The Theory of the Cell State and the Question of Cell Autonomy in Nineteenth and Early Twentieth-Century Biology

C Cambridge University Press Science in Context 20(1), 71–95 (2007). Copyright  doi:10.1017/S0269889706001141 Printed in the United Kingdom The Theo...
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C Cambridge University Press Science in Context 20(1), 71–95 (2007). Copyright  doi:10.1017/S0269889706001141 Printed in the United Kingdom

The Theory of the Cell State and the Question of Cell Autonomy in Nineteenth and Early Twentieth-Century Biology Andrew Reynolds Cape Breton University, Nova Scotia, Canada

Argument A central thesis of the cell theory of biological organization is that plant and animal cells are, to some degree, autonomous vital units. Just how much autonomy cells possess was a matter of serious debate in the decades surrounding the turn of the twentieth century. The idea of cell autonomy was most strikingly expressed in the “theory of the cell state,” an idea based upon the metaphorical conception of higher plants and animals as social colonies of cells or elementary organisms, commonly associated with Rudolf Virchow and Ernst Haeckel. This paper explores the question of cell autonomy as it was debated within late nineteenthand early twentieth-century embryology, cytology, and physiology. While greater evidence for cell autonomy emerged from tissue culture experiments, there arose, almost simultaneously, a tendency within physiology and biochemical studies to conceive of the cell metaphorically as a chemical factory and as a subordinate part of a larger organismal whole. I argue that while these metaphors suggested conflicting views of cell autonomy, they were highly effective devices for explaining and investigating within their respective fields: the autonomous cell-organism in embryology and morphology, the subordinate cell-factory in physiology and biochemistry.

“The problem of life became twofold – the life of the community and the life of the individual . . . two great questions presented themselves: What is an individual? What is a society of individuals?" (Merz 1965, 2:415) “The principle of autonomy of the anatomical elements can be considered as one of the most fruitful in modern physiology. This principle, or under another name, this cell theory, is not a vain expression. It has been a mistake to forget it when concerned with complex organisms.” (Bernard [1878] 1974, 265) 1. Introduction In the 1850s the German pathologist Rudolf Virchow (1821–1902) introduced the metaphor of der Zellenstaat (the Cell State) to describe humans and other multicellular organisms as compound associations of individual cells. Virchow did so as part of developing the earlier cell theory into a novel and sweeping study of disease which

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he called “cellular pathology.” Following Virchow’s lead, the evolutionary zoologist Ernst Haeckel (1834–1919) adapted and further popularized Virchow’s metaphor into what eventually came to be called “the theory of the cell state” in his many books and papers.1 Both Virchow and Haeckel emphasized the priority of the individual cells within the tissues and organs of a living body as the true units of vital phenomena, making humans and other higher animals (Metazoa) and plants (Metaphyta) composite arrangements of these more “elementary organisms.”2 But with Haeckel, who was one of the first among German biologists to take up Darwin’s theory of descent, the priority of the cell over the organism as a whole also assumed an evolutionary significance, in the sense that multicellular plants and animals were said to have evolved from colonial associations of the one-celled organisms which he classified together as the kingdom Protista. Throughout the latter half of the nineteenth century and into the early decades of the twentieth, this theory of animals and plants as evolved aggregates of cell-organisms, facilitated by the social-political metaphor of the cell state, enjoyed wide popularity among biologists. The metaphor of the cell state draws a comparison between the cells of an organism and the citizens of a human society or state, and in doing so it implies that a cell, like a citizen, is an individual organism in its own right, with a degree of independence or autonomy from the larger corporate body of which it is a part. This autonomy is in some instances morphologically evident (as in the case of blood cells and sex cells), but is typically less obvious physiologically speaking. The autonomy of tissue cells, which are typically connected in tightly integrated tissues and organs, is generally less apparent, but it received quite striking confirmation early in the twentieth century when tissue culture experiments revealed that cells removed from an animal can continue to live, grow, and divide on their own in complete isolation from the rest of the body. The conception of higher plants and animals as complex aggregates of more elementary organisms provided an important impetus to studies in anatomy, embryology, physiology, cytology, and evolutionary biology throughout the nineteenth and early twentieth centuries. For if cells are the primary carriers of vital phenomena then one must ask, What vital properties do cells possess? How do they behave? How do they interact? How does an organism composed of so many more elementary individuals manage to function as a stable and harmonious whole? How does a “higher” organism with differentiated tissues and organs develop from a collection of originally similar cells, all of which can be traced back to a single fertilized ovum? How did such composite and complex colonies of cells evolve in the first place? If cells are to be considered as organisms in their own right, might they also be composed of even more fundamental vital units or organisms? And if so, how do those elements stand in relation to one another and to the cell as a whole? In short the cell theory made 1 For earlier discussions of the cell state metaphor, see Temkin 1949; Canguilhem 1969; Weindling 1981; idem. 1989b; and Sapp 2003, especially chaps. 8 and 9. 2 This label for cells was proposed by the physiologist Ernst Br¨ucke (1819–92) (see Br¨ucke 1861).

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questions about the existence of different levels of organization a major theme within the biological sciences. Advocates of the cell theory, such as the French physiologist Claude Bernard (1813– 78), who is quoted in the epigraph of this paper, stressed the relative independence and autonomy of the individual cells making up a plant or animal, while their critics insisted that it is an error to lose sight of the organism as a whole in the attempt to understand the vital activity of cells, tissues, organs, and complete organisms. Opposition to the cell theory and the thesis of cell autonomy came in two chief varieties: (1) a form of explanatory holism which insisted that an adequate understanding of organismal structure and function must be sought in the collective whole of cells as they constitute a complete organism; and (2) a form of reductionism maintaining on the contrary that adequate explanations of cellular structure and function could only be obtained by further reduction to some combination of molecular forces dispersed throughout the protoplasmic substance of the cell. By the end of the nineteenth century biologists were split over the question of whether the cell is autonomous in two separate but related senses: as a stable unit of real biological organization and as an adequate unit of scientific analysis. In other words, did the cell offer the ultimate level of biological organization and investigation? or must it be further analyzed into more elementary units? or perhaps one must move upward, so to speak, to the level of the whole organism to understand the phenomena of development and physiological function. With respect to these debates over levels of organization and analysis it was a genuine question whether the cell would maintain its autonomy in either of these two senses. Within the debates reviewed in this paper three separate but related questions can be identified: 1) Are cells independent entities, both morphologically and physiologically speaking? Closely related to this question are those regarding whether “higher” plants and animals are compound arrangements of distinct cell units or some other arrangement in which the cellular structure plays only a secondary role; have the Metaphyta and Metazoa evolved from colonies of social protists or by the internal formation of cell membranes within an originally multinucleated ciliate? 2) Do the causes of the embryological development of specialized tissues and organs lie in the individual cells or are cells themselves the effect of a more fundamental organization which is dispersed throughout an original protoplasmic mass, (the ovum), which is inherited from parent organisms? In other words, do the cells build the organism or does an organism build the cells? 3) Are cells themselves elementary or composite? Are they the fundamental and primary units of life or might they perhaps be “colonies” of even more elementary vital units? At the heart of the cell state theory is the age-old philosophical question concerning the relationship between part and whole, the One and the Many. Indeed, as Georges

