso- miles beneath the continents. pher; the story of our internal environment by famous American (ii) Mantle: the overall thickness of ∼1800 miles with two distinct physiologist, Prof. Homer W. Smith (1895–1962), based on the layers: an outer basaltic layer and an inner layer of metal- evolution of kidneys, is a cult classic within the community of phys- lic oxides plus sulfides. The continents, composed mainly of iologists, zoologists and evolutionary biologists. With inimitable granites, float on the mantle as relatively lighter chunks. lucid prose, the disquisition traced the evolution of kidneys—from (iii) Core: a very dense layer composed mostly of heavy molten archaic aquatic invertebrates to contemporary mammals—while metals, such as iron and nickel. correlating its findings to a series of environmental changes that the planet had been through. The book is an indispensable the- Unfortunately, such theories continue to rely on indirect exper- sis for those who are interested in understanding kidneys as vital imental evidence, such as the propagation velocities of seismic organs, and even more importantly, as an archive of evolutionary waves and, thus, leave room for interpretation and debate.
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