A Homeric view of kidney evolution: A reprint of H.W. Smith's classic essay with a new introduction

In From Fish to Philosopher (1953), Homer W. Smith melds his groundbreaking physiological studies with geological and evolutionary musings to present an amazingly integrated view of how adaptation of a single organ may have contributed to the evolution of man. A condensed version of this thesis was presented in a lecture to the School of Medicine at the University of Kansas in 1943 and later published by the University of Kansas Press (Smith, 1943). This holistic view of how selection led to adaptation of the kidney in response to the move from saltto freshwater, and in the example of the elasmobranchs and bony fishes back to saltwater again, is an extraordinary piece of evolutionary exposition. Knowledge has advanced since 1940 but as a work of integrative logic, and a beautiful piece of writing, it has few rivals. This essay begins with the cooling of the earth four billion years ago. The cooling of the crust produced periodic upheavals that had major effects on the earth’s atmospheric conditions, which in turn led to changes in selective pressure. Smith describes how the migration from the oceans to freshwater challenged the physiology of invertebrates and protovertebrates and proposes how these pressures were dealt with through the evolution of the kidney. As upheavals drove the early freshwaterinhabiting vertebrates either back to the sea or onto the land, once again physiological barriers had to be overcome, largely by the kidney. Some of Smith’s early physiological studies were conducted on the African lungfish and the changes that occur as these animals escape drought through estivation (summer sleep: the opposite of winter hibernation) in mud burrows. These animals can survive for years without food when encased in dry mud. In this state, the animal needs to adapt from a situation in which water influx and excretion are dominant processes to one in which there is absolutely no water intake and no production of urine. The lungfish therefore cyclically deals with similar physiological pressures to those faced by vertebrates in the course of evolution and musing on these changes probably contributed enormously to the thesis presented in the essay reproduced here. As a researcher investigating development of the kidney, I find this vision of evolution modifying organogenesis (and organogenesis modifying physiology) to be extremely useful. A wealth of comparative systems exist in nature that could allow us to link genetic change to developmental adaptation. One particularly useful example outlined by Smith is the aglomerular kidney’s of certain marine fishes. Which of the genes postulated to be essential for glomerular development are no longer expressed during organogenesis in these animals? One such gene, WT1, is still present in the genome of the aglomerular (Marshall, 1929) pufferfish (Miles et al., 1998), but has changes that may render it nonor partially functional. As the genomes of both glomerular (zebrafish) and aglomerular (Fugu) fish are now available, this problem is ripe for exploration. Amphibians initially live in an aqueous environment, but in many species spend large amounts of adult time terrestrially. These animals switch kidneys along with environments during metamorphosis with larval pronephroi dedicated to excreting water and adult mesonephroi dedicated to retaining it (Vize et al., 2003). What developmental adaptations are associated with this transition? How do the permanently aquatic water excreting mesonephric kidneys of zebrafish differ from those of the water-retaining amphibians? Both Danio and Xenopus genomes will soon be completely sequenced and provide powerful tools for investigating such questions. Smith’s essay provides a framework for thinking about how genetic change may drive physiological specialization and brings to light a wealth of interesting material and experimental possibilities. If readers enjoy this essay, they will be even more impressed by the expanded detail offered in From Fish to Philosopher (1953). Other excellent works by Smith include a semifictional account of his adventures obtaining lungfish for physiological studies in Kamongo (1932); an edited collected works, Homer William Smith: His Scientific and Literary Achievements (1962); and the philosophical Man and His Gods (1952), with a foreword by Albert Einstein.