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Canguilhem (1969, 62) has written: “The history of the concept of the cell is inseparable from the history of the concept of the individual.”3 The cell theory, and the metaphor of the cell state in particular, forced biologists to consider the essentially philosophical question, “Am I a One or a Many?” Virchow’s response was that the philosopher’s “I” is the result of the biologist’s “We” (Virchow [1859] 1958, 139). But the debate that ensued regarding whether humans and other animals are to be construed as single organisms or colonies of cells required biologists to tackle other fundamental and essentially philosophical questions regarding the definitions of a colony and individual. Arriving at the correct conception of the organic individual has proven to be a perplexing task. Is it the cell? Is it a multicellular organism in which the cells are obligately interdependent upon one another? Can a community of organisms – a “super-organism” – count as an individual? Can a species? Can they all count as different levels of individual? These are questions which continue to attract the attention of philosophers and biologists, especially those concerned with the “units of selection” problem.4 Answering these questions involves grappling with the question of the degree of autonomy each level or unit might be said to possess. Ultimately, beginning in the first decades of the twentieth century, the metaphor of the cell as an autonomous citizen within a larger social body lost its allure. At this time biochemical and physiological investigations began to replace morphological and evolutionary considerations of organisms and cells. As biochemistry matured as a professional discipline, another metaphor came to dominate, one more suited for the particular types of questions being pursued by the new breed of investigators, so that today one more commonly hears the cell described as a “chemical factory.” 2. Virchow, Haeckel, Spencer, and social theories of the organism Virchow introduced the metaphor of the cell state in a series of papers beginning in the 1850s, in a move to incorporate the cell theory into the study of disease, producing what he called “cellular pathology” (cf. Virchow 1855). Haeckel adapted the metaphor to evolutionary theory by making it a central feature of his theories of morphology, phylogeny, and embryology. For Haeckel evolution is the history of the development of progressively more complicated levels of individuality, starting with single-celled organisms to multicellular ones with specialized organs via the division 3

All translations are my own unless otherwise specified. For a philosophical study, see Wilson 1999; for biological studies, see Buss 1987, Maynard Smith et al. 1995, and Gould 2002, especially chap. 8. On the question of where to draw the line between a colony of organisms and an organism proper, the modern evolutionary biologist John Tyler Bonner writes that “the answer seems to be that there is no sharp division line when a group of cell individuals merge to form a true multicellular individual; there is a continuum between the two extremes” (Bonner 1962, 121). Herbert Spencer expressed a similar opinion in 1865, stating that if one takes the idea of evolution seriously, it is to be expected that there will be difficulties in discerning where one level of individuality blends into another (see Spencer 1865, 1:204). 4

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of physiological labor, right up to the emergence of complicated human societies and states (cf. Haeckel 1866). The reputations and influence of Virchow and Haeckel ensured that their perspective of higher animals and plants as social aggregates of cells received widespread attention and eventual acceptance. Implicit in the cell theory from its inception, in the writings of Schleiden and Schwann for instance, is the idea that higher plants and animals are associations of cells, and given the almost irresistible pull to consider cells as elementary living beings, the bodies of “higher” organisms become consequently colonies of such elementary organisms. If one could not resist the temptation to analogize with human affairs, the plant or animal body rather easily became a “society” of cells. The English philosopher Herbert Spencer (1820–1903) had also independently recognized the analogy between a human society and a multicellular organism early in the 1850s, and expressed it through his metaphor of the “Social Organism” (cf. Spencer [1860] 1969), a British equivalent of the German Zellenstaat.5 Like Haeckel, Spencer emphasized the existence of a hierarchy of different levels of organic individuality from single-celled organisms, to colonies, multicellular tissue-forming animals, right up to animal and human societies. The analogy of the “social organism” was somewhat ambiguous in meaning, and could be used to do work in either direction, allowing inferences to be drawn from features of human societies to features of multicellular animals or the reverse.6 The political implications of the cell state metaphor were highlighted by Haeckel who distinguished the republican nature of plants (Zellenrepublik) from the hierarchical arrangement of animals (Zellenmonarchie) (see Haeckel 1875, 36; 1878, 16–17; 1905, 431; 1923, 157, 179). The distinction rested upon the possession of a centralized nervous system in higher animals, which meant that many of the cells in animal tissues and organs are subordinated to the body as a whole, and in the “higher” vertebrates physiological function is controlled to a large degree by the brain. 3. Reaction to the cell state theory 3.1. The British context By the latter half of the nineteenth century the theory of the cell state had caught on among a wide range of European and North American researchers. But because of

5 The following is an illustrative example of Spencer’s use of the analogy: “Hence we are warranted in considering the body as a commonwealth of monads, each of which has independent powers of life, growth, and reproduction; each of which unites with a number of others to perform some function needful for supporting itself and all the rest; and each of which absorbs its share of nutriment from the blood. And when thus regarded, the analogy between an individual being and a human society, in which each man, whilst helping to subserve some public want, absorbs a portion of the circulating stock of commodities brought to his door, is palpable enough” (Spencer [1850] 1868, 493). 6 For more on Spencer’s theory of the social organism, see Hilts 1994 and Elwick 2003.

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its ambiguous nature and its ready applicability to political issues, the idea of the cell state was not always handled equivalently by writers of different nations. There are, for instance, some notable differences in how the metaphor was expressed by Englishspeaking writers in contrast to their German counterparts. In Britain the metaphor appears to have played a different political and social role, likely because the political and social contexts in Britain were rather different from those in Germany. Britain, for instance, was already a politically unified nation with a well established national identity in which people (at least the professional male naturalists who would have employed the metaphor in their writing) enjoyed a comparatively large degree of social and political freedom. And, as Paul Weindling has noted, there were different traditions of social values held by scientists in the two nations. Weindling (1989a, 28) states, for instance, that while German Darwinists tended to idealize the state, their British counterparts showed a greater commitment to liberal political economic theory and utilitarian ideals. Nyhart (1996, 15) also remarks that no leading British naturalist of the 1840s or 50s used the cell state metaphor or similar politically charged language in their professional work. By contrast, she notes, the analogy of the physiological division of labor was widely used by figures such as William Benjamin Carpenter (1813–85), Charles Darwin (1809–82), and Spencer. As Camille Limoges (1994) has shown, the division of labor principle made its way from Adam Smith’s work on political economy to biology via the invertebrate zoologist Henri Milne-Edwards (1800–85). As Nyhart (1996, 16) suggests, the division of labor principle, being a part of liberal political economy, did not have the same taint of radical politics as did the cell state metaphor and so was more comfortably taken up by British naturalists who were striving to achieve greater respectability and state support for their growing disciplines. T. H. Huxley (1825–95), for one, approached the metaphors of the “cell state” and the “social organism” with caution. This is not surprising, given his criticism of the German cell theory and his own novel attempts to define the biological individual in terms of a complete life cycle rather than in morphological terms (see Richmond 2000). In his 1853 review of the cell theory Huxley had argued that rather than being the cause of biological organization, cells are the result of a pre-existent organization lying in the molecular forces dispersed throughout the living substance of plants and animals. The conception of an organism promoted by the Schleiden-Schwann cell theory, Huxley quipped, is that of a “beehive,” and for this he substituted his own memorable image, whereby he compared the cells of a plant or animal body to “shells scattered in orderly lines along the sea-beach,” which only indicate “where the vital tides have been, and how they have acted” (Huxley 1853, 277). Huxley’s criticism of the idea that cells are autonomous living units with priority over the whole organism would later prove very popular with critics of the cell theory at the end of the nineteenth century. Huxley also discussed Spencer’s analogy of “the social organism” in an essay of 1871, where he wrote: “It appears to me that this feature constitutes the difference between the social and the physiological organism. Among the higher physiological organisms, there is none which is developed by the conjunction of a number of primitively

