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Tolerance

“Tolerance” never made it into Raymond Williams’ Keywords, a rare mistake: it should have been a tempting subject for his critical sensibility.[1] By the late-eighteenth century, the word often had come to substitute in English for the older “toleration,” meaning forbearance, patience, and indulgence of the opinions of others. Later, physiologists took up its connotation of the endurance of hardship, transferring the concept to the scene of medical investigation: they gauged the tolerance of large doses of drugs and other noxious agents. Early in the twentieth century, microbiologists requisitioned the term.  They used it to signify the host’s survival despite infection with a parasite — in effect, the ability to become a healthy carrier of some microbe. Tolerance soon became a key word in microbiology and animal ecology. According to Australian virologist F. Macfarlane Burnet, the most intriguing aspect of the immune system was its tolerance of its own body, what he called the “self,” and not its mundane mechanisms of resisting foreign agents. One could not know the immune self — the absence of self-antigenicity — without understanding tolerance. Indeed, the sovereign self of an organism was in effect whatever its immune system would tolerate. Thus “tolerance” has been one of those vagrant concepts or metaphors like “self,” “resistance,” and even “immunity” that ambulate gainfully, if awkwardly, through various domains, doing work in political, philosophical, literary, and scientific discourses.[2]

In 1948, after musing for more than a decade on the production of antibodies, or the nature of the vertebrate immune response, Burnet decided that “recognition of ‘self’ from ‘not-self’ is probably the basis of immunology.”[3] But still he wondered how this tolerance of self, or lack of self-antigenicity, could develop. The following year, with protégé Frank Fenner, he speculated that recognition and tolerance of self must occur principally during embryonic life. “If in embryonic life,” they predicted, “expendable cells from a genetically distinct race are implanted and established, no antibody response should develop against the foreign cells when the animal takes on independent existence.”[4] That is, the organism as it formed had the capacity to tolerate foreign elements. A few years later, Peter Medawar and his colleagues managed to induce experimentally this immunological tolerance, to show that embryonic mice became “indifferent” to cells transplanted into them.[5] For their studies of immunological tolerance, Burnet and Medawar secured the 1960 Nobel Prize in Physiology or Medicine.

Gradually, though, there has been a slippage from tolerance to self. Commonly, Burnet is perceived as the advocate of the immune self, which proved an alluring concept. But his fame as the theorist of self devalues his curious speculations on tolerance, a far more supple notion. In effect, “self” has stabilized and locked in “tolerance” and made it a tool of sovereignty, a figment of the Cold-War imaginary. The ramifications of tolerance could render possible a more extensive and ecological, even selfless, self — encompassing the others within, such as the gut microbiome, and could explain those failures of self-recognition, the autoimmune diseases. The immune self has turned tolerance into a stage one goes through, not a life-long negotiation or struggle.

“Tolerance” was a word long familiar to Burnet. He mentioned the term in some articles in the 1930s and in Biological Aspects of Infectious Disease (1940), the founding text of disease ecology. Initially, his usage was conventional, referring to an organism’s tolerance of increasing doses of drugs and to the carrier’s tolerance of germs. Burnet’s Ph.D. supervisor at the University of London, J.C.G. Ledingham, had made a name for himself expatiating on how tolerance of microbes can allow asymptomatic infection in carriers.[6] In the 1930s, Burnet also was reading widely in animal ecology. He must have heard of Victor E. Shelford’s “law of tolerance,” which stated that an organism survived only if environmental conditions remained within a range of tolerance.[7] Charles Elton, whom Burnet read carefully, incorporated the idea of tolerance in his justification of the niche concept.[8] By the late 1940s, tolerance came to infuse Burnet’s immunological speculations. While Burnet thus made efforts to translate ecological thought into immunological theory, the appeal of the immune self seems ultimately to have restricted the conceptual transfer. My sense is that his understanding of immunological tolerance started off ecological, but soon ran into an ontological impasse, getting stuck on notions of the preformed self. Certainly his later interpreters often let a rigid self, or autonomous biological individuality, blind them to the ecology of tolerance. Burnet himself could be equivocal.

In the past twenty years, ecological immunologists have ventured further down the path on which Burnet hesitated. The immune self has become more dynamic, interactive, and encompassing. “The problem centers on tolerance,” Alfred I. Tauber tells us.[9] Rather than posit a self that must be defended, we should consider the communal and relational grounding of tolerance and immunogenicity. According to Janelle S. Ayres and David S. Schneider, “studies of tolerance will provide an improved foundation to describe our interactions with all microbes: pathogenic, commensal and mutualistic.” By tolerance they mean “a change in sensitivity to elicitors.”[10] Scott F. Gilbert, Jan Sapp, and Tauber also argue that proposing such “interactive relationships among species blurs the boundaries of the organism and obscures the notion of essential identity.”[11] Sadly, in these ecological visions, Burnet usually is seen as an enemy, not an ally; as a straw man, not a progenitor; as antigen, not complement.

