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Rethinking individuality: the dialectics of the holobiont

Abstract

Given immunity’s general role in the organism’s economy—both in terms of its internal environment as well as mediating its external relations—immune theory has expanded its traditional formulation of preserving individual autonomy to one that includes accounting for nutritional processes and symbiotic relationships that require immune tolerance. When such a full ecological alignment is adopted, the immune system becomes the mediator of both defensive and assimilative environmental intercourse, where a balance of immune rejection and tolerance governs the complex interactions of the organism’s ecological relationships. Accordingly, immunology, which historically had affiliated with the biology of individuals, now becomes a science concerned with the biology of communities. With this translocation, the ontological basis of the organism is undergoing a profound change. Indeed, the recent recognition of the ubiquity of symbiosis has challenged the traditional notions of biological individuality and requires a shift in the metaphysics undergirding biology, in which a philosophy of the organism must be characterized by ecological dialectics “all-the-way-down.”

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Notes

  1. 1.

    The cognitive metaphor is not a new development in immunology’s conceptual formulation. This cognitive orientation is seen in immunologists descriptions of macrophages “seeing” antigen, antibodies “recognizing” epitopes, T and B cells possessing “memory;” and adaptive immunity comprising a “learning” process (Tauber 1997). Indeed, at the level of cell communication, the immune system, neural system, and endocrine system coalesce to constitute an integrative sensory network for the body (Gilbert 2003; Ader 2006; Sotelo 2015). In ecological developmental biology (see below), this molecular sensing network is critical for integrating the developing organism with its biotic and abiotic environments as well as mediating competition within the organism (Nijhout and Emlen 1998; Bonett et al. 2010).

  2. 2.

    Much of this re-orientation revolves around understanding the mechanisms of immune tolerance that have allowed symbiotic relationships to take hold (a topic reviewed by Chiu and Eberl in this special issue).

  3. 3.

    For instance, Bacteroides the taiotomicron induces angiogenin-4 gene expression in mouse’s intestinal cells. This angiogenin-4 not only instructs the mouse’s gut mesenchyme to organize itself into capillaries; it also is bacteriocidal for Listeria and Enterococcus, two of the major competitors of Bacteroides as well as being human pathogens (Hooper et al. 2003; Cash et al. 2006).

  4. 4.

    To capture the complex intercourse between the human and non-human living world, Latour (1999) regards the ecosystem as a polity in which all constituents participate in a constant negotiation of belonging and elimination. To recognize shapes on the microbial surface, immunocompetent vertebrate cells alter their genomic DNA and become “diplomats” in the sense Latour describes, namely they ‘negotiate’ or mediate rejection or assimilation. “Diplomacy,” writes Stengers (2005 93), “is a technology of belonging,” which, especially in the case of the holobiont, determines who “we” are.

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Acknowledgments

SFG is funded by Swarthmore College and the National Science Foundation, and he wishes to thank Dr. Heather Davis and Sarah R. Gilbert for constructive conversations on these issues. We also thank the editor for his assistance in these revisions.

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Gilbert, S.F., Tauber, A.I. Rethinking individuality: the dialectics of the holobiont. Biol Philos 31, 839–853 (2016). https://doi.org/10.1007/s10539-016-9541-3

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Keywords

  • Immunity
  • Individuality
  • Holobiont
  • Organism
  • Symbiosis
  • Ecosystem