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independent existences into a complex whole” (Huxley [1871] 1968, 274). Huxley’s objection amounts to the observation that unlike human states and societies, none of the higher animals or plants results from the aggregation of previously autonomous and freeliving cells or multicellular organisms.7 As Marsha Richmond has argued, this stems from Huxley’s opposition to what he saw as a preformationist theory of development cast in the guise of cell theory. The epigenetic perspective favored by Huxley would not consider the development of a higher organism as the mere aggregation of previously complete and autonomous cell units. Huxley’s criticism did not, however, prevent other British biologists from using the metaphor of the cell state in their descriptions of plants and animals. George J. Allman (1812–98), for instance, in his 1879 presidential address to the British Association for the Advancement of Science proclaimed: “The whole complex organism is a society of cells, in which every individual cell possesses an independence, an autonomy, not at once so obvious as in the blood-cells, but not the less real” (Allman [1879] 1970, 241– 242). Allman went on to describe how these cells at the same time have subordinated a portion of their autonomy to the whole, and how the diversity of cell types has arisen through the division of physiological labor. The metaphor of the physiological division of labor was a perfect match for the metaphor of the cell state (although logically independent of it), since the various cell types could be readily compared to the classes of skilled workers and professions in a modern state. It was an important aspect in the presentation of physiology by the influential Cambridge zoologist Sir Michael Foster (1836–1907). Foster’s A Text Book of Physiology first appeared in 1877 and went through six editions and part of a seventh. It served as an important conduit for the evolutionary approach in physiology in England (see Geison 1978, 336). In it Foster made the quite striking declaration: “The higher animals, we learn from morphological studies, may be regarded as groups of amoebae peculiarly associated together” (Foster [1877] 1880, 4).8 According to 7 There are examples of a multicellular organism being formed by the aggregation of previously independent and free-living single-celled organisms. These are found among the cellular slime molds (e.g. Dictyostelium), the myxobacteria or “slime bacteria,” and finally a form of ciliate protozoan (see Bonner 1993, 49–54). Neither of the last two examples would have been known to Huxley or Spencer since they were not observed until early in the twentieth century (in the case of the myxobacteria) and even more recently in the case of the ciliates. The cellular slime molds were discovered by Oskar Brefeld (1839–1925) and described by him in 1869, but Huxley was correct that the formation of a multicellular organism by aggregation of previously independent organisms is not found among any of the “higher” animals. There are, however, examples among the marine invertebrates in which colonial organisms do at times dissolve into multiple autonomous parts, which are capable of living, for a time, independent lives. Such are the colonial Radiolaria (single-celled plankton), the Siphonophora, and the colonial flagellate Magosphaera planula (discovered by Haeckel in 1869). Sponges too are colonial organisms which can be forcibly separated into individual amoeboid organisms by being squeezed through a fine mesh, and after a time the individual amoebae will reassemble themselves into the original colonial form. Many biologists, such as Haeckel, Huxley, and others, were led to theorize about the problem of organic individuality as a result of their study of marine invertebrate organisms (see Nyhart 1996). 8 I have only had access to the third and fifth editions, though quotations from and descriptions of the first edition in (Geison 1978, 217) indicate that the relevant passages on the human as a collection of amoebae were

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Foster’s presentation of physiology, the various types of tissues and organs are the result of specialization following from the division of physiological labor among those cells that have found themselves co-habitating in originally loosely organized collectives over great expanses of evolutionary time. Like many of his time, Foster regarded the amoeba as a mere speck of living protoplasm and the simplest example of what was to be understood by the concept of a cell.9 Foster’s conception of the higher animal organism as a social arrangement of protozoan-like cells was echoed by the French psychologist Alfred Binet (1857–1911), who wrote in his book on the psychic life of micro-organisms: We shall not regard it as strange, perhaps, to find so complete a psychology in the history of the lower organisms, when we call to mind that, agreeably to the ideas of evolution now accepted, a higher animal is nothing more than a colony of protozoans. Every one of the cells composing such an animal, has retained its primitive properties, giving them a higher degree of perfection by division of labor and by selection. (Binet [1888] 1910, vii)

While few others would go quite so far as to describe humans and other animals as colonies of protozoans, the thesis that the Metazoa had evolved from a colony of protozoans or Protista (to use Haeckel’s term) found wide acceptance in the latter half of the nineteenth century, at least as a viable working hypothesis. 3.2. The German context The integration of cell theory with evolution begun by Haeckel was further elaborated by one of his students, the embryologist Wilhelm Roux (1850–1924). Roux would, of course, become well known as the founder of the experimental approach in developmental biology, the program he called Entwicklungsmechanik. But prior to this, in 1881, he published Der Kampf der Theile im Organismus (The Struggle of the Parts in the Organism) (Roux 1881). His object was to account for what he called the functionelle Anpassung (functional adaptation) of organs and tissues via a Darwinian competition for nutrition and space among the various cells (as well as organs, tissues, and molecules) within an organism. By means of a competition within the organism for the T¨uchtigsten (fittest) cells, Roux argued, a gradual improvement in function and morphology would result, as the organism would come to consist of better adapted cell-lines (Roux 1881). This would provide an entirely mechanistic explanation for the Zweckm¨assigkeit (purposiveness or adaptedness) of the internal composition of organisms, a feature which Roux believed had been left unaccounted for by Darwin there from the first. Notably, however, the sentence describing higher animals as groups of amoebae was dropped in the fifth edition of 1888 and those to follow. 9 On how the ameoba became emblematic of the cell concept in the latter half of the nineteenth century, see Reynolds 2004.