Obsessed with immunological metaphysics in his last decade, Jacques Derrida distrusted mere tolerance, attributing to it ties to sovereign reason. Tolerance struck him as a “scrutinized hospitality, always under surveillance, parsimonious and protective of its sovereignty.”[12] It represented a conditioned hospitality that the immune system protected against the wholly other. Derrida yearned for a different sort of immune system, one that harbored radical alterity: a commune system, perhaps. Yet rival philosopher Roberto Esposito is more sanguine about tolerance. In Immunitas, he writes: “At the heart of this historical, process-based conception of identity as a system open to the challenges of the outside world, and indeed ultimately formed by them, lies the complex function of immune tolerance.” He continues: “if tolerance is a product of the immune system itself, it means that, far from having a single-response repertoire, that of rejecting other-than-self, it includes the other within itself, not only as its driving force but also as one of its effects.”[13] Through tolerance, one might refigure immunity as ecological community.

The passage from politics and philosophy to microbiology and immunology, and back again, is crowded and bustling. In the twenty-first century, tolerance appears finally to have prevailed in the commotion. Practicing tolerance, anthropologist A. David Napier tells us, makes possible our future. “This is why,” he writes, “we all need to start replacing competition with thoughts of others, with embryology, with tolerance and generosity, even with goodness—why science, in the absence of artful living, will wallow in its own entropy.”[14] How apt, and yet so poignant: an embryonic manifesto for radical tolerance. How Burnetian—perhaps.

 

Warwick Anderson is an Australian Research Council Laureate Fellow and Professor at the University of Sydney. He is the co-author, with Ian R. Mackay, of Intolerant Bodies: A Short History of Autoimmunity (Baltimore: Johns Hopkins, 2014). He has written (mostly with Mackay) on immunological history for Isis, the Journal of the History of Biology, the Journal of Neuroimmunology, and the New England Journal of Medicine. In 1984, he was a medical resident on the Royal Melbourne Hospital’s clinical immunology ward, which Mackay directed.


[1] Raymond Williams, Keywords: A Vocabulary of Culture and Society (London: Fontana, 1975).

[2] Warwick Anderson and Ian R. Mackay, Intolerant Bodies: A Short History of Autoimmunity (Baltimore: Johns Hopkins University Press, 2014); and Warwick Anderson, “Getting ahead of one’s self: the common culture of immunology and philosophy,” Isis 105 (2014): 606-16.

[3] F.M. Burnet, “The basis of allergic diseases,” Medical J. Australia I (1948): 29-35, p. 30.

[4] F.M. Burnet and Frank Fenner, The Production of Antibodies, 2nd ed. (Melbourne: Macmillan, 1949), p. 31.

[5] Rupert E. Billingham, Leslie Brent, and P.B. Medawar, “Actively acquired tolerance of foreign cells,” Nature 172 (1953): 603-6.

[6] J.C.G. Ledingham, The Carrier Problem in Infectious Diseases (London: Longmans, Green and Co., 1912).

[7] Victor E. Shelford, Animal Communities in Temperate America (Chicago: University of Chicago Press, 1913).

[8] Charles S. Elton, Animal Ecology (London: Sidgwick and Jackson, 1927).

[9] Alfred I. Tauber, “Review of Thomas Pradeu The Limits of the Self,” Notre Dame Philosophical Reviews http://ndpr.nd.edu/news/31627-the-limits-of-the-self-immunology-and-biological-identity. Accessed 25 September 2014. See also Tauber, “The immune system and its ecology,” Philosophy of Science 75 (2008): 224-45.

[10] Janelle S. Ayres and David S. Schneider, “Tolerance of infections,” Annual Review of Immunology 30 (2012): 271-94, pp. 271, 273.

[11] Scott F. Gilbert, Jan Sapp, and Alfred I. Tauber, “A symbiotic view of life: we have never been individuals,” Quarterly Review of Biology 87 (2012): 325-41, p. 326.

[12] Jacques Derrida, “Autoimmunity: real and symbolic suicides,” in Philosophy in a Time of Terror: Dialogues with Jürgen Habermas and Jacques Derrida, interviewed by Giovanna Borradori (Chicago: University of Chicago Press, 2003), p. 128.

[13] Roberto Esposito, Immunitas: The Protection and Negation of Life, trans. Zakiya Hanafi (Cambridge: Polity, 2011), pp. 166, 167.

[14] A. David Napier, The Age of Immunology: Conceiving a Future in an Alienating World (Chicago: University of Chicago Press, 2003), p. 253.

Image: “The Oil and Vinegar Nebula.” Flickr.


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