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and Wallace.10 Though Roux did not explicitly mention the concept of the Zellstaat (cell state), its influence on his conceptualization of the problem can be discerned fairly easily. For instance, in response to the perceived objection that an organism could not continue to exist should its parts be at odds with one another, he asked, “Can the state not persist, if its citizens are everywhere vying with one another and the most capable succeed in having a more general influence on events?” (Roux 1881, 65). Richard Altmann (1852–1900) was one of the most notable proponents of the idea that cells are themselves derived from colonies of more elementary organisms. Altmann explored this idea in his book Die Elementarorganismen und ihre Beziehungen zu den Zellen (cf. Altmann 1890). If the cell is – as Br¨ucke said – an organism, Altmann asked, then what vital units or smaller organisms is it composed of? Altmann proposed that the small granules visible in the protoplasm of cells are really the elementary organisms, and he proposed to call these “bioblasts.” The cell, under this interpretation, is a colony of such bioblasts. In effect the autonomy of the cell – as the basic unit of vital organization – was being called into question.11 As it turned out, some of Altmann’s bioblasts, (e.g. mitochondria) are now recognized to be priorly independent bacteria which at some point in evolutionary history took up a symbiotic existence within a larger bacterial host.12 Proposals of this kind were made in order to account for the properties of protoplasm, the origin of cytoplasmic organelles (e.g. plant chloroplasts, mitochondria, centrosomes), the nucleus, and, it was suggested in the 1890s, even the chromosomes may be colonies of more elementary organisms which had lost their original autonomy and independence through symbiotic union.13 As the focus of attention at the end of the nineteenth century began to concentrate increasingly on the cell nucleus and its role in the problem of heredity, biologists began to apply the idea of competition to the internal components of the cell itself. This became a major theme of August Weismann’s (1834– 1919) theoretical writings on the mechanism of heredity (see for instance Weismann 1892).14 Like Altmann and many others, Weismann proposed that the cell is not the

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In later editions of Nat¨urliche Sch¨opfungsgeschichte Haeckel would refer to Roux’s thesis as the doctrine of “cellular selection” (see for instance Haeckel 1898, 255–57). August Weismann referred to Roux’s theory of the “struggle of parts” as “histonal or tissue selection” (see “Intra-selection or selection among tissues” in Weismann 1904, 1:240–252). For a more recent development of the idea of intracellular competition, see Buss 1987. 11 “The cells are not the elementary organisms, rather they are colonies of elementary organisms with peculiar laws of colonisation” (Altmann 1890, 8). 12 The cells of eukaryotic organisms, like ourselves, are the result of this merger between two (and possibly more) early prokaryotes (see Sapp 1994 for the history of the endo-symbiotic theory of eukaryotic origins). 13 The thesis that the nucleus and the chromosomes are similarly constructed was put forth by the Japanese biologist Shˆosaburˆo Watas´e (1862–1929) (see Sapp 1994). 14 As Hall 1969 documented, from the middle to the close of the nineteenth century a menagerie of subvisible living particles was postulated in the attempt to explain the properties of living protoplasm, thus making of protoplasm itself a colony of more fundamental living units. These included Spencer’s “physiological units,” Darwin’s “gemmules,” Haeckel’s and Louis Elsberg’s “plastidules,” Karl von N¨ageli’s “micellae,” Richard Altmann’s “bioblasts,” Weismann’s “biophors,” Hugo De Vries’s “pangens,” Oscar Hertwig’s “idioblasts,” and Verworn’s and Eduard Pfl¨uger’s “biogens.”

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ultimate vital unit. This distinction he assigned to a complex molecular group he called the “Biophor,” which in turn aggregated to form increasingly complex levels of organization, the determinants, ids, and so on up to the cell itself, and ultimately larger multicellular organisms as a whole. 3.3. The cell in developmental and embryological debates Throughout the 1890s the cell theory came under frequent criticism, notably from those working in the field of embryology. One such critic was the American Charles Otis Whitman (1842–1910), the first director of the Marine Biological Laboratory at Woods Hole, Massachusetts. Whitman was originally an enthusiastic supporter of both the cell theory and the theory of the cell state. In an address of 1890, for example, he remarked that naturalists were very familiar with the fact that the living organism is a “commonwealth of cells,” wherein the division of labor has effected a great deal of specialization and interdependence of the constituent cells. Whitman extended the analogy further, writing that, “On the same grounds that the sociologist affirms that a society is an organism, the biologist declares that an organism is a society” (Whitman 1890; quoted in Sapp 1994, 220–21 n. 9).15 But Whitman later came to have doubts about the cell theory as an explanation of animal development. In his paper, “The Inadequacy of the Cell-Theory of Development,” Whitman spoke out against what he called the “cell-standpoint” and in favor of the “organism-standpoint” (Whitman 1893, 639, 642). Drawing upon evidence from studies of comparative embryology he declared “that the formation of the embryo is not controlled by the form of [cell] cleavage. The plastic forces heed no cell-boundaries, but mould the germ-mass regardless of the way it is cut up into cells” (ibid., 644). Growth and differentiation can occur without the formation of new cells, he argued, as the existence of internally complex single-celled protists like Paramecium and other ciliates shows. He compared the concept of a cell to a ghost that haunts the researcher’s observations. “We are so captured with the personality of the cell that we habitually draw a boundaryline around it, and question the testimony of our microscopes when we fail to find such an indication of isolation” (ibid., 645).16 On this note Whitman quoted at length from the German botanist Julius Sachs (1832–97), whose criticism of the cell theory had great influence at the end of the century. Sachs had written: To many, the cell is always an independent living being, which sometimes exists for itself alone, and sometimes “becomes joined with” others – millions of its like, in order to form a cell-colony, or, as H¨ackel has named it for the plant particularly, a cell-republic. To others 15 Sapp lists the title of Whitman’s talk as “Socialization and Organization, Companion Principles of All Progress. The Most Important Need of American Biology.” It should read, “Specialization and Organization, . . .” 16 Note what a nice example of the theory-ladeness of observation this is.

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again, to whom the author of this book also belongs, cell-formation is a phenomenon very general, it is true, in organic life, but still only of secondary significance; at all events, it is merely one of the numerous expressions of the formative forces which reside in all matter, in the highest degree, however, in organic substance. (Ibid., 647; quoted from Sachs 1887, 73)

Moreover, the principle of the division of physiological labor, Whitman noted, is an anthropomorphism too readily applied, by some (like his earlier self), to every level of biological organization. “The higher organism is regarded as a colony of cells; the cell as a colony of simpler units, nucleus, centrosome, and so on; the nucleus as a colony of chromosomes; the chromosome, according to Weismann’s terminology, as a colony of ‘ids’; the ‘id’ as a colony of ‘determinants’; the ‘determinant’ as a colony of ‘biophores,’ and the ‘biophore’ as a colony of molecules” (ibid., 649). Having said this, it comes as a bit of a surprise to see that, near the end of the paper, Whitman proposes that the real secret to the “formative processes” of organization, growth, and development must ultimately be found, not in cell-formation, but in the existence of certain hypothetical vital particles or elements which Whitman proposed to call “idiosomes” (ibid., 657).17 Once again we see the autonomy of the cell as the true elementary organism being challenged. Whitman’s essay ends with an approving quotation of T. H. Huxley’s evocative sea-shell imagery, making the point that cells are the result, not the cause, of biological organization. Whitman’s critique was shortly followed by a debate over the adequacy of the cell theory carried out in the pages of the Quarterly Journal of Microscopical Science during the years 1895–96, by the Cambridge embryologist Adam Sedgwick (1854–1918) and the Oxford zoologist Gilbert Bourne (1861–1933) (cf. Sedgwick 1895, 1896; Bourne 1896).18 On the basis of his research into the ontogeny of Peripatus (common name “velvet worm,” phylum Onychophora), Sedgwick challenged the theses that all higher animals are aggregates of independent cells, and that the multicellular Metazoa had evolved from a colony of single-celled protozoans. In the case of the developing Peripatus, Sedgwick argued, it is closer to the truth to say that the organism develops via a multinucleated phase in which there are not several independent cells, but one continuous mass of protoplasm (dubbed by Haeckel a syncytium) with multiple nuclei. Around the several nuclei, cell membranes eventually form, but never to the extent that the resulting cells are isolated and independent units, since they remain in continuous contact with one another by various protoplasmic strands. Sedgwick also appealed to empirical evidence from the development of some animals, where even though the cellular organization is clear, connecting strands of protoplasm between adjacent cells 17 For an interesting contemporary discussion of Whitman’s (and N¨ageli’s and Weismann’s) “idioplasm” theory, see Graf 1897. 18 Sedgwick was the grandnephew of the eminent geologist of the same name. Bourne was Linacre Professor of Zoology at Oxford (1906–21) and a skilled oarsman. His text on rowing is considered a classic and is still in print.

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still remain. Cells in the process of development and differentiation are not, therefore, as distinct and isolated as some formulations of the cell theory made them out to be. These remarks were not entirely original with Sedgwick. The Austrian-American anatomist Carl Heitzmann (1836–96), for one, had argued earlier that the entire plant or animal body constituted a continuous syncytium, so that according to Heitzmann “there is no such thing as an isolated, individual cell in the tissues, as all cells prove to be joined throughout the organism, thus rendering the body in toto an individual” (Heitzmann 1883, 56).19 From this Heitzmann drew the striking conclusion that “Man is a complex amoeba” (ibid., 36). Sedgwick charged that the idea of the cell as a distinct and autonomous entity had assumed the role of a fetish which was distorting researchers’ objective observations of anatomical reality. In short, they were seeing distinct independent cells because that’s what the cell theory was telling them they should see. Consequently the hypothesis that the Metazoa are evolved colonies of separate independent cells must also be subject to serious doubt.20 In essence Sedgwick was criticizing both the cell theory and Haeckel’s recapitulation thesis, which stated that an adult animal is assembled from distinct cells (via the process of repeated cell cleavage starting with an original fertilized egg cell), and that the cause or explanation of this ontogenetic process is the previous evolution of multicellular organisms from colonies of single-celled protists. Bourne began his defense of the cell theory by stating that he was “unable to find, in the writings of any reputable biologist, any statement to the effect that an organism is composed of independent and isolated units” (Bourne 1896, 144).21 He mentioned that he found, however, that students are prone to interpret the words of respected biologists in this way. He gave examples from Augustus D. Waller’s (1856– 1922) textbook of human physiology, where the author writes, “the highest form of living matter is the human body, which is literally a ‘nation’ of cells derived from a single cell called the ovum, living together, but dividing the work” and that “the organism is a community; its individuals are cells” (Waller [1891] 1893, 2). Bourne then admitted that this is a “too free use of illustrative language” and that “in every illustration there lurks a fallacy,” but rejoined that the misdirection is unintended. He then went on to defend Haeckel from the charge of teaching that animals are colonies of independent and isolated cells by noting that going back to his first great work

19

This volume contains reprints of several of his earlier papers on protoplasm and cell theory. For further discussion of the Bourne-Sedgwick and other late nineteenth-century debates about protozoan and metazoan cell comparisons, see Richmond 1989. See also Hughes 1959, 133–37, where the debate is considered in the light of more recent developments in cytology. 21 Bourne did not mention Foster, who as we have seen described higher animals as large goups of amoebae. He might also have mentioned Darwin, surely a reputable biologist, who in discussing the hypothetical gemmules of his pangenesis theory wrote: “We cannot fathom the marvelous complexity of an organic being; but on the hypothesis here advanced this complexity is much increased. Each living creature must be looked at as a microcosm – a little universe, formed of a host of self-propagating organisms, inconceivably minute and as numerous as the stars in heaven” (Darwin 1868, 204). 20

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of 1866, the Generelle Morphologie, Haeckel explicitly stated that while plants are cell republics, in animals the cells are much less independent and are subordinated in their interests to the higher order individual that is the animal body (Bourne 1896, 145).22 Bourne gave what he called the popular form of “the cell theory of development” in the following summary: “The multicellular organism is a colony, consisting of an aggregation of separate elementary parts, viz. cells. The cells are independent life units, and the organism subsists in its parts and in the harmonious interaction of those parts” (ibid., 162–63). He then admitted that the evidence of protoplasmic connections between the cells of plants and various animals shows that this summary is not generally true. But neither, he retorted, is the absolute contrary, viz. that “the metazoon is a continuous mass of nucleated vascular protoplasm, subsisting in the unity of its mass” (ibid., 163). He then distinguished what he took to be the essential propositions of the cell theory. These were: “The multicellular organism is an aggregate of elementary parts, viz. cells. The elementary parts are independent life units. The harmonious interaction of the independent life units constitutes the organism. Therefore the multicellular organism is a colony (cell republic according to H¨ackel)” (ibid.).23 Of these four he wished to retain only the first proposition unaltered. The key issue of the debate between himself and Sedgwick, as Bourne saw it, hinged upon the question whether the elementary parts of an organism (the cells) could be justifiably considered independent life units. Bourne himself eventually conceded that cells were only independent in posse, since in many cases they are so subordinated to the rest of the organism, on account of the differentiation and specialization which they have undergone, as to have lost their potential for independent activity when separated from the whole (ibid., 165). In a line reminiscent of the quotation cited earlier from Julius Sachs, Bourne wrote: I have finally been led to the conclusion . . . that the cell concept is a valuable expression of our experience of organic life, both morphologically and physiologically, but that in higher organisms cells are . . . not independent life units . . . but a phenomenon so general as to be of the highest significance; they are the constant and definite expression of the formative forces which reside in so high a degree in organic matter. (Ibid., 171)

In the last decade of the nineteenth century the cell state theory still had key proponents among German zoologists such as Oscar Hertwig (1849–1922) and Max Verworn (1863–1921). Both were former students of Haeckel and defended the stance that a general understanding of life processes (Allgemeine Physiologie) would have to be

22

Bourne is correct that Haeckel does mention this distinction in the greater integration of animal cells as compared to the looser organization in plants, but as mentioned earlier he does not at this time invoke the metaphor of a Zellenmonarchie to do so. Sedgwick is equally correct that in the Generelle Morphologie Haeckel described both plants and animals as states or societies of cells. 23 This list corresponds more or less closely to John Baker’s study of the cell theory in Baker 1948–1952.

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a cell physiology (cf. Hertwig 1893 and Verworn 1895).24 As evidence accumulated, however, that the cells of plants and animals are frequently not physically isolated from one another, but are connected through protoplasmic bridges (plasmodesmata), the metaphor of the cell state was used with greater caution, and restrictions on the analogy between the metazoan cell and the independent and autonomous citizen of the human polity were frequently noted. This is well illustrated in E. B. Wilson’s (1856–1939) classic text on cytology, The Cell in Development and Inheritance ([1896] 1st ed.; [1900] 2nd ed.; 1928, 3rd ed.). Wilson attributed to Schwann the opinion that the whole multicellular organism is no more than the sum of its cell parts, then wrote: This conclusion, afterward elaborated by Virchow and Haeckel to the theory of the ‘cell-state,’ took a very strong hold on the minds of biological investigators, and is even now widely accepted. It is, however, becoming more and more clearly apparent that this conception expresses only a part of the truth, and that Schwann went too far in denying the influence of the totality of the organism upon the local activities of the cells. (Wilson [1896] 1900, 58)

Wilson agreed that with regard to its structure and origin the tissue-cell has the same morphological value as a single-celled plant or animal. “Physiologically, however,” he added, “the tissue-cell can only in a limited sense be regarded as an independent unit; for its autonomy is merged in a greater or less degree into the general life of the organism” (ibid.). This had been admitted by Haeckel himself as early as 1866 in his Generelle Morphologie, and it was also the opinion finally adopted by Bourne in his defense of “the cell theory.” As for the status of the cell in the process of development, Wilson maintained that “the cell is no more than a particular area of the germinal substance” consisting of a certain amount of cytoplasm and “idioplasm” within a nucleus, whose character is “primarily a manifestation of the general formative energy acting at a particular point under given conditions” (ibid., 427). However, Wilson noted, “once such a circumscribed area has been established, it may . . . emancipate itself in a greater or less degree from the remainder of the mass” (ibid.; emphasis added). Despite expressing some reservations about the idea of the cell state, in the third edition Wilson wrote of the cell state theory, “Its value as a means of biological analysis needs no other demonstration than the immense advances that it made possible” (Wilson 1928, 102). Among these advances Wilson credited “a revolution in the prevailing views of vital action” and a great impetus to the fields of physiology, pathology, and morphology (ibid., 5). Despite requiring some qualification, “especially as applied to the phenomena of growth,” Wilson wrote, “the conviction of its essential truth has survived all criticism, and as measured by its continued fruitfulness, it still stands among the most important generalizations of modern biology” (ibid.). In the 24 Both men also advocated the analogy of the cell state as a legitimate and informative concept in social and political studies (see Weindling 1991 for details).

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section titled “The cell in relation to the multicellular body,” Wilson addressed the criticisms of the cell state theory, noting principally the loss of physiological autonomy of tissue-cells to the organism as a whole. But this, he rejoined, did not undermine what he described as “our fundamental conception of the cell-state” (ibid., 103). The evidence he drew upon for retaining this conception was essentially twofold: (1) the fact that in some cases aggregating cells do form a complete organism (Wilson noted recent experiments showing that sponges forced to dissociate into individual amoeboid cells can reassemble themselves into a complete multicellular whole),25 and (2) that cells can be damaged or transplanted (as recent grafting experiments showed) to new locations or even to organisms of an entirely different species, without affecting the general equilibrium of the body in question (Wilson 1928, 1030–32). The thesis of cell autonomy and the theory of the cell state continued to be challenged into the early twentieth century. Clifford Dobell (1886–1949), a protistologist and student of Adam Sedgwick, further criticized advocates of the cell theory in 1911 for the common practice of referring to organisms of the protist kingdom as primitive single-celled organisms and purporting them to be homologous to the tissue-cells of higher plants and animals. Dobell insisted that the Protista be designated “a-cellular” rather than “uni-cellular,” for in his opinion they were better viewed as homologous to an entire animal or plant, not as mere sub-units of a cell-state or colony (cf. Dobell 1911).26 Dobell was reacting against the speculative phylogenizing that had been inspired by Haeckel’s example, and he insisted that the Protista were of biological significance in their own right (on account of their peculiar non-cellular mode of organization), not just as potential clues to metazoan ancestry. On the question of the evolutionary origins of the Metaphyta and Metazoa, Dobell preferred the hypothesis expounded by Sedgwick (and presaged by T. H. Huxley in his review of the cell theory), that rather than having evolved from a colony of social amoeba-like protists, the common ancestor was a multinucleated ciliate, within whose body internal membranes had formed around the various nuclei. Dobell included in his critique the criticisms of earlier writers such as Huxley, Sachs, Whitman, and Sedgwick.27 In the very next year (1912) Julian S. Huxley (1887–1975) published a short book on the question of The Individual in the Animal Kingdom, in which he wrote that the cells have preserved a very large amount of independence, and indeed do most forcibly present themselves to the mind as bands of beings like ourselves that have voluntarily enlisted under some beneficent tyrant of a general. That analogy, between cells and men, body and state, has been too often and too far pressed; its incompleteness is at once 25

These experiments were carried out by the American zoologist H. V. Wilson (1863–1939), of no relation to E. B. Wilson (see Wilson 1907). 26 For analysis of Dobell’s arguments, see Richmond 1989 and Corliss 1989. 27 E. B. Wilson remarked of these criticisms that they “seem to ignore the probable historical origin of multicellular from unicellular organisms, as well as the fundamental general similarity between the protistan cell and that of the metazo¨on or metaphyte, both in structure and mode of origin” (Wilson 1928, 103, n. 1).

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grasped with the realization that no such general does or can exist for the cell-battalions to obey. (Huxley 1912, 92–93)

He continued to use the analogy, however, throughout the first few decades of the twentieth century, though with similar qualifying remarks (cf. Huxley 1922, 3:684). Huxley’s colleague J. A. Thomson (1861–1933), who had studied for a time with Haeckel in Germany, provides another notable display of how the theory of the cell state continued to receive a suitably qualified endorsement: Every animal, Virchow said, appears as a sum of vital units. Not that we are to think of an ordinary animal as a colony of cells, as a mob is a collection of angry men, or even as a battalion is a co-ordination of disciplined soldiers. It is nearer the truth to think of the fertilised egg-cell . . . dividing and re-dividing into cells so that the unified business of life may be more effectively carried on by division of labour. As one of the greatest of botanists said: It is not that the cells form the plant; it is rather that the plant makes the cells. (Thomson 1922, 2:305–306)

The botanist referred to here is Anton de Bary (1831–88), who criticized what he called the “hegemony of the cell.” The line so often attributed to de Bary, “Die Pflanze bildet Zellen, nicht die Zelle bildet Pflanzen,” became a popular slogan among later critics of the cell theory.28 4. Evidence for cell autonomy from tissue cultures Julian Huxley continued his use of the cell state theory in a massive collaborative effort with the author H. G. Wells (1866–1946) and his biologist son, G. P. Wells (1901–85). The trio published their popular book The Science of Life in 1931. In this layperson’s introduction to modern biology the cell state metaphor plays an important role. But now its appropriateness had been buttressed by recent developments in tissue culture techniques, which revealed that many animal cells are in fact capable of leading independent and isolated lives, so long as they are provided a suitable environment. As the authors wrote, “We may compare the body to a community, and the cells to the individuals of which this vast organized population is composed. It is very important to realize that this is not merely allegorical comparison. It is a statement of proven fact, for – we resort to the stress of italics – single cells can be isolated from the rest of the body, and kept alive” (Wells et al. 1934, 29; emphasis in the original). The authors cite (ibid., 30) the work of Thomas S. P. Strangeways (1866–1926), of the University of Cambridge, as the source of their discussion, though the beginning 28 This oft-quoted line appears actually to be a rephrasing of de Bary’s original, in which he laments the “Hegemonie der Zelle,” established by Schleiden, which has led to the popular conviction that “die Zelle die Pflanze und nicht umgekehrt die Pflanze Zellen bilde” (see de Bary 1879, 222).

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of tissue culture is typically credited to Ross G. Harrison (1870–1959) who observed in 1907 the growth of nerve cells he had removed from spinal cord tissue in an artificially prepared medium.29 Wilhelm Roux has also been credited with successfully maintaining cells from a chicken embryo for several days in a dish of saline solution in 1885 (though Jane M. Oppenheimer expresses doubt that it could have been so long [Oppenheimer 1967, 100–101]). Strangeway’s recent improvements of cell isolation techniques evidently encouraged Huxley and his co-authors to describe the human body as a “cell community”; and yet they still did so with some qualification. “Naturally,” they wrote, “when they are parts of a living body the cells are disciplined, they do not wander about where they like, growing actively and reproducing themselves, as the cells in a culture do. An organ such as the brain or liver is like the City during working hours, a tissue-culture is like Regent’s Park on a Bank Holiday, a spectacle of rather futile freedom” (Wells et al. 1934, 31). They noted too the important differences between a cell in a higher animal and a naturally isolated amoeba cell. The animal cell they compared to a “trim, bowler-hatted clerk, trotting with umbrella and attach´e case to his appointed desk in the city” and the amoeba to a “solitary savage on a desert island” (ibid., 169). The savage amoeba is a “jack-of-all-trades” capable of carrying out all the functions necessary for an independent life removed from civilized society, while the animal cell removed from its tissue and maintained in a culture dish must be pampered and carefully looked after if it is to survive on its own. Its greater specialization for certain of life’s tasks has made it more dependent on the rest of the cellular society to which it belongs, in analogy with the plight of the citizen of a modern technological and bureaucratic society who has lost the basic skills necessary for survival in a state of nature. The techniques of cell culture provided then further credence to the thesis of cell autonomy by showing that even from a physiological perspective, under the right conditions, individual cells taken from a highly integrated tissue or organ are capable of functioning as a living unit, and resemble more “primitive” protozoan organisms in doing so. It is interesting to note in this respect that Theodor Schwann had from the beginning defended the legitimacy of the cell theory by writing that “the failure of growth in the case of any particular cell, when separated from an organized body, is as slight an objection to this theory, as it is an objection against the independent vitality of a bee, that it cannot continue long in existence after being separated from its swarm” (Schwann 1847, 192–93). It was this line evidently that provoked T. H. Huxley to complain that according to the cell theory of Schleiden and Schwann an organism is a “beehive, its actions and forces resulting from the separate but harmonious action of all its parts” (Huxley 1853, 254). Surely the ability of isolated tissue cells to function as independent “organisms” was an extraordinary piece of evidence in favor of the “cell-standpoint.” To witness 29

See Landecker 2002 for a discussion of Harrison’s work in tissue culture and the debate over the autonomy of nerve cells or neurons isolated from the body.

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a cell separated from the tissue of a “higher” animal crawl about in a dish by means of the pseudopodial processes characteristic of the “lower” amoeba, must have been a remarkable thing. And yet, it is important to note that in the same year as The Science of Life appeared (1931), Julian Huxley’s friend and colleague, the Cambridge experimental zoologist James Gray (later Sir) (1891–1975), could still find reason to resist the emphasis of the cell as the primary unit of vital organization and activity. In his influential textbook of experimental cytology, Gray declared that “Nearly every experimental biologist has declined to accept” the view that “a metazo¨on is to be regarded as a colony of cells in which each cell is a fundamental unit of function” (Gray 1931, 2). For Gray, whose objective was not to write a popular work of biology, but rather to put cytology upon firmer chemical-physical foundations, the cell was a merely convenient unit for the study of functional activity. In itself the cellular organization of organisms is only a mechanical necessity to be accounted for by the fact that there are structural and functional limitations (concerning surface area to volume ratio), on how large a single unit of living protoplasm can be. If an organism is to grow beyond these limitations of size, it will naturally break itself up into a compartmentalized or cellular arrangement. The cellular organization of plants and animals was then of secondary importance behind the more essential chemical and physical properties of living protoplasm. “There can be little doubt,” Gray wrote in a tone reminiscent of T. H. Huxley, de Bary, Whitman, and Sedgwick, “that the most natural unit of life is the living organism, and when we find, in some cases, that its constituent cells are united by intercellular processes it is impossible to admit the validity of the cell unit without further enquiry” (ibid., 3–4). It was still open to opponents of the cell standpoint, moreover, to object that the achievements of tissue culture experiments were merely artificial manipulations, and that the fact remained that in the natural order of things the cell was typically subordinated to the organism as a whole. Such was the response of the American zoologist William Emerson Ritter (1856–1944), Director of the Scripps Institution for Biological Research at the University of California, La Jolla (now the Scripps Institute of Oceanography). In his two-volume book The Unity of the Organism, or the Organismal Conception of Life, Ritter offered a sustained critique of the cell theory. Though he admitted that recent research on isolated tissue cultures looked like solid confirmation of the view that cells are “wholly independent elements whose co¨operation explains the organism,” Ritter remained ultimately unconvinced. Such tissues, maintained in vitro for no matter how long a time, he suggested were better described as u¨ berlebende Gewebe (surviving tissues), to emphasize their unnatural circumstance (Ritter 1919, 168). He expressed concerns about the “relative trustworthiness and value of experimental studies of the sort devised by” Harrison, Alexis Carrel (1873–1944) and others, since they dealt with behaviour of cells and tissues under abnormal conditions (ibid., 70). In addition to this he noted that none of the cells in these tissue cultures had successfully organized themselves into “normal” organs. But even if this were eventually accomplished it would prove that “these cells and organs are capable of independent life in an ontogenic

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sense only. It would not prove them so independent in a full sense, that is, in a phylogenic as well as an ontogenic sense” (ibid., 177). It seems Ritter was arguing that, by definition, a normal organ could only be one that had developed under the “morphological plan of the organism.” With the terms so defined it is clear that Ritter could not lose this argument. It is not clear though what ultimate difference it would make if Ritter were correct. What is more important, it seems to me, is that given all the concessions Ritter was willing to make as to the capacity for isolated cells to behave and function as living entities when separated from their normal organismal environment, it becomes clear that the dispute over the thesis of cell autonomy was largely one of emphasis. Both camps conceded the other side’s evidence, but wished to maintain, nevertheless, that the facts emphasized by themselves ought to be considered more important or fundamental.30 Note, for instance, that what Ritter preferred to call “surviving cells,” were, from the perspective of a supporter of the cell-standpoint like E. B. Wilson, “emancipated” cells. This dispute can be seen as part of the general tension between what Garland Allen (1978 and 2005) has called mechanistic and holistic materialism. Ritter was not advocating any kind of Drieschian vitalism. He insisted that biologists must approach their studies from the perspective of the organism as a whole, and that the cells should be regarded as “organs of the organism just as muscles and glands and hearts and eyes and feet are so regarded” (Ritter 1919, 191; emphasis in original). Studies of the cell by means of the methods of biochemistry, Ritter noted, lead one to regard the cell as an “organized laboratory” (ibid.). This metaphor would naturally appeal to an advocate of the “organismal conception” like Ritter since, unlike an elementary organism, a laboratory does not run itself or exist for its own sake, rather it is an instrument used by the total organism for its own ends. And indeed, as biochemical investigations of the cell came increasingly to dominate the attention of cytologists of the early twentieth century, the metaphor of the cell as a chemical factory replaced that of the cell as an elementary organism.31 Concern shifted from the evolutionary history of cells to their mechanical function in the present so much that by the middle of the twentieth century the Cambridge histologist E. N. Willmer (1902–2001) had to make a concerted plea for the relevance of evolutionary considerations for cytology (cf. Willmer 1951).32

30

The plant physiologist Julius Sachs himself said as much when he wrote: “It depends, therefore, entirely upon our mode of consideration, and upon the point of departure of our consideration, whether we regard the cells as independent so-called elementary organisms, or merely as parts of a multi-cellular plant” (Sachs 1887, 77). That said, Sachs considered the second interpretation to be the more correct. See for instance page 431 where he states: “Growth is the primary, and cell-division the secondary and independent phenomenon.” 31 For the eventual supplanting of the elementary organism metaphor by the chemical factory metaphor in the conception of cells, see Reynolds 2005. 32 Tellingly Willmer’s argument for the importance of understanding cell evolution for cytology and cell physiology is the very last essay in the volume.

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Conclusion Within the debates reviewed here three separate but related questions were identified: 1) Are cells independent entities, both morphologically and physiologically speaking? Closely related to this question we saw was the further one regarding whether “higher” plants and animals are arranged according to a cellular or a syncytial organization, and whether the Metaphyta and Metazoa had evolved from colonies of social protists or by the internal formation of cell membranes within a multinucleated ciliate. 2) Are cells the cause of the development of specialized tissues and organs which occurs during ontogeny or are they the effect of a more fundamental organization which is dispersed throughout an original protoplasmic mass, (the fertilized ovum), and which is inherited from parent organisms? That is, do the cells build the organism or the reverse? This is the continuation of the debate between preformationist and epigenetic accounts of development, cast in terms of cell theory.33 3) Are cells themselves elementary or composite? Are they the fundamental and primary units of life or are they “colonies” of more elementary vital units? All three questions constituted a threat to the autonomy and stability of the concept of the cell as an, or perhaps the, elementary vital unit. The cell theory, and in particular the thesis of cell autonomy, came under attack during this period from two separate directions: One, advocates of philosophical holism with their emphasis upon the “organismic standpoint”; and two, the emphasis by biochemists on the cell as a factory or machine for the production of enzymes, proteins, and other chemically important molecules. Critics such as Heitzmann and Sedgwick were essentially denying that cells exist (as discrete autonomous units); theirs was an ontological claim. On the other hand, those like T. H. Huxley, Sachs, de Bary, Ritter, and Gray were not denying that cells exist, but that they provided an adequate unit of analysis for understanding organismic form, function, and development; their dispute with the cell theory was methodological. The disputes were, I have argued, in an important way one of emphasis. Both sides admitted the key bits of evidence marshalled by the opposition, but wished to maintain nonetheless that their own viewpoint was the more general or instructive. They were also in part disputes arising from the choice of language in the sense that they turned on the choice of metaphors used to describe cells. Just as the concept of a “citizen” can only make sense when considered against the background of a “state” or “society,” so by choosing to compare the cell to a citizen, advocates of the cell state theory were inviting the holism-reductionism or holism-individualism debate to be raised. If we refer to the parts as “individuals” or “people” perhaps one may be inclined to agree with Mrs. Thatcher that “There is no society, only people.” But if we’re going to describe cells as “citizens” of an organic state or society then we cannot 33 See Maienschein 1986, 21–26; idem. 1988, 168–175; and Benson 1994 for details regarding the organismal versus cell standpoints and their associations with the modern forms of epigenesis and preformation in late nineteenth and early-twentieth century embryology as advocated by C. O. Whitman, E. B. Wilson, and others.

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overlook the fact that citizens are not entirely independent beings qua citizens, for they acquire particular properties as a result of the influence of the larger organization of which they are a part. To see this one need only ask whether an individual stranded on a desert island could ever become a “citizen,” or be said to remain one for that matter, if she or he cannot vote or participate in other social functions. To those who viewed this choice of language as overly-reductionist, the practice of referring to cells as “elementary organisms” and comparing them to free-living autonomous amoebae, obscured this and suggested that the higher organism – “a cell state” – was being reduced to a mere colony of autonomous cells. In their eyes this overly-reductionist perspective called for a holistic redress. In this sense too the dispute was essentially framed as one of emphasis, in that the terms chosen to define the problem helped to shape the problem itself. If the technique of cell culture ultimately showed that tissue-cells do have the potential for autonomous life outside of the body, that they can be “emancipated” as Wilson put it, from their normal subordination to the body, the phenomenon of induction, whereby cells in a developing embryo become differentiated as a result of their physical contact with neighboring cells, showed the important influence of the individual cell’s interactions with the larger cell community. From an evolutionary perspective, it may be attractive to describe cells as organisms to emphasize the community of descent among all living things and the continuous chains which link all current living beings to an original ancestor or ancestral group. But as many researchers became increasingly preoccupied with the biochemistry of the cell and its nuclear hereditary mechanisms, the idea that higher plants and animals are “states” of amoeba-like elementary organisms ceased to have much relevance or allure. The preference on the part of biochemists to see the cell as a chemical factory, organ, or instrument of the organism as a whole, reflects a different set of interests, questions, and experimental methods. Ultimately, however, these contrasting views of the cell as organism and as a proper component of organisms have both been accommodated within modern biological science. Acknowledgments Support for this research was provided by research grants from Cape Breton University and the Social Sciences and Humanities Research Council of Canada. I would also like to thank the following people for their assistance and/or encouragement: John Tyler Bonner, Lynn Nyhart, Abigail Lustig, Bernie Lightman, Dave MacAulay, and anonymous reviewers for their helpful suggestions. References Allen, Garland. 1978. Life Science in the Twentieth Century. Cambridge History of Science Series. Cambridge: Cambridge University Press